An overview of siderophores for iron 
acquisition in microorganisms living in the 
extreme
Authors: Luis O. De Serrano, Anne K. Camper, & 
Abigail M. Richards.
NOTICE: The final publication is available at Springer via http://dx.doi.org/10.1007/
s10534-016-9949-x. 
De Serrano LO, Camper AK, Richards AM “An overview of siderophores for iron acquisition in 
microorganisms living in the extreme,” Biometals,2016 Aug;29(4):551–71.
Made available through Montana State University’s ScholarWorks 
scholarworks.montana.edu 
An overview of siderophores for iron acquisition in 
microorganisms living in the extreme
Luis O. De Serrano . Anne K. Camper . Abigail M. Richards
L. O. De Serrano (&)  A. K. Camper
Department of Microbiology & Immunology, Montana State University, Bozeman, MT 59717, USA
A. K. Camper
Department of Civil & Environmental Engineering, Montana State University, Bozeman, MT 59717, USA
A. M. Richards
Department of Chemical & Biological Engineering, Montana State University, Bozeman, MT 59717, USA
L. O. De Serrano  A. K. Camper  A. M. Richards Center for Biofilm Engineering, Montana State University, Bozeman, MT 59717, USA
Abstract 
Siderophores are iron-chelating molecules produced by microbes when intracellular iron con-centrations 
are low. Low iron triggers a cascade of gene activation, allowing the cell to survive due to the synthesis 
of important proteins involved in side-rophore synthesis and transport. Generally, siderophores are 
classified by their functional groups as catecholates, hydroxamates and hydroxycarboxylates. Although 
other chemical structural modifications and functional groups can be found. The functional groups 
participate in the iron-chelating process when the ferri-siderophore complex is formed. Classified as 
acidophiles, alkaliphiles, halophiles, thermophiles, psychrophiles, piezophiles, extremophiles have par-
ticular iron requirements depending on the environ-mental conditions in where they grow. Most of the 
work done in siderophore production by extremo-philes is based in siderophore concentration and/or 
genomic studies determining the presence of side-rophore synthesis and transport genes. Siderophores 
produced by extremophiles are not well known and more work needs to be done to elucidate chemical 
structures and their role in microorganism survival and metal cycling in extreme environments.
Keywords
Iron acquisition  Siderophores  Siderophore synthesis and transport  Extremophiles
Introduction
Almost all microorganisms require iron for their cellular processes. Iron is involved in several pivotal 
cellular processes, including amino acid synthesis, oxygen transport, respiration, nitrogen fixation, 
methanogenesis, the citric acid cycle, photosynthesis and DNA biosynthesis. Iron concentrations in the 
extracellular environment are low (10-18 M) and limited by the insolubility of Fe (OH)3. Microorgan-
isms require micromolar concentrations of iron, but many environments, such surface ocean water, 
has concentrations ranging from 0.01 to 2 nM (Luther and Wu 1997). Iron can be present in its ferric 
(Fe+3) or ferrous (Fe+2) forms. The redox potential of the latter is suitable as a protein catalytic
center (Krewulak and Vogel 2008). For pathogenic microorganisms, iron
The outer membrane of gram-negative cells does
not have a proton motive force that will provide the
energy required for active transport, so that role is
performed by the TonB, ExbB and ExbD proteins. The
amino- and carboxy-terminal domains provide the
energy required to transport ferri-siderophores across
the outer membrane. The remaining proteins, ExbB
and ExbD, assist TonB in energy transduction.
In the periplasm there are periplasmic siderophore
binding proteins (PSBP) to transport ferric siderophores
across thecytoplasmicmembrane.Theword siderophore
is included in this term because there are about eight
different clusters of periplasmic binding proteins (Crosa
et al. 2004; Krewulak and Vogel 2008) that bind
oligosaccharides, sugars, phosphate, amino acids (polar
and non-polar), organic polyanions, peptides, iron com-
plexes and other metals. FhuD, FbpA and BtuF are the
most studied PSBPs and are associated with iron uptake
metabolism and transport. Specific group-coordinating
PSBPs will shuttle their corresponding siderophore
through the periplasm until the PSBP-siderophore-iron
complex reaches transporters on the cytoplasm.
The transporters are a class of ATP-binding cas-
settes (ABC transporter proteins). The best example
known today is the FhuBDC. The complex couples
ATP hydrolysis to transport the iron-siderophore
through the cytoplasmicmembrane into the cytoplasm.
FhuD is the PSBP for hydroxamate siderophores, and
well-studied due to its complete structure elucidation.
FhuB and FhuC are ABC transporter proteins. Due to
their transmembrane domains, FhuBC form channels
where the siderophore-iron complex passes through. It
also has two nucleotide binding domains that hydro-
lyze ATP. In brief, FhuD transfers the siderophore-iron
complex to FhuB, the complex is translocated to the
channel; in the meantime FhuC hydrolyses ATP.
Finally the siderophore-iron complex is dissociated
by an electron transfer to ferric iron (Fe?3), converting
it to ferrous iron (Fe?2).
Ferrous iron uptake
Themechanism of ferrous iron intake, contrary to ferric
iron acquisition, is not well understood. Ferrous iron
solubility is higher at neutral pH compared to ferric iron
and this facilitates transport across the membrane.
Ferrous iron concentration is higher under anaerobic or
reducing conditions. Two different systems for ferrous
availability is even lower due to mammalian host 
proteins (heme, lactoferrin, transferrin and ferritin) 
that sequester iron from the plasma (Krewulak and 
Vogel 2008). In overcome the scarcity of iron, many 
organisms have developed different mechanisms for 
iron capture: siderophores, hemophores, ferric binding 
proteins and transferrin/lactoferrin receptors (Sandy 
and Butler 2009). These molecules and proteins work 
together to increase the iron acquisition capabilities of 
the microbial cell. Siderophores are small molecules 
of approximately 500–1200 Da in size which specif-
ically bind ferric iron with high affinity, are excreted 
into the environment, thus increasing the bioavailabil-
ity of this otherwise insoluble nutrient.
The production of siderophores by disease causing 
microbes and many terrestrial microorganisms is well 
studied. The prevalence of siderophore production 
within extreme environments or by microbes classified 
as ‘‘extremophiles’’ is less so. This review will briefly 
summarize iron acquisition and siderophores pro-
duced by both terrestrial and pathogenic microbes. A 
discussion of the siderophores synthesized by extre-
mophiles (acidophiles, alkaliphiles, thermo/hyperther-
mophiles, psychrophiles, piezophiles etc.) or 
siderophores produced by microbes tolerant of 
extreme conditions (pH, salinity, temperature, pres-
sure) will follow.
Acquisition and transport of ferric iron 
siderophore-mediated iron acquisition
The active transport of ferric iron across the cell 
(Fig. 1; Crosa et al. 2004), is due to the use of porins 
for the high molecular weight ferric-siderophore 
complex, and requires different transport proteins 
and receptors. Outer membrane receptors are respon-
sible for of recognizing iron-bound siderophores 
outside the cell, and include FhuA, FecA and FepA 
found in Escherichia coli (Ferguson et al. 
1998, 2000, 2002, 2001; Yue et al. 2003), and BtuB, 
FpvA and FptA found in Pseudomonas aeruginosa 
(Cobessi et al. 2005a, b; Cornelis et al. 2009). Their 
structure is composed of b-barrel and cork domains,
(Krewulak and Vogel 2008) the former of which spans 
the membrane and helps to form a hollow space where 
the iron-sidrophore complex passes through to the 
periplasm, while the cork domain binds the iron-
siderophore complex and brings it into the b-barrel.
iron uptake have been described: Feo and Sit (Carpenter
and Payne 2014; Hantke 1987;Weaver et al. 2013). The
Feo and Sit operon systems, co-repressed by Fur and
iron (II), code for membrane-bound and cytoplasmic
proteins that participate in the active transport of ferrous
iron. Both ferrous uptake systems described are required
for pathogenicity (Boyer et al. 2002; Fisher et al. 2009;
Tsolis et al. 1996).
Regulatory characteristics of siderophore
production
Fur-mediated regulation of siderophore production
Bacteria utilize siderophores to obtain the ironnecessary
for their survival. However, iron is toxic and must be
tightly regulated within the cell. The most studied iron
regulation system is fur (for ferric uptake regulation)
(Hantke 2004; Lorenzo et al. 2004). Figure 2 presents a
general description of the regulatory system at high and
low iron concentration, inducing transcription of side-
rophore synthesis proteins and transportation into the
extracellular space for iron scavenging. At high iron
concentrations, the Fur protein undergoes conforma-
tional changes, attaches to the fur box to hinder the
transcription of siderophore genes. At low iron concen-
trations, no iron (II) is bounded to the Fur protein,
allowing the transcription of siderophore-related genes.
Siderophore regulation by quorum sensing
In addition to iron-dependent regulation, some bacteria
regulate siderophore production by means of quorum
sensing. Quorum sensing occurs in a cell density-
dependentmanner and helps regulate different functions
Fig. 1 Iron acquisition in a gram-negative bacterial cell. OM
outer membrane, CM cytoplasmic membrane, PSBP periplas-
mic siderophore binding protein, PBP periplasmic binding
protein. ABC transporter includes proteins ExbB and ExbD and
help in ATP hydrolysis to obtain energy for active transport.
Adapted from Krewulak and Vogel (2008)
enterobactins; hydroxamates, as in desferrioxamines;
and a-hydroxycarboxilates, as in achromobactins
(Fig. 3). These functional groups are donors of three
OO’ in order that six oxygen atoms coordinate the
ferric iron. Mixed functional group siderophores, such
as the siderophore aerobactin which contains two
hydroxamates and one hydroxycarboxilic acid group,
are also observed. A quintessential representative of a
catecholate siderophore is enterobactin (Fig. 4) and is
produced by E. coli and other enteric pathogens
(Gehring et al. 1997). Salmochelin is a glucosylated
form of enterobactin produced by Salmonella enterica
and uropathogenic E. coli (Bister et al. 2004).
The best known example of hydroxamate side-
rophores are the ferrioxamines (so-called desferriox-
amines when no ferric iron is coordinated). Their
structural composition is alternating units of succinic
Fig. 2 Siderophore-
mediated iron acquisition
system regulated by the Fur
protein. Adapted from Crosa
et al. (2004)
Fig. 3 Siderophore functional groups: catechols (a), hydroxa-
mates (b) and a-hydroxycarboxylates (c). Note the OO0 groups
provided by the hydroxyl and carbonyl moieties. Adapted from
Krewulak and Vogel (2008)
in the cell, triggering the corresponding phenotype 
response. Different physiological conditions are affected 
by quorum sensing, including: biofilm formation (Chris-
tiaen et al. 2014; Kadirvel et al. 2014), swarming 
motility (Vasavi et al. 2014), bioluminescence (Packi-
avathy et al. 2013), antibiotic production and resistance 
(Fineran et al. 2005), production of pharmaceuticals 
(Raina et al. 2012) and toxins (Tal-Gan et al. 2013).
Due to some contradictory findings, it is unclear how 
quorum sensing regulates siderophore synthesis, there-
fore more research efforts need to address this lack of 
information. Siderophore production is significantly 
impacted by quorum sensing in some bacteria, especially 
pathogens. Stintzi et al. (1998) described that lasR 
mutants were affected in siderophore production, specif-
ically pyoverdine in P. aeruginosa. Another siderophore 
produced by P. aeruginosa is pyochelin and it was not 
affected by the deficiency in the autoinducer production. 
In contrast, Burkholderia cepacia quorum sensing 
mutants tend to overproduce the siderophore ornibactin 
(Lewenza et al. 1999). Complementation restored side-
rophore production to original levels.
Siderophore coordination groups
Siderophore classification is based on certain func-
tional groups that are involved in ferric iron coordi-
nation. Those groups include catechols, as in
acid and monohydroxylated diamine, either N-hy-
droxycadaverine or N-hydroxyputrescine. Some des-
ferrioxamines are in cyclic form, such as
desferrioxamine E (Fig. 4) (Ejje et al. 2013;
Konetschny-Rapp et al. 1992), while others are linear,
such as desferrioxamines B (Fig. 4) (Ejje et al. 2013;
Martinez et al. 2001) and G (Bergeron et al. 1992; Ejje
et al. 2013). More recently, di- and tri-hydroxamic
acid siderophores (putrebactins, scabichelins and
turgichelins) have been characterized from She-
wanella putrefaciens, Streptomyces antibioticus,
Streptomyces scabies and Streptomyces turgidiscabies
(Kodani et al. 2013; Soe and Codd 2014).
Achromobactin is produced by Pseudomonas
syringae pv. syringae (Berti and Thomas 2009) and
is a tris-a-hydroxycarboxylate siderophore (Fig. 4). A
second siderophore that falls in this group is vibrio-
ferrin (Fig. 4), categorized as a bis-a-hydroxycarbox-
ilic siderophore (Amin et al. 2009; Harris et al. 2007).
Some siderophores use only citrate to coordinate ferric
iron (Fig. 4). Rhizoferrin’s two coordinating groups
are donated from two citrates as well as those from
staphyloferrin A (Fig. 4) (Cotton et al. 2009; Drechsel
et al. 1991; Harris et al. 2007; Meiwes et al. 1990).
There are many siderophores that contain mixed
coordinating functional groups. This group of side-
rophores is composed by bidentate ligand and also
amphiphilic siderophores. Examples are aerobactins,
amphibactins, ochrobactins, marinobactins, aquache-
lins, lystabactins, rhodobactins and amychelins among
others (Fig. 5; Dhungana et al. 2007; Neilands 1995;
Seyedsayamdost et al. 2011; Zane and Butler 2013).
Siderophores produced by extremophiles
Microorganisms living in extreme environmental con-
ditions (high acidities, alkalinities, temperatures, or
barometric pressures; the ability to grow in organic
solvents; or low temperatures) are known as
Fig. 4 Enterobactin (catechol, a), desferrioxamine E (cyclic
hydroxamate, b), achromobactin (hydroxycarboxylate, c),
vibrioferrin (hydroxycarboxylate, d), citrate (e),
desferrioxamine B (linear, hydroxamate, f) and staphyloferrin
A (hydroxycarboxylate, g) structures. Adapted from Sandy and
Butler (2009)
Scarce information is available for siderophore-
mediated iron acquisition in extremophiles (Ye et al.
2004) but some physiological groups (halophiles and
thermophiles) have more available structural infor-
mation than others (alkaliphiles, acidophiles, piezo-
philes and psychrophiles). Microbial Fe(III) reduction
has been described in diverse conditions, including
acidic (Kusel et al. 1999), alkaliphilic (McMillan et al.
2010; Ye et al. 2004), thermophilic (Liu et al. 1997;
Zhang et al. 2013; Zhou et al. 2001), psychrophilic
(Zhang et al. 1999) and halophilic (Emmerich et al.
2012; Handley and Lloyd 2013) environments.
Depending on the metabolic requirements and envi-
ronmental conditions, ferric iron could be an essential
micronutrient (although in extreme acidic conditions
ferrous, and not ferric, iron is available).
Siderophores produced by acidophiles
Iron bioavailability in acidic environments is high
when comparing to neutral pH environments. At such
environmental situations soluble ferric iron is at a
Fig. 5 Some mixed functional groups siderophores: lystabactins (a–c), aerobactin (d), rhodobactin (e) and amychelin (f). Adapted
from Sandy and Butler (2009), Seyedsayamdost et al. (2011) and Dhungana et al. (2007)
extremophiles. It is important to make the distinction 
between tolerant and extremophile microorganisms. 
Certain microbes isolated in non-extreme environments, 
can grow in specific extreme conditions [like high 
pressure, (Olsson-Francis et al. 2010) or high temper-
ature and in the presence of organic solvents (Tang et al. 
2009)], however surpassing their tolerance level could 
cause death of the microbe (Huidrom et al. 2011).
Microorganisms classified as acidophiles (living at 
pH \ 4), alkaliphiles (pH [ 8), thermophiles (from 
about 40 to 110 C), piezophiles (high barometric 
pressures) and psychrophiles (-20–10 C) depending 
on their extreme environment. Although these phys-
iological classifications exist, it is important to note 
that a species could have two or more physiological 
requirements (for example: halophile and ther-
mophile, alkaliphile and halophile, or piezophile and 
psychrophile). Extremophiles possess the required 
cellular machinery to survive such conditions (Calo 
et al. 2010; Doukyu and Ogino 2010; Eichler 2003; 
Georlette et al. 2003; Jarrell et al. 2011; Kogej et al. 
2006; Scandurra et al. 1998).
concentration of 0.1 M (at pH 2) (Quatrini et al. 2007).
In neutrophilic environments the ferric iron bioavail-
able concentration is at 10-18 M. Ferrous iron pre-
dominates in acidic conditions presenting risk for
cellular toxicity due to the production of radicals.
Therefore, acidic environments present two main
challenges to microorganisms living in such condi-
tions: (1) cellular iron homeostasis needs to be
maintained to avoid toxic levels and (2) iron utilized
as energy source and an important micronutrient for
optimal cellular metabolic functions (Quatrini et al.
2007) regulated.
Microbial iron oxidation for the production of
cellular energy tend to occurs frequently in acidic
environments and several studies described the dif-
ferent mechanisms of iron acquisition and manage-
ment of selected acidophiles (Bonnefoy and Holmes
2012). Osorio et al. took a bioinformatics approach for
the study of iron transport proteins in three acidithio-
bacilli (Osorio et al. 2008). It was found that
Acidithiobacillus ferrooxidans, Acidithiobacillus
thiooxidans and Acidithiobacillus caldus possess the
corresponding genetic information to oxidize ferrous
iron. The A. ferrooxidans Fur box regulator was
studied by another group of scientists and it was
determined to have the ability to complement Dfur
E.coli (Quatrini et al. 2005). Other bioinformatic
studies present valuable information regarding iron
homeostasis in Ferroplasma acidarmanus (Potrykus
et al. 2011). Genes responsible for iron metabolism
were up-regulated when F. acidarmanuswas grown in
iron poor conditions.
There is some genomic computational analysis
information available on siderophore-mediated iron
acquisition (Osorio et al. 2008; Potrykus et al. 2011).
A. ferrooxidans and A. thiooxidans have the genetic
capability for citrate (a siderophore) production, a
citrate efflux pump and a TonB-dependent Fe(III)-
dicitrate transport systems (Osorio et al. 2008).
Potrykus et al. (2011) determined that F. acidarmanus
carries a gene for siderophore synthesis and internal-
ization (ZP_05571308 and ZP_05571695, respec-
tively). However, the type of siderophore produced
by F. acidarmanus was not determined, leaving an
open question regarding the structure of the side-
rophore produced.
Phylogenetic and diversity studies have been per-
formed on acidic soil environments due to plant
growth-promotion capabilities of secondary
metabolite production of rhizobia. The studies focused
on siderophore production and other growth-promot-
ing metabolites produced by acidophilic rhizobacteria
like Bacillus, but no structural characterization of the
siderophore was performed (Yadav et al. 2011). In that
study, researchers found that most of the isolates
produced siderophores (31 out of 49 isolates). Similar
results were obtained by studies done by Karagoz et al.
(2012). The isolates were related to Pseudomonas
putida (7), P. fluorescens (2), Rhizobium radiobacter
(1), P. syringae (1) and Bacillus atrophaeus (1). An
earlier report by Verma et al. measured siderophore
production activity in acidic soil isolates related to P.
fluorescens (Verma et al. 2007). No structural studies
were carried on in order to characterize the
siderophore(s) produced by the isolates, but it is likely
that pyoverdine (produced by Pseudomonas species)
is a candidate (Kalinowski et al. 2006).
Siderophores produced by alkaliphiles
Alkaliphilic microorganisms are capable of growth
and reproduction at high pH environments, typically
[8. At such environmental conditions, iron exists in
its ferric form (Fe?3), reacting with oxygen to
produce Fe (OH)3 and reducing its bioavailability.
Alkaliphiles must overcome this physiological prob-
lem to survive, making siderophore-mediated iron
acquisition a critical physiological step (McMillan
et al. 2010; Sarethy et al. 2011). Several studies
have examined alkaliphiles isolated from different
environments that foster lower solubility and
bioavailability to determine their physiological
requirements (carbon and energy sources) and their
possible utilization of certain metals (Blum et al.
1998; Luque-Almagro et al. 2005a, b; Wood and
Kelly 1991; Ye et al. 2004).
Iron uptake by complexation with chelators has
been studied previously in alkaline, anaerobic condi-
tions (Ye et al. 2004). Additional strategies selected
alkaliphiles use to obtain iron employ the interaction
with cyanide (Luque-Almagro et al. 2005a, b, 2011).
In these reports, researchers described the physiolog-
ical characteristics of Pseudomonas pseudoalcalige-
nesCECT5344, especially its biodegradation potential
by the bacterial utilization of ferrocyanide. The
microorganism was able to synthesize siderophores
but no chemical characterizations were performed.
Other microorganisms, like Streptomyces, produce
respiratory inhibitors with iron-chelating properties
(Pick 2004). It was demonstrated in the report that the
iron-bound antimycin A was utilized by the halotol-
erant alga, Dunaniella salina, as a possible iron-
acquisition pathway. Although researchers do not
classify antimycin A as a siderophore, its chemical
structure resembles that of enterobactin (Fig. 6).
These reports demonstrate the capacity of microor-
ganisms to utilize xenosiderophores, or siderophores
produced by other microorganisms. In another study
by Gascoyne and co-workers, bacterial isolates were
obtained from different sample types including chalk
soils, cement work wastes, alkaline soils and soda
lakes (Gascoyne et al. 1991a, b). Researchers demon-
strated that isolates were capable of obtaining iron and
gallium by a siderophore-mediated mechanisms.
Assay-mediated structural characterization (Arnow
and Atkin assays) confirmed hydroxamic and cate-
cholic acids type siderophores.
The studies presented here demonstrate the capa-
bilities of alkaliphiles to thrive in low iron concentra-
tions and their evolutionary responses to such
environmental conditions that help them in their
survival. However information regarding specific
siderophore structures is scarce since most of the
studies only determine siderophore presence via the
chrome azurol sulfonate (CAS) assay. Future investi-
gations of siderophores isolation and microbial
ecology organisms in alkaline pH environments
should focus not only on siderophore detection, but
characterization, to better understand the specific
mechanisms of iron uptake.
Siderophores produced at high-temperatures:
thermophiles
High-temperature environments are widely spread on
Earth, from thermal hot springs in Yellowstone
National Park (Beam et al. 2014; Kozubal et al.
2013; Wu et al. 2013a) and Mexico (Brito et al. 2014),
to deep-sea vents (Kaye et al. 2011; Pettit 2011), mines
(Gounder et al. 2011) and volcanoes (Amaresan et al.
2014; Connell et al. 2009). A diverse population of
organisms are found, representing the three branches
of the tree of life: eukaryotes (Connell et al. 2009),
archaea (Beam et al. 2014; Hedlund et al. 2013;
Kozubal et al. 2013) and bacteria (Kaye et al. 2011;
Temirov et al. 2003). New organisms and even phyla
are being discovered, and their physiological charac-
teristics determined, in such environmental conditions
(Beam et al. 2014; Kozubal et al. 2013). For example,
one possible mechanism for iron reduction in high-
temperature is explained by methanogenic bacteria. In
brief, ferric iron reduction decrease the reduction
potential of the system allowing methanogenesis
(which in return helps the methanogen to grow and
Fig. 6 Enterobactin and antimycin A chemical structures
in turn enhance ferric iron reduction) (Zhang et al.
2013).
Thermophiles are producers of a plethora of
secondary metabolites like siderophores that could
be key players for drug developments including
antibiotics, antifungals, antibacterials and anticancer
drugs (Pettit 2011), but little information about
siderophore production and structural characterization
is available (Temirov et al. 2003). Iron transport
systems have been characterized in few thermophilic
bacteria (Guerry et al. 1997). In some cases side-
rophore production assays are performed to charac-
terize the isolates obtained, but no structural
elucidation is attained (Sudek et al. 2009). The more
common, siderophore-producing species present were
Pseudomonas and Pseudoalteromonas, representing
more than half of isolated microorganisms (41 and
26 %, respectively). The microorganisms withstood
fluid temperatures up to 81 C in basalt rock and iron
mat samples in situ. Further in vitro studies of
siderophore and metal chelation from volcanic rocks
revealed the transfer of the iron and other metals from
the rock matrix to the aqueous phase of glacial
meltwater, increasing iron bioavailability (Bau et al.
2013). Therefore, it is not surprise to find metal
oxidizing bacteria with siderophore-producing bacte-
ria, creating a community where mutualism is the key
for survival.
To the best of our knowledge, there are three reports
that present the structural characterization of side-
rophores produced by thermophilic species. Machuca
and co-workers purified and partially characterized a
low-molecular mass component (530 Da) from the
fungus Thermoascus aurantiacus grown at 48 C and
low-pH conditions (Machuca et al. 1999). X-ray
fluorescence determined the presence of iron, calcium
and magnesium in the purified metabolite samples,
indicating potential metal chelation (main character-
istic of siderophores). The following study investi-
gated the siderophore production of the
thermoresistant bacterium B. licheniformis VK21
(Temirov et al. 2003). The purified compound, SVK21
(Fig. 7), was analyzed with NMR spectroscopy and its
structure was determined to be 2,3-dihydroxybenzoyl-
glycyl-threonine, which after comparison with bacil-
libactin, it was suggested to be a fragment of the latter.
The final study elucidated the structure and
Fig. 7 SVK21 siderophore produced by B. licheniformis VK21
Fig. 8 Fuscachelins
produced by the thermophile
T. fusca
in previous reports discussed here, no structural
characterizations were made. However, siderophore
producers were related to Bacillus, Sanguibacter,
Arthrobacter and other species for which siderophore
structures are known (e.g., bacillibactin, sanguibactin,
pyoverdine and pyochelin).
Studies of single species siderophore production
are found in literature. One report characterized a
bacterium, Pseudomonas sp. PGERs17 (MTCC 9000),
isolated from the northern Indian Himalayas (Mishra
et al. 2008). Siderophore production was confirmed by
CAS assay at as low as 4 C, but higher siderophore
production values were recorded at room temperature.
No structural characterization of the siderophores
produced was achieved, suggesting only pyoverdines
and pyochelins as potential siderophore candidates in
this microorganism. Ren et al. studied the bacterium
Bacillus sp. PZ-1 (Ren et al. 2015). Siderophore
production was confirmed but no structural character-
ization studies were performed.
The lack of information regarding structure of
siderophores may be due to the difficulty to grow
psychrophilic microorganisms. But the presence of
iron acquisition systems and confirmation of side-
rophore production genes must be the motivation to
engage in such studies to increase important scientific
knowledge.
Siderophores produced by halophiles
The halophilic environments are those found in the
oceans, salterns, desserts and soda (hypersaline) lakes
and the microbial richness and diversity that thrives in
them has been described (Bamforth 1984; Crognale
et al. 2013; Emmerich et al. 2012; Ghozlan and Deif
2006; Pandit et al. 2015; Sunagawa et al. 2015).
Halophilic microorganisms were found in the rhizo-
sphere of halotolerant plants. Some bacterial species
are unable to produce siderophores (Tipre et al. 2015)
but others are capable of such mechanism (Sahay et al.
2012). In the latter report, researchers found that 21 %
of the hypersaline-lake isolated bacteria produce
siderophores. No structural characterizations were
made to elucidate the chemical structure of those
siderophores produced. After 16S rRNA gene
sequencing, the siderophore-producing microorgan-
isms were related to bacterial species of which some
siderophore structures are known (bacillibactin, mari-
nobactins, amphibactins, sodachelins and halochelins)
biosynthesis of fuscachelins (Fig. 8), produced by the 
moderate thermophile Thermobifida fusca, (Dimise 
et al. 2008). These few studies show that there is still 
more to investigate to unveil the relationship between 
secondary metabolites and important biogeochemical 
processes.
Siderophores produced by psychrophilic 
microorganisms
Low-temperature environments represent one of the 
most hostile living conditions. For some time they 
were thought to be inhabitable (Horowitz et al. 1972). 
An example of such extreme environmental condi-
tions (average temperature of -22 C and winter 
temperatures as low as -60 C) is the McMurdo Dry 
Valleys in Antarctica (Friedmann et al. 1987; Fried-
mann and Ocampo 1976; Siebert et al. 1996). In spite 
of the hostile conditions, living organisms’ presence 
was confirmed and it was demonstrated that they 
thrived in those environments (Friedmann and 
Ocampo 1976). Even the production of siderophores 
was described in such environment (Siebert et al. 
1996) suggesting the presence of iron acquisition 
systems. Iron acquisition studies have been done on 
psychrophilic microorganisms (e.g., Oleispira antarc-
tica) based on genome sequencing (Kube et al. 2013). 
Siderophore biosynthesis genes were also described in 
the microorganism and the genes were expressed 
during iron-limiting conditions. No structural charac-
terization of the particular siderophore was done.
Bioprospecting studies have been done in low-
temperature environments with the aim of isolating 
plant growth-promoting bacteria (Balcazar et al. 2015; 
Yadav et al. 2015a). In those studies siderophore 
production experiments were performed but no struc-
tural characterizations were done. Since isolates were 
related to Pseudomonas sp., and other species mem-
bers of siderophore-producing phyla (Actinobacteria, 
Firmicutes, b-Proteobacteria and c-Proteobacteria), 
this suggest that these microorganisms could produce 
pyoverdines, pyochelins, bacillibactins, yersini-
abactins and aerobactins.
Another study presented the results for diversity 
and functional annotation of psychrotrophic bacteria 
(Yadav et al. 2015b). The samples were obtained from 
soil and water from a cold desert and generated 325 
bacterial isolates. Siderophore producers were identi-
fied by the typical CAS assay revealing 29 strains. As
(Figueroa et al. 2015; Gledhill et al. 2004; Martinez
and Butler 2007; Richards et al. 2006, 2007; Woo and
Kim 2008). Other siderophore-producing microorgan-
isms have been isolated from marsh water and soil
samples but they failed to determine structure of
siderophores (Malviya et al. 2014) or the presence of
siderophore-mediated iron reduction (Rossello-Mora
et al. 1995). Several published studies isolated side-
rophore producers from soda, or hypersaline, lakes
(Figueroa et al. 2015, 2012; Ramadoss et al. 2013;
Richards et al. 2006, 2007; Serrano Figueroa 2015).
Chemical structure characterizations were performed
by mass spectrometry and fatty acid methyl ester, and
siderophores were classified as amphiphilic side-
rophores: sodachelins and halochelins (Fig. 9). Rama-
doss and co-workers found that a total of three isolates
(SL3, SL32 and PU62), out of 84, from different
hypersaline lakes of India produced siderophores. No
chemical structure studies were done but phylogenetic
analysis determined that SL3 was related to
Halobacillus; SL32 to Bacillus pumilus; and PU62
to Bacillus halodenitrificans. Known siderophore
production studies have been done on Halobacillus
species to the best of our knowledge, however Bacillus
species produce bacillibactin and we could infer that
SL32 and PU62 may produce this siderophore.
Additional reports described studies done for side-
rophore production with desert-isolated Kocuria tur-
fanensis 2M4 and Bacillus licheniformis A2 bacteria
(Goswami et al. 2014a, b) but in both reports no
structural characterization was presented. Therefore,
we suggest bacillibactin as the siderophore produced
Fig. 9 Halochelins (a, b) and sodachelins (c) produced by Halomonas sp. SL01 (a, b) and SL28 (c)
by B. licheniformis A2 but further confirmation is
needed. A more recent study confirmed the production
of siderophores by another desert-isolated bacterium,
B. cereus brm, however no chemical characterizations
were performed (Vishal and Manuel 2015).
Iron acquisition studies have linked siderophores to
proper and optimal cell development of halophiles
(Anderson et al. 2011; Buyer et al. 1991; Hopkinson
and Morel 2009; Wilhelm et al. 1998). Every year
halophilic, siderophore-producing microorganisms
are characterized by different research groups. Most
of the siderophores produced by halophiles are
classified as amphiphiles, meaning that the same
molecule will have polar and non-polar properties.
The polar headgroup is the iron binding site and it is
attached to one or two of a series of fatty acids
(Gauglitz et al. 2012; Ito and Butler 2005; Martin et al.
2006; Martinez et al. 2003, 2000; Owen et al. 2005).
Figure 10 shows selected amphiphilic siderophore
structures presenting the structural feature of a-
hydroxycarboxylic acid moiety, usually in the form
of b-hydroxyaspartic acid or citric acid, conferring
photochemical reactivity to the molecule as demon-
strated previously (Barbeau et al. 2003, 2002; Butler
et al. 2001; Butler and Theisen 2010).
As observed from the review in siderophore-
producing halophiles there is considerable information
available about marine amphiphilic siderophores.
However, little information is published regarding
soda, hypersaline lakes and deserts. It is important to
ensure the studies of these environments and look for
secondary metabolite production, specifically side-
rophore production, and their relationship to iron
acquisition and biogeochemical pathways.
Fig. 10 Suites of marine amphiphilic siderophores structures characterized: marinobactins (a), aquachelins (b), amphibactins (c), 
loihichelins (d), moanachelins (e) and synechobactins (f). Adapted from Sandy and Butler (2009)
Siderophores produced by piezophiles
Piezophilic microorganisms (previously known as
barophiles) grow and reproduce under high hydro-
static, or barometric, pressures ([1100 atm) (Deming
and Colwell 1981). Typically that level of pressuriza-
tion can be found in deep-sea environments (due to the
pressure of the water column), under the basaltic sea
floor (caused by both the water column and Earth’s
crust weight) and underground (subsurface) environ-
ments. In addition to hydrostatic pressure, most of the
temperatures are below 4 C, and up to 400 C nearby
hydrothermal vents presenting a double challenge for
microorganisms living in such conditions. It was
thought by most scientists that life could not withstand
the conditions present in these environments until
independent studies by Certes and Regnard in 1884
stated the contrary. Posterior studies presented the
evidence of life at depths greater than 10,000 m under
sea level (Zobell and Morita 1957). Organisms living
under the influence of high pressures evolved mem-
branes with modified fatty acyl moieties in the
phospholipids, making the membrane more fluid
(Abe 2013). During the early times of deep-sea studies
(piezobiology), a main objective was always present in
the experimental design: to keep high hydrostatic
pressures when sampling deep-sea water and sedi-
ments, avoiding decompression that may kill obligate
piezophiles. Nowadays scientists have developed
modern sampling systems that solve the decompres-
sion problem (Fang et al. 2010). With the assistance of
robots and submarines sediments can be sampled and
novel piezophilic species isolated to lead to an
understanding of nutritional and physical require-
ments for their optimal cellular function (Bale et al.
1997; Nogi et al. 1998). In addition, with modern
molecular biology techniques in non-cultivable
approaches can be used to describe the microbial
population living under the influence of high pressures
(Fleming et al. 2013; Jorgensen et al. 2013;Wang et al.
2008).
Siderophore production and iron reduction are
closely linked in microorganisms (Adams et al.
1992) by the effects of some physical and physico-
chemical conditions in the latter. Nutrient availability
could also exert an effect on the viable cell count of
these microorganisms (Wirsen and Molyneaux 1999).
Microbial iron reduction and oxidation processes have
been described in the literature. Model simulations
proved that increasing the hydrostatic pressure on
organisms causes a decrease of the energy yield of
cellular reactions like oxygen reduction (Fang et al.
2010). In contrast, ferric iron reduction free energy
increases as the pressure increases. Several studies
have demonstrated that microorganisms belonging to
the domains Bacteria and Archaea possess the
required genetic machinery (Fleming et al. 2013;
Jorgensen et al. 2013; Wang et al. 2008) and other
investigations presented in vitro evidence of microbial
iron reduction and oxidation (Picard et al. 2014; Wu
et al. 2013b). Wang and co-workers isolated an iron-
reducing bacterium, Shewanella piezotolerans WP3
and determined by its genome sequencing the pres-
ence of mtr-omc gene cluster involved in metal
reduction in most Shewanella species. The group of
Jorgensen and co-workers discovered that members of
the deep sea archaeal group constitute up to 50 % of
the microbial population in certain sediment horizons.
Also that group of investigators determined that there
were significant variations in iron oxide and dissolved
iron levels, implying redox reactions occurring in the
microscopic community.
Not much information is available regarding side-
rophore-mediated iron acquisition and it is limited to
simple, but significant, siderophore production exper-
iments. The first evidence of potential siderophore
production by genome analysis of the deep-sea
bacterium, Pseudomonas sp. 10B238, confirmed the
presence of non-ribosomal peptide synthetases genes
(Pan and Hu 2015). Additional genome studies have
confirmed heterologous expression of hydrothermal
deep-sea metagenomic DNA in E. coli, producing the
siderophore avaroferrin (Fig. 11) and putrebactin
(Fujita and Sakai 2014). The only direct siderophore
isolation and structure identification was reported
from the deep-sea microorganism Streptomyces oli-
vaceus FXJ8.012 which produces tetroazolemycins A
and B (Fig. 11; Liu et al. 2013).
In another study, arsenic-rich groundwater samples
demonstrated the presence of siderophore-producing
microorganisms (Sarkar et al. 2013). Siderophore
structural studies were not done in this study but we
can infer that ochrobactins (Martin et al. 2006) and
alcaligin (Li et al. 2013) may be the ones produced
since bacterial species corresponding to these side-
rophores were isolated and identified through 16S
rRNA analysis. Since scarce siderophore structures
were directly linked to siderophore production, there is
the hydrophilic lohichelins (Homann et al. 2009). This
affects their extraction: amphibactins, moanachelins
and ochrobactins are mainly obtained from cell pellet
extracts, contrasting to the supernatant extracts that
contain loihichelins. Marinobactins have been the
most studied of the amphiphilic siderophores and have
different degrees of hydrophobicity and hydrophilicity
(Martinez and Butler 2007; Xu et al. 2002). Membrane
partitioning studies were also done with ochrobactins
giving similar results to those of the marinobactins
(Martin et al. 2006). Aquachelins are quite hydrophilic
especially aquachelins I and J isolated from Halomo-
nas meridiana (Vraspir et al. 2011). Synechococcus
sp. produces synechobactins (Fig. 10) which are
related to the siderophore schizokinen (Ito and Butler
2005). Other siderophores can be taken up by another
type of microorganism and then undergo changes in
their structure. In Vibrio harveyi, enterobactin
Fig. 11 Additional
siderophores produced by
piezophilic microbes:
avaroferrin (a),
tetroazolemycin A (b) and
tetroazolemycin B (c)
a need to elucidate novel siderophore from piezophilic 
isolates. In this manner we may be able to link iron 
reduction and acquisition in these microorganisms 
with their siderophore production, and understand 
their role in deep-ocean and sediment biogeochemical 
processes.
Concluding remarks
Observing Fig. 10, we can conclude there might be 
certain levels of hydrophilicity or hydrophobicity in 
amphiphilic siderophores due to some molecular 
characteristics (length of fatty acyl moieties and 
headgroup). A clear example of this is the hydropho-
bicity of amphibactins (Gledhill et al. 2004; Vraspir 
et al. 2011), moanachelins (Gauglitz and Butler 2013) 
and ochrobactins (Gauglitz et al. 2012) contrasting to
undergoes a chemical modification (addition of fatty
acids moieties with different levels of saturation and
hydroxylation) to transform it into an amphi-enter-
obactin (Zane et al. 2014). The relevance of amphi-
philic siderophores chemical characteristics determine
their extraction process, important in the study of new
family members.
Another property of amphiphilic siderophores is the
capacity of the molecules to self-assemble in micelles
and vesicles upon iron coordination (Bednarova et al.
2008; Luo et al. 2002;Martinez et al. 2000; Owen et al.
2007, 2005, 2008). The science behind this phe-
nomenon is based on the critical micelle concentration
(cmc) of the amphiphile molecule. When the concen-
tration of the amphiphilic siderophore is over the cmc
and the siderophore is not bound to iron, micelle
formation occurs. Adding ferric iron (*1 Eq.) to the
solution causes micelle size reduction, but if the iron
concentration increases ([1 Eq.) a micelle-to-vesicle
transition happens (Owen et al. 2005). A brief
description of this process appears in Fig. 12.
Iron is ubiquitous in the environment and required
by most living organisms. It is not bioavailable due to
its poor solubility in water, but microorganisms have
developed iron acquisition systems to overcome this
problem. These acquisition systems help regulate a
balanced iron concentration across the cell. Side-
rophore production and respective receptors and
transport proteins are part of that system and help
obtain iron from the extracellular environment in iron-
limiting conditions. In general, three different func-
tional groups (hydroxamates, catacholates and
hydroxycarboxylates) are found in the siderophore
molecule and assist in ferric iron coordination.
Different structures are found in diverse environments
including extreme environments. Extremophiles
evolved to overcome the hostile conditions in such
environments ensuring their survival and have devel-
oped mechanisms for iron acquisition. The physiolog-
ical requirements for extremophiles are so complex
and interweaved that a single extremophilic species
could possess characteristics from two or more
physiological groups (e.g., thermoacidophilic bacte-
ria, haloalkaliphilic archaea etc.). Halophiles synthe-
size a variety of siderophores and some information is
available regarding their structural composition.
These structures contrast with the siderophore pro-
duction and structural characterization studies from
other physiological requirements groups (like piezo-
philes and acidophiles). Siderophores help maintain
the equilibrium of iron in extreme environments
providing physiological niches for extremophiles.
More studies on extremophiles and siderophore
production should be performed along characteriza-
tion studies to elucidate siderophore chemical
structures.
Acknowledgments Special thanks for the co-authors, Drs.
Abigail M. Richards and Anne K. Camper, for their thoughtful
insight and review of the manuscript. Thank you to members of
the Camper Laboratory and graduate students and staff from the
Center for Biofilm Engineering, Montana State University,
Bozeman, USA.
Compliance with ethical standards
Conflict of Interest The authors declare that they have no
conflict of interest.
Fig. 12 Micelle and vesicle
formation on amphiphilic
siderophores due to critical
micelle concentration (cmc)
and ferric iron chelation
References
Abe F (2013) Dynamic structural changes in microbial mem-
branes in response to high hydrostatic pressure analyzed
using time-resolved fluorescence anisotropy measurement.
Biophys Chem 183:3–8. doi:10.1016/j.bpc.2013.05.005
Adams JB, Palmer F, Staley JT (1992) Rock weathering in
deserts—mobilization and concentration of ferric iron by
microorganisms. Geomicrobiol J 10:99–114
Amaresan N, Kumar K, Sureshbabu K, Madhuri K (2014) Plant
growth-promoting potential of bacteria isolated from
active volcano sites of Barren Island, India. Lett Appl
Microbiol 58:130–137. doi:10.1111/lam.12165
Amin S, Green D, Kupper F, Carrano C (2009) Vibrioferrin, an
unusual marine siderophore: iron binding, photochemistry,
and biological implications. Inorg Chem 48:11451–11458.
doi:10.1021/ic9016883
Anderson I et al (2011) Novel insights into the diversity of
catabolic metabolism from ten haloarchaeal genomes. Plos
One 6:12. doi:10.1371/journal.pone.0020237
Balcazar W, Rondon J, Rengifo M, Ball MM, Melfo A, Gomez
W, Yarzabal LA (2015) Bioprospecting glacial ice for
plant growth promoting bacteria. Microbiol Res 177:1–7.
doi:10.1016/j.micres.2015.05.001
Bale SJ, Goodman K, Rochelle PA, Marchesi JR, Fry JC,
Weightman AJ, Parkes RJ (1997) Desulfovibrio profundus
sp nov, a novel barophilic sulfate-reducing bacterium from
deep sediment layers in the Japan Sea. Int J Syst Bacteriol
47:515–521
Bamforth SS (1984) Microbial distributions in Arizona Deserts
and Woodlands. Soil Biol Biochem 16:133–137. doi:10.
1016/0038-0717(84)90103-2
Barbeau K, Zhang GP, Live DH, Butler A (2002) Petrobactin, a
photoreactive siderophore produced by the oil-degrading
marine bacterium marinobacter hydrocarbonoclasticus.
J Am Chem Soc 124:378–379. doi:10.1021/ja0119088
Barbeau K, Rue EL, Trick CG, Bruland KT, Butler A (2003)
Photochemical reactivity of siderophores produced by
marine heterotrophic bacteria and cyanobacteria based on
characteristic Fe(III) binding groups. Limnol Oceanogr
48:1069–1078
Bau M, Tepe N, Mohwinkel D (2013) Siderophore-promoted
transfer of rare earth elements and iron from volcanic ash
into glacial meltwater, river and ocean water Earth Plane-
tary. Sci Lett 364:30–36. doi:10.1016/j.epsl.2013.01.002
Beam JP, Jay ZJ, Kozubal MA, Inskeep WP (2014) Niche
specialization of novel Thaumarchaeota to oxic and
hypoxic acidic geothermal springs of Yellowstone
National Park. ISME J 8:938–951. doi:10.1038/ismej.
2013.193
Bednarova L, Brandel J, d’Hardemare A, Bednar J, Serratrice G,
Pierre J (2008) Vesicles to concentrate iron in low-iron
media: an attempt to mimic marine siderophores. Chem-A
Eur J 14:3680–3686. doi:10.1002/chem.200701644
Bergeron RJ, Liu ZR, McManis JS, Wiegand J (1992) Structural
alterations in desferrioxamine compatible with iron clear-
ance in animals. J Med Chem 35:4739–4744. doi:10.1021/
jm00103a012
Berti AD, Thomas MG (2009) Analysis of achromobactin
biosynthesis by pseudomonas syringae pv. syringae B728a.
J Bacteriol 191:4594–4604. doi:10.1128/jb.00457-09
Bister B, Bischoff D, Nicholson GJ, Valdebenito M, Schneider
K, Winkelmann G, Hantke K, Sussmuth RD (2004) The
structure of salmochelins: C-glucosylated enterobactins of
Salmonella enterica. Biometals 17:471–481. doi:10.1023/
B:BIOM.0000029432.69418.6a
Blum JS, Bindi AB, Buzzelli J, Stolz JF, Oremland RS (1998)
Bacillus arsenicoselenatis, sp nov, and Bacillus selenitire-
ducens, sp nov: two haloalkaliphiles from Mono Lake,
California that respire oxyanions of selenium and arsenic.
Arch Microbiol 171:19–30
Bonnefoy V, Holmes D (2012) Genomic insights into microbial
iron oxidation and iron uptake strategies in extremely
acidic environments. Environ Microbiol 14:1597–1611.
doi:10.1111/j.1462-2920.2011.02626.x
Boyer E, Bergevin I, Malo D, Gros P, Cellier MFM (2002)
Acquisition of Mn(II) in addition to Fe(II) is required for
full virulence of Salmonella enterica serovar Typhimur-
ium. Infect Immun 70:6032–6042. doi:10.1128/iai.70.11.
6032-6042.2002
Brito EMS et al (2014) Microbial diversity in Los Azufres
geothermal field (Michoacan, Mexico) and isolation of
representative sulfate and sulfur reducers. Extremophiles
18:385–398. doi:10.1007/s00792-013-0624-7
Butler A, Theisen RM (2010) Iron (III)-siderophore coordina-
tion chemistry: reactivity of marine siderophores. Coordin
Chem Rev 254:288–296. doi:10.1016/j.ccr.2009.09.010
Butler A, Martinez J, Barbeau K (2001) Reactivity of new self-
assembling amphiphilic siderophores and alpha-hydroxy
acid-containing siderophores from oceanic bacteria.
J Inorg Biochem 86:30
Buyer JS, Delorenzo V, Neilands JB (1991) Production of the
siderophore aerobactin by a halophilic pseudomonad. Appl
Environ Microbiol 57:2246–2250
Calo D, Kaminski L, Eichler J (2010) Protein glycosylation in
Archaea: Sweet and extreme. Glycobiology
20:1065–1076. doi:10.1093/glycob/cwq055
Carpenter C, Payne SM (2014) Regulation of iron transport
systems in enterobacteriaceae in response to oxygen and
iron availability. J Inorg Biochem 133:110–117. doi:10.
1016/j.jinorgbio.2014.01.007
Christiaen SEA, Matthijs N, Zhang X-H, Nelis HJ, Bossier P,
Coenye T (2014) Bacteria that inhibit quorum sensing
decrease biofilm formation and virulence in Pseudomonas
aeruginosa PAO1. Path Dis 70:271–279. doi:10.1111/
2049-632x.12124
Cobessi D, Celia H, Pattus F (2005a) Crystal structure at high
resolution of ferric-pyochelin and its membrane receptor
FptA from Pseudomonas aeruginosa. J Mol Biol
352:893–904. doi:10.1016/j.jmb.2005.08.004
Cobessi D, Celia H, Wirth C, Schalk I, Pattus F (2005b)
Structures of iron-siderophore outer membrane receptors
from P. aeruginosa. Eur Biophys J 34:642
Connell L, Barrett A, Templeton A, Staudigel H (2009) Fungal
diversity associated with an active deep sea volcano: vai-
lulu’u seamount, samoa. Geomicrobiol J 26:597–605.
doi:10.1080/01490450903316174
Cornelis P, Matthijs S, Van Oeffelen L (2009) Iron uptake
regulation in Pseudomonas aeruginosa. Biometals
22:15–22. doi:10.1007/s10534-008-9193-0
Cotton JL, Tao J, Balibar CJ (2009) Identification and charac-
terization of the staphylococcus aureus gene cluster coding
for staphyloferrin A. Biochem 48:1025–1035. doi:10.1021/
bi801844c
Crognale S, Mathe I, Cardone V, Stazi SR, Raduly B (2013)
Halobacterial community analysis of Mierlei Saline Lake
in Transylvania (Romania). Geomicrobiol J 30:801–812.
doi:10.1080/01490451.2013.774073
Crosa JH, Mey AR, Payne SM (2004) Iron transport in bacteria,
1st edn. ASM Press, Washington, DC
Deming JW, Colwell RR (1981) Barophilic Bacteria Associated
with Deep-Sea Animals. Bioscience 31:507–511. doi:10.
2307/1308493
Dhungana S et al (2007) Purification and characterization of
rhodobactin: a mixed ligand siderophore from Rhodococ-
cus rhodochrous strain OFS. Biometals 20:853–867.
doi:10.1007/s10534-006-9079-y
Dimise EJ, Widboom PF, Bruner SD (2008) Structure elucida-
tion and biosynthesis of fuscachelins peptide siderophores
from the moderate thermophile Thermobifida fusca. Proc
Natl Acad Sci USA 105:15311–15316. doi:10.1073/pnas.
0805451105
Doukyu N, Ogino H (2010) Organic solvent-tolerant enzymes.
Biochem Eng J 48:270–282. doi:10.1016/j.bej.2009.09.
009
Drechsel H, Metzger J, Freund S, Jung G, Boelaert JR,
Winkelmann G (1991) Rhizoferrin—a novel siderophore
from the fungus rhizopus-microsporus var rhizopodi-
formis. Biol Met 4:238–243. doi:10.1007/bf01141187
Eichler J (2003) Facing extremes: archaeal surface-layer (glyco)
proteins. Microbiol 149:3347–3351. doi:10.1099/mic.0.
26591-0
Ejje N, Soe CZ, Gu J, Codd R (2013) The variable hydroxamic
acid siderophore metabolome of the marine actinomycete
Salinispora tropica CNB-440. Metallomics 5:1519–1528.
doi:10.1039/c3mt00230f
Emmerich M, Bhansali A, Loesekann-Behrens T, Schroeder C,
Kappler A, Behrens S (2012) Abundance, distribution, and
activity of Fe(II)-oxidizing and Fe(iii)-reducing microor-
ganisms in hypersaline sediments of Lake Kasin, Southern
Russia. Appl Environ Microbiol 78:4386–4399. doi:10.
1128/aem.07637-11
Fang J, Zhang L, Bazylinski DA (2010) Deep-sea piezosphere
and piezophiles: geomicrobiology and biogeochemistry.
Trends Microbiol 18:413–422. doi:10.1016/j.tim.2010.06.
006
Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W
(1998) Siderophore-mediated iron transport: crystal struc-
ture of FhuA with bound lipopolysaccharide. Science
282:2215–2220. doi:10.1126/science.282.5397.2215
Ferguson AD, Braun V, Fiedler HP, Coulton JW, Diederichs K,
Welte W (2000) Crystal structure of the antibiotic albo-
mycin in complex with the outer membrane transporter
FhuA. Protein Sci 9:956–963
Ferguson AD et al (2001) Active transport of an antibiotic rifa-
mycin derivative by the outer-membrane protein FhuA.
Structure 9:707–716. doi:10.1016/s0969-2126(01)00631-1
Ferguson AD, Chakraborty R, Smith BS, Esser L, van der Helm
D, Deisenhofer J (2002) Structural basis of gating by the
outer membrane transporter FecA. Science 295:1715–1719.
doi:10.1126/science.1067313
Figueroa LOS, Schwarz BH, Richards AM (2012) Characteri-
zation of New Siderophores Produced by a Soda Lake
Isolate. Abstr Gen Meet Amer Soc Microbiol 112:404
Figueroa LOS, Schwarz B, Richards AM (2015) Structural
characterization of amphiphilic siderophores produced by
a soda lake isolate, Halomonas sp SL01, reveals cysteine-,
phenylalanine- and proline-containing head groups.
Extremophiles 19:1183–1192. doi:10.1007/s00792-015-
0790-x
Fineran PC, Slater H, Everson L, Hughes K, Salmond GPC
(2005) Biosynthesis of tripyrrole and beta-lactam sec-
ondary metabolites in Serratia: integration of quorum
sensing with multiple new regulatory components in the
control of prodigiosin and carbapenem antibiotic produc-
tion. Mol Microbiol 56:1495–1517. doi:10.1111/j.1365-
2958.2005.04660.x
Fisher CR, Davies NMLL, Wyckoff EE, Feng Z, Oaks EV,
Payne SM (2009) Genetics and virulence association of the
shigella flexneri sit iron transport system. Infect Immun
77:1992–1999. doi:10.1128/iai.00064-09
Fleming EJ, Davis RE, McAllister SM, Chan CS, Moyer CL,
Tebo BM, Emerson D (2013) Hidden in plain sight: dis-
covery of sheath-forming, iron-oxidizing Zetaproteobac-
teria at Loihi Seamount, Hawaii, USA. FEMS Microbiol
Ecol 85:116–127. doi:10.1111/1574-6941.12104
Friedmann EI, Ocampo R (1976) Endolithic blue-green-algae in
dry valleys—primary producers in Antarctic desert
ecosystem. Science 193:1247–1249. doi:10.1126/science.
193.4259.1247
FriedmannEI,McKayCP,NienowJA(1987)The cryptoendolithic
microbial environment in the Ross Desert of Antarctica—
satellite-transmitted continuos nanoclimate data, 1984 to
1986. Polar Biol 7:273–287. doi:10.1007/bf00443945
Fujita MJ, Sakai R (2014) Production of avaroferrin and
putrebactin by heterologous expression of a deep-sea
metagenomic DNA. Mar Drugs 12:4799–4809. doi:10.
3390/md12094799
Gascoyne DJ, Connor JA, Bull AT (1991a) Capacity of side-
rophore—producing alkalophilic bacteria to accumulate
iron, gallium and aluminum. Appl Microbiol Biotechnol
36:136–141
Gascoyne DJ, Connor JA, Bull AT (1991b) Isolation of bacteria
producing siderophores under alkaline conditions. Appl
Microbiol Biotechnol 36:130–135
Gauglitz J, Butler A (2013) Amino acid variability in the peptide
composition of a suite of amphiphilic peptide siderophores
from an open ocean Vibrio species. J Biol Inorg Chem
18:489–497. doi:10.1007/s00775-013-0995-3
Gauglitz JM, Zhou HJ, Butler A (2012) A suite of citrate-
derived siderophores from a marine Vibrio species isolated
following the Deepwater Horizon oil spill. J Inor Biochem
107:90–95. doi:10.1016/j.jinorgbio.2011.10.013
Gehring AM, Bradley KA, Walsh CT (1997) Enterobactin
biosynthesis in Escherichia coli: isochorismate lyase
(EntB) is a bifunctional enzyme that is phosphopanteth-
einylated by EntD and then acylated by EntE using ATP
and 2,3-dihydroxybenzoate. Biochem 36:8495–8503.
doi:10.1021/bi970453p
Georlette D, Damien B, Blaise V, Depiereux E, Uversky VN,
Gerday C, Feller G (2003) Structural and functional
adaptations to extreme temperatures in psychrophilic,
mesophilic, and thermophilic DNA ligases. J Biol Chem
278:37015–37023. doi:10.1074/jbc.M305142200
Ghozlan H, Deif H, Abu Kandil R, Sabry S (2006) Biodiversity
of moderately halophilic bacteria in hypersaline habitats in
Egypt. J Gen Appl Microbiol 52:63–72. doi:10.2323/jgam.
52.63
Gledhill M, McCormack P, Ussher S, Achterberg E, Mantoura
R, Worsfold P (2004) Production of siderophore type
chelates by mixed bacterioplankton populations in nutrient
enriched seawater incubations. Mar Chem 88:75–83.
doi:10.1016/j.marchem.2004.03.003
Goswami D, Dhandhukia P, Patel P, Thakker JN (2014a)
Screening of PGPR from saline desert of Kutch: growth
promotion in Arachis hypogea by Bacillus licheniformis
A2. Microbiol Res 169:66–75. doi:10.1016/j.micres.2013.
07.004
Goswami D, Pithwa S, Dhandhukia P, Thakker JN (2014b)
Delineating kocuria turfanensis 2M4 as a credible PGPR: a
novel IAA-producing bacteria isolated from saline desert.
J Plant Interact 9:566–576. doi:10.1080/17429145.2013.
871650
Gounder K et al (2011) Sequence of the hyperplastic genome of
the naturally competent thermus scotoductus SA-01. BMC
Genom 12:14. doi:10.1186/1471-2164-12-577
Guerry P, PerezCasal J, Yao RJ, McVeigh A, Trust TJ (1997) A
genetic locus involved in iron utilization unique to some
Campylobacter strains. J Bacteriol 179:3997–4002
Handley KM, Lloyd JR (2013) Biogeochemical implications of
the ubiquitous colonization of marine habitats and redox
gradients by Marinobacter species. Front Microbiol 4:10.
doi:10.3389/fmicb.2013.00136
Hantke K (1987) Ferrous iron transport mutants in escherichia-
coli-K12. FEMS Microbiol Lett 44:53–57. doi:10.1111/j.
1574-6968.1987.tb02241.x
Hantke K (2004) Ferrous iron transport. In: Crosa JH, Mey AR,
Payne SM (eds) Iron transport in bacteria, vol 1. ASM
Press, Washington, DC, pp 178–184
Harris W, Amin S, Kupper F, Green D, Carrano C (2007) Borate
binding to siderophores: Structure and stability. J Am
Chem Soc 129:12263–12271. doi:10.1021/ja073788v
Hedlund BP, Dodsworth JA, Cole JK, Panosyan HH (2013)
An integrated study reveals diverse methanogens,
Thaumarchaeota, and yet-uncultivated archaeal lineages
in Armenian hot springs Anton Van Leeuwenhoek.
Anton Leeuw Int J G 104:71–82. doi:10.1007/s10482-
013-9927-z
Homann V, Sandy M, Tincu J, Templeton A, Tebo B, Butler A
(2009) Loihichelins A-F, a suite of amphiphilic side-
rophores produced by the marine bacterium halomonas
LOB-5. J Nat Prod 72:884–888. doi:10.1021/np800640h
Hopkinson B, Morel F (2009) The role of siderophores in iron
acquisition by photosynthetic marine microorganisms.
Biometals 22:659–669. doi:10.1007/s10534-009-9235-2
Horowitz NH, Hubbard JS, Cameron RE (1972) Microbiology
of dry Valleys of Antarctica. Science 176:242. doi:10.
1126/science.176.4032.242
Huidrom P, Rajkumar B, Sharma GD (2011) Screening of native
bacteria isolated from tea garden soil of South Assam for
their abiotic stress tolerance. J Pure Appl Microbiol
5:349–353
Ito Y, Butler A (2005) Structure of synechobactins, new side-
rophores of the marine cyanobacterium Synechococcus sp
PCC 7002. Limnol Oceanogr 50:1918–1923
Jarrell KF et al. (2011) Archaeal surface appendages: their
function and the critical role of N-linked glycosylation in
their assembly. In: Conference on instruments, methods,
and missions for astrobiology XIV, SPIE, San Diego, CA,
Aug 23–25 2011. doi:81520o10.1117/12.892939
Jorgensen SL, Thorseth IH, Pedersen RB, Baumberger T, Sch-
leper C (2013) Quantitative and phylogenetic study of the
Deep Sea Archaeal Group in sediments of the Arctic mid-
ocean spreading ridge. Front Microbiol 4:299. doi:10.
3389/fmicb.2013.00299
Kadirvel M, Fanimarvasti F, Forbes S, McBain A, Gardiner JM,
Brown GD, Freeman S (2014) Inhibition of quorum sens-
ing and biofilm formation in Vibrio harveyi by 4-fluoro-
DPD: a novel potent inhibitor of Al-2 signalling. Chem
Commun 50:5000–5002. doi:10.1039/c3cc49678c
Kalinowski BE, Johnsson A, Arlinger J, Pedersen K, Odeggrd-
Jensen A, Edberg F (2006) Microbial mobilization of
uranium from shale mine waste. Geomicrobiol J
23:157–164. doi:10.1080/01490450600599197
Karagoz K, Ates F, Karagoz H, Kotan R, Cakmakci R (2012)
Characterization of plant growth-promoting traits of bac-
teria isolated from the rhizosphere of grapevine grown in
alkaline and acidic soils. Eur J Soil Biol 50:144–150.
doi:10.1016/j.ejsobi.2012.01.007
Kaye J, Sylvan J, Edwards K, Baross J (2011) Halomonas and
Marinobacter ecotypes from hydrothermal vent, sub-
seafloor and deep-sea environments. FEMSMicrobiol Ecol
75:123–133. doi:10.1111/j.1574-6941.2010.00984.x
Kodani S et al (2013) Structure and biosynthesis of scabichelin,
a novel tris-hydroxamate siderophore produced by the
plant pathogen Streptomyces scabies 87.22. Org Biomol
Chem 11:4686–4694. doi:10.1039/c3ob40536b
Kogej T, Gorbushina AA, Gunde-Cimerman N (2006) Hyper-
saline conditions induce changes in cell-wall melanization
and colony structure in a halophilic and a xerophilic black
yeast species of the genus Trimmatostroma. Mycol Res
110:713–724. doi:10.1016/j.mycres.2006.01.014
Konetschny-Rapp S, Jung G, Raymond KN, Meiwes J, Zahner
H (1992) Solution Thermodynamics of the Ferric Com-
plexes of New Desferrioxamine Siderophores Obtained by
Directed Fermentation. J Am Chem Soc 114:2224–2230.
doi:10.1021/ja00032a043
Kozubal MA et al (2013) Geoarchaeota: a new candidate phy-
lum in the Archaea from high-temperature acidic iron mats
in Yellowstone National Park. ISME J 7:622–634. doi:10.
1038/ismej.2012.132
Krewulak KD, Vogel HJ (2008) Structural biology of bacterial
iron uptake. Biochim Biophys Acta 1778:1781–1804.
doi:10.1016/j.bbamem.2007.07.026
Kube M et al (2013) Genome sequence and functional genomic
analysis of the oil-degrading bacterium Oleispira Antarc-
tica. Nature Commun 4:11. doi:10.1038/ncomms3156
Kusel K, Dorsch T, Acker G, Stackebrandt E (1999) Microbial
reduction of Fe(III) in acidic sediments: isolation of
Acidiphilium cryptum JF-5 capable of coupling the
reduction of Fe(III) to the oxidation of glucose. Appl
Environ Microbiol 65:3633–3640
Lewenza S, Conway B, Greenberg EP, Sokol PA (1999) Quo-
rum sensing in Burkholderia cepacia: identification of the
LuxRI homologs CepRI. J Bacteriol 181:748–756
Li XY, Hu Y, Gong J, Zhang LS, Wang GJ (2013) Comparative
genome characterization of Achromobacter members
reveals potential genetic determinants facilitating the adap-
tation to a pathogenic lifestyle. Appl Microbiol Biotechnol
97:6413–6425. doi:10.1007/s00253-013-5018-3
Liu SV, Zhou JZ, Zhang CL, Cole DR, GajdarziskaJosifovska
M, Phelps TJ (1997) Thermophilic Fe(III)-reducing bac-
teria from the deep subsurface: the evolutionary implica-
tions. Science 277:1106–1109. doi:10.1126/science.277.
5329.1106
Liu N, Shang F, Xi LJ, Huang Y (2013) Tetroazolemycins A and
B, two new oxazole-thiazole siderophores from deep-sea
streptomyces olivaceus FXJ8.012. Mar Drugs
11:1524–1533. doi:10.3390/md11051524
Lorenzo Vd, Perez-Martin J, Escolar L, Pesole G, Bertoni G
(2004) Mode of binding of the fur protein to target DNA:
negative regulation of iron-controlled gene expression. In:
Crosa JH, Mey AR, Payne SM (eds) Iron transport in
bacteria, vol 1. ASM Press, Washington, DC, pp 185–196
Luo XZ, Wu SX, Liang YQ (2002) Vesicle formation induced
by metal ions from micelle-forming sodium hexade-
cylimino diacetate in dilute aqueous. Chem Commun
5:492–493. doi:10.1039/b110797f
Luque-Almagro VM, Blasco R, Huertas MJ, Martinez-Luque
M, Moreno-Vivian C, Castillo F, Roldan MD (2005a)
Alkaline cyanide biodegradation by Pseudomonas pseu-
doalcaligenes CECT5344. Biochem Soc Transact
33:168–169
Luque-Almagro VM et al (2005b) Bacterial degradation of
cyanide and its metal complexes under alkaline conditions.
Appl Environ Microbiol 71:940–947. doi:10.1128/aem.71.
2.940-947.2005
Luque-Almagro VM, Blasco R, Martinez-Luque M, Moreno-
Vivian C, Castillo F, RoldanMD (2011) Bacterial cyanide
degradation is under review: Pseudomonas pseudoal-
caligenes CECT5344, a case of an alkaliphilic cyan-
otroph. Biochem Soc Trans 39:269–274. doi:10.1042/
bst0390269
Luther GW, Wu JF (1997) What controls dissolved iron con-
centrations in the world ocean? A comment. Mar Chem
57:173–179. doi:10.1016/s0304-4203(97)00046-7
Machuca A, Aoyama H, Duran N (1999) Isolation and partial
characterization of an extracellular low-molecular mass
component with high phenoloxidase activity from Ther-
moascus aurantiacus. Biochem Biophys Res Commun
256:20–26. doi:10.1006/bbrc.1998.9927
Malviya N, Yandigeri MS, Yadav AK, Solanki MK, Arora DK
(2014) Isolation and characterization of novel alkali-
halophilic actinomycetes from the Chilika brackish water
lake. India Ann Microbiol 64:1829–1838. doi:10.1007/
s13213-014-0831-1
Martin J, Ito Y, Homann V, Haygood M, Butler A (2006)
Structure and membrane affinity of new amphiphilic
siderophores produced by Ochrobactrum sp SP18. J Biol
Inorg Chem 11:633–641. doi:10.1007/s00775-006-0112-y
Martinez J, Butler A (2007) Marine amphiphilic siderophores:
marinobactin structure, uptake, and microbial partitioning.
J Inorg Biochem 101:1692–1698. doi:10.1016/j.jinorgbio.
2007.07.007
Martinez J, Zhang G, Holt P, Jung H, Carrano C, Haygood M,
Butler A (2000) Self-assembling amphiphilic siderophores
from marine bacteria. Science 287:1245–1247. doi:10.
1126/science.287.5456.1245
Martinez JS, Haygood MG, Butler A (2001) Identification of a
natural desferrioxamine siderophore produced by a marine
bacterium. Limnol Oceanogr 46:420–424
Martinez J, Carter-Franklin J, Mann E, Martin J, Haygood M,
Butler A (2003) Structure and membrane affinity of a suite
of amphiphilic siderophores produced by a marine bac-
terium. Proc Natl Acad Sci USA 100:3754–3759. doi:10.
1073/pnas.0637444100
McMillan DGG et al (2010) Acquisition of iron by alkaliphilic
bacillus species. Appl Environ Microbiol 76:6955–6961.
doi:10.1128/aem.01393-10
Meiwes J, Fiedler HP, Haag H, Zahner H, Konetschny-Rapp S,
Jung G (1990) Isolation and characterization of staphylo-
ferrin A, a compound with siderophore activity from Sta-
phylococcus hyicus DSM 20459. FEMS Microbiol Lett
55:201–205
Mishra PK,Mishra S, Selvakumar G, Bisht SC, Bisht JK, Kundu
S, Gupta HS (2008) Characterisation of a psychrotolerant
plant growth promoting Pseudomonas sp strain PGERs17
(MTCC 9000) isolated from North Western Indian Hima-
layas. Ann Microbiol 58:561–568
Neilands JB (1995) Siderophores—structure and function of
microbial iron transport compounds. J Biol Chem
270:26723–26726
Nogi Y, Kato C, Horikoshi K (1998)Moritella japonica sp. nov.,
a novel barophilic bacterium isolated from a Japan Trench
sediment. J Gen Appl Microbiol 44:289–295. doi:10.2323/
jgam.44.289
Olsson-Francis K, de la Torre R, Cockell CS (2010) Isolation of
Novel Extreme-Tolerant Cyanobacteria from a Rock-
Dwelling Microbial Community by Using Exposure to
Low Earth Orbit. Appl Environ Microbiol 76:2115–2121.
doi:10.1128/aem.02547-09
Osorio H, Martinez V, Nieto PA, Holmes DS, Quatrini R (2008)
Microbial iron management mechanisms in extremely
acidic environments: comparative genomics evidence for
diversity and versatility. BMCMicrobiol 8:1. doi:10.1186/
1471-2180-8-203
Owen T, Pynn R, Martinez J, Butler A (2005) Micelle-to-vesicle
transition of an iron-chelating microbial surfactant, mari-
nobactin E. Langmuir 21:12109–12114. doi:10.1021/
la0519352
Owen T, Pynn R, Hammouda B, Butler A (2007) Metal-de-
pendent self-assembly of a microbial surfactant. Langmuir
23:9393–9400. doi:10.1021/la700671p
Owen T, Webb S, Butler A (2008) XAS study of a metal-in-
duced phase transition by a microbial surfactant. Langmuir
24:4999–5002. doi:10.1021/la703833v
Packiavathy IASV, Sasikumar P, Pandian SK, Veera Ravi A
(2013) Prevention of quorum-sensing-mediated biofilm
development and virulence factors production in Vibrio
spp. by curcumin. Appl Microbiol Biotechnol
97:10177–10187. doi:10.1007/s00253-013-4704-5
Pan HQ, Hu JC (2015) Draft genome sequence of the novel
strain Pseudomonas sp 10B238 with potential ability to
produce antibiotics from deep-sea sediment. Mar Genom
23:55–57. doi:10.1016/j.margen.2015.05.003
Pandit AS et al (2015) A snapshot of microbial communities
from the Kutch: one of the largest salt deserts in the World.
Extremophiles 19:973–987. doi:10.1007/s00792-015-
0772-z
Pettit RK (2011) Culturability and secondary metabolite diversity
of extreme microbes: expanding contribution of deep sea
and deep-sea vent microbes to natural product discovery.
Mar Biotechnol 13:1–11. doi:10.1007/s10126-010-9294-y
Picard A, Testemale D, Wagenknecht L, Hazael R, Daniel I
(2014) Iron reduction by the deep-sea bacterium She-
wanella profunda LT13a under subsurface pressure and
temperature conditions. Front Microbiol 5:796. doi:10.
3389/fmicb.2014.00796
Pick U (2004) The respiratory inhibitor antimycin A specifically
binds Fe(III) ions and mediates utilization of iron by the
halotolerant alga Dunaliella salina (Chlorophyta).
Biometals 17:79–86. doi:10.1023/a:1024480720962
Potrykus J, Jonna VR, Dopson M (2011) Iron homeostasis and
responses to iron limitation in extreme acidophiles from the
Ferroplasma genus. Proteomics 11:52–63. doi:10.1002/
pmic.201000193
Quatrini R, Lefimil C, Holmes DS, Jedlicki E (2005) The ferric
iron uptake regulator (Fur) from the extreme acidophile
Acidithiobacillus ferrooxidans. Microbiol 151:2005–2015.
doi:10.1099/mic.0.27581-0
Quatrini R, Lefimil C, Veloso FA, Pedroso I, Holmes DS,
Jedlicki E (2007) Bioinformatic prediction and experi-
mental verification of Fur-regulated genes in the extreme
acidophile Acidithiobacillus ferrooxidans. Nucleic Acids
Res 35:2153–2166. doi:10.1093/nar/gkm068
Raina S, De Vizio D, Palonen EK, Odell M, Brandt AM, Soini
JT, Keshavarz T (2012) Is quorum sensing involved in
lovastatin production in the filamentous fungus Aspergillus
terreus? Process Biochem 47:843–852. doi:10.1016/j.
procbio.2012.02.021
Ramadoss D, Lakkineni VK, Bose P, Ali S, Annapurna K (2013)
Mitigation of salt stress in wheat seedlings by halotolerant
bacteria isolated from saline habitats. Springer Plus 2:7.
doi:10.1186/2193-1801-2-6
Ren GM, Jin Y, Zhang CM, Gu HD, Qu JJ (2015) Character-
istics of Bacillus sp PZ-1 and its biosorption to Pb(II).
Ecotoxicol Environ Saf 117:141–148. doi:10.1016/j.
ecoenv.2015.03.033
Richards AM, Peyton BM, Apel WA (2006) Characterization of
siderophores produced by halophilic microorganisms iso-
lated from Soap Lake inWashington State. Abstr GenMeet
Am Soc Microbiol 106:387
Richards AM, Peyton BM, Gerlach R, Apell WA (2007)
Characterization of siderophores produced by halo-alka-
liphiles isolated from terrestrial environments. Abstr Gen
Meet Am Soc Microbiol 107:565
Rossello-Mora RA et al (1995) Isolation and taxonomic char-
acterization of a halotolerant, facultatively iron-reducing
bacterium system. Appl Microbiol 17:569–573
Sahay H, Mahfooz S, Singh AK, Singh S, Kaushik R, Saxena
AK, Arora DK (2012) Exploration and characterization of
agriculturally and industrially important haloalkaliphilic
bacteria from environmental samples of hypersaline
Sambhar lake, India. World J Microbiol Biotechnol
28:3207–3217. doi:10.1007/s11274-012-1131-1
Sandy M, Butler A (2009) Microbial iron acquisition: marine
and terrestrial siderophores. Chem Rev 109:4580–4595.
doi:10.1021/cr9002787
Sarethy IP, Saxena Y, Kapoor A, Sharma M, Sharma SK, Gupta
V, Gupta S (2011) Alkaliphilic bacteria: applications in
industrial biotechnology. J Ind Microbiol Biotechnol
38:769–790. doi:10.1007/s10295-011-0968-x
Sarkar A, Kazy SK, Sar P (2013) Characterization of arsenic
resistant bacteria from arsenic rich groundwater of West
Bengal, India. Ecotoxicology 22:363–376. doi:10.1007/
s10646-012-1031-z
Scandurra R, Consalvi V, Chiaraluce R, Politi L, Engel PC
(1998) Protein thermostability in extremophiles. Biochi-
mie 80:933–941. doi:10.1016/s0300-9084(00)88890-2
Serrano Figueroa LO (2015) A study on amphiphilic side-
rophore detection, structure elucidation and their iron-
mediated vesicle self-assembly. Montana State University,
Bozeman
Seyedsayamdost MR, Traxler MF, Zheng S-L, Kolter R, Clardy
J (2011) Structure and biosynthesis of amychelin an unu-
sual mixed-ligand siderophore from Amycolatopsis sp.
AA4. J Am Chem Soc 133:11434–11437. doi:10.1021/
ja203577e
Siebert J, Hirsch P, Hoffmann B, Gliesche CG, Peissl K, Jen-
drach M (1996) Cryptoendolithic microorganisms from
Antarctic sandstone of linnaeus terrace (Asgard range):
diversity, properties and interactions. Biodiver Conserv
5:1337–1363. doi:10.1007/bf00051982
Soe CZ, Codd R (2014) Unsaturated macrocyclic dihydroxamic
acid siderophores produced by shewanella putrefaciens
using precursor-directed biosynthesis. ACS Chem Biol
9:945–956. doi:10.1021/cb400901j
Stintzi A, Evans K, Meyer JM, Poole K (1998) Quorum-sensing
and siderophore biosynthesis in Pseudomonas aeruginosa:
lasR/lasI mutants exhibit reduced pyoverdine biosynthesis.
FEMS Microbiol Lett 166:341–345. doi:10.1111/j.1574-
6968.1998.tb13910.x
Sudek LA, Templeton AS, Tebo BM, Staudigel H (2009)
Microbial ecology of Fe (hydr)oxide mats and Basaltic
rock from Vailulu’u seamount, American Samoa. Geomi-
crobiol J 26:581–596. doi:10.1080/01490450903263400
Sunagawa S et al (2015) Structure and function of the global
ocean microbiome. Science 348:1261359. doi:10.1126/
science.1261359
Tal-Gan Y, Stacy DM, Foegen MK, Koenig DW, Blackwell HE
(2013) Highly potent inhibitors of quorum sensing in
staphylococcus aureus revealed through a systematic syn-
thetic study of the group-iii autoinducing peptide. J Am
Chem Soc 135:7869–7882. doi:10.1021/ja3112115
Tang YJ et al (2009) Analysis of metabolic pathways and fluxes
in a newly discovered thermophilic and ethanol-tolerant
geobacillus strain. Biotechnol Bioeng 102:1377–1386.
doi:10.1002/bit.22181
Temirov YV, Esikova TZ, Kashparov IA, Balashova TA,
Vinokurov LM, Alakhov YB (2003) A catecholic side-
rophore produced by the thermoresistant Bacillus licheni-
formis VK21 strain. Russ J Bioorg Chem 29:542–549.
doi:10.1023/B:RUBI.0000008894.80972.2e
Tipre S, Pindi PK, Sharma S (2015) Biotechnological potential
of a Halobacterium of family Bacillaceae Indian.
J Biotechnol 14:65–71
Tsolis RM, Baumler AJ, Heffron F, Stojiljkovic I (1996) Con-
tribution of TonB- and Feo-mediated iron uptake to growth
of Salmonella typhimurium in the mouse. Infect Immun
64:4549–4556
Vasavi HS, Arun AB, Rekha P-D (2014) Anti-quorum sensing
activity of Psidium guajava L. flavonoids against Chro-
mobacterium violaceum and Pseudomonas aeruginosa
PAO1. Microbiol Immunol 58:286–293. doi:10.1111/
1348-0421.12150
Verma R, Naosekpam AS, Kumar S, Prasad R, Shanmugam V
(2007) Influence of soil reaction on diversity and antifungal
activity of fluorescent pseudomonads in crop rhizospheres.
Bioresour Technol 98:1346–1352. doi:10.1016/j.biortech.
2006.05.030
Vishal VK, Manuel VBR (2015) Effect of ACC-deaminase
producing Bacillus cereus brm on the growth of Vigna
radiata (Mung beans) under salinity stress. Res J Biotech-
nol 10:122–130
Vraspir JM, Holt PD, Butler A (2011) Identification of new
members within suites of amphiphilic marine siderophores.
Biometals 24:85–92. doi:10.1007/s10534-010-9378-1
Wang F et al (2008) Environmental adaptation: genomic anal-
ysis of the piezotolerant and psychrotolerant deep-sea iron
reducing bacterium shewanella piezotolerans WP3. PLoS
One 3:e1937. doi:10.1371/journal.pone.0001937
Weaver EA, Wyckoff EE, Mey AR, Morrison R, Payne SM
(2013) FeoA and FeoC are essential components of the
vibrio cholerae ferrous iron uptake system, and FeoC
interacts with FeoB. J Bacteriol 195:4826–4835. doi:10.
1128/jb.00738-13
Wilhelm SW, MacAuley K, Trick CG (1998) Evidence for the
importance of catechol-type siderophores in the iron-lim-
ited growth of a cyanobacterium. Limnol Oceanogr
43:992–997
Wirsen CO, Molyneaux SJ (1999) A study of deep-sea natural
microbial populations and barophilic pure cultures using a
high-pressure chemostat. Appl Environ Microbiol
65:5314–5321
Woo S-M, Kim S-D (2008) Structural identification of side-
rophore(AH18) from bacillus subtilis AH18, a biocontrol
agent of phytophthora blight disease in red-pepper Korean.
J Microbiol Biotechnol 36:326–335
Wood AP, Kelly DP (1991) Isolation and characterization of
thiobacillus-halophilus Sp-nov, A sulfur-oxidizing auto-
trophic eubacterium from a Western Australian Hyper-
saline Lake. Arch Microbiol 156:277–280. doi:10.1007/
bf00262998
Wu LL, Brucker RP, Beard BL, Roden EE, Johnson CM (2013a)
Iron isotope characteristics of hot springs at chocolate pots,
Yellowstone National Park. Astrobiology 13:1091–1101.
doi:10.1089/ast.2013.0996
Wu WF, Wang FP, Li JH, Yang XW, Xiao X, Pan YX (2013b)
Iron reduction and mineralization of deep-sea iron
reducing bacterium Shewanella piezotolerans WP3 at
elevated hydrostatic pressures. Geobiology 11:593–601.
doi:10.1111/gbi.12061
Xu G, Martinez J, Groves J, Butler A (2002) Membrane affinity
of the amphiphilic marinobactin siderophores. J Am Chem
Soc 124:13408–13415. doi:10.1021/ja026768w
Yadav S, Kaushik R, Saxena AK, Arora DK (2011) Diversity
and phylogeny of plant growth-promoting bacilli from
moderately acidic soil. J Basic Microbiol 51:98–106.
doi:10.1002/jobm.201000098
Yadav AN, Sachan SG, Verma P, Saxena AK (2015a)
Prospecting cold deserts of north western Himalayas for
microbial diversity and plant growth promoting attributes.
J Biosci Bioeng 119:683–693. doi:10.1016/j.jbiosc.2014.
11.006
Yadav AN, Sachan SG, Verma P, Tyagi SP, Kaushik R, Saxena
AK (2015b) Culturable diversity and functional annotation
of psychrotrophic bacteria from cold desert of Leh Ladakh
(India). World J Microbiol Biotechnol 31:95–108. doi:10.
1007/s11274-014-1768-z
Ye Q, Roh Y, Carroll SL, Blair B, Zhou JZ, Zhang CL, Fields
MW (2004) Alkaline anaerobic respiration: isolation and
characterization of a novel alkaliphilic and metal-reducing
bacterium. Appl Environ Microbiol 70:5595–5602. doi:10.
1128/aem.70.9.5595-5602.2004
Yue WW, Grizot S, Buchanan SK (2003) Structural evidence
for iron-free citrate and ferric citrate binding to the TonB-
dependent outer membrane transporter FecA. J Mol Biol
332:353–368. doi:10.1016/s0022-2836(03)00855-6
Zane HK, Butler A (2013) Isolation, structure elucidation, and
iron-binding properties of lystabactins, siderophores iso-
lated from a marine Pseudoalteromonas sp. J Nat Prod
76:648–654. doi:10.1021/np3008655
Zane HK, Naka H, Rosconi F, SandyM, HaygoodMG, Butler A
(2014) Biosynthesis of amphi-enterobactin siderophores
by Vibrio harveyi BAA-1116: identification of a bifunc-
tional nonribosomal peptide synthetase condensation
domain. J Am Chem Soc 136:5615–5618. doi:10.1021/
ja5019942
Zhang CL, Stapleton RD, Zhou JZ, Palumbo AV, Phelps TJ
(1999) Iron reduction by psychotrophic enrichment cul-
tures. FEMS Microbiol Ecol 30:367–371. doi:10.1111/j.
1574-6941.1999.tb00664.x
Zhang J, Dong HL, Liu D, Agrawal A (2013) Microbial
reduction of Fe(III) in smectite minerals by thermophilic
methanogen Methanothermobacter thermautotrophicus.
Geochim Cosmochim Acta 106:203–215. doi:10.1016/j.
gca.2012.12.031
Zhou J, Liu S, Xia B, Zhang C, Palumbo AV, Phelps TJ (2001)
Molecular characterization and diversity of thermophilic
iron-reducing enrichment cultures from deep subsurface
environments. J Appl Microbiol 90:96–105. doi:10.1046/j.
1365-2672.2001.01192.x
Zobell CE, Morita RY (1957) Barophilic bacteria in some deep
sea sediments. J Bacteriol 73:563–568