Scholarly Work - Center for Biofilm Engineering

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    Biofilm reactors for the treatment of used water in space:potential, challenges, and future perspectives
    (Elsevier BV, 2023-12) Espinosa-Ortiz, Erika J.; Gerlach, Robin; Peyton, Brent M.; Roberson, Luke; Yeh, Daniel H.
    Water is not only essential to sustain life on Earth, but also is a crucial resource for long-duration deep space exploration and habitation. Current systems in space rely on the resupply of water from Earth, however, as missions get longer and move farther away from Earth, resupply will no longer be a sustainable option. Thus, the development of regenerative reclamation water systems through which useable water can be recovered from “waste streams” (i.e., used waters) is sorely needed to further close the loop in space life support systems. This review presents the origin and characteristics of different used waters generated in space and discusses the intrinsic challenges of developing suitable technologies to treat such streams given the unique constrains of space exploration and habitation (e.g., different gravity conditions, size and weight limitations, compatibility with other systems, etc.). In this review, we discuss the potential use of biological systems, particularly biofilms, as possible alternatives or additions to current technologies for water reclamation and waste treatment in space. The fundamentals of biofilm reactors, their advantages and disadvantages, as well as different reactor configurations and their potential for use and challenges to be incorporated in self-sustaining and regenerative life support systems in long-duration space missions are also discussed. Furthermore, we discuss the possibility to recover value-added products (e.g., biomass, nutrients, water) from used waters and the opportunity to recycle and reuse such products as resources in other life support subsystems (e.g., habitation, waste, air, etc.).
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    Potential biofilm control strategies for extended spaceflight missions
    (Elsevier BV, 2020-12) Zea, Luis; McLean, Robert J. C.; Rook, Tony A.; Angle, Geoffrey; Carter, D. Layne; Delegard, Angela; Denvir, Adrian; Gerlach, Robin; Gorti, Sridhar; McIlwaine, Doug; Nur, Mononita; Peyton, Brent M.; Stewart, Philip S.; Sturman, Paul; Justiniano, Yo Ann Velez
    Biofilms, surface-adherent microbial communities, are associated with microbial fouling and corrosion in terrestrial water-distribution systems. Biofilms are also present in human spaceflight, particularly in the Water Recovery System (WRS) on the International Space Station (ISS). The WRS is comprised of the Urine Processor Assembly (UPA) and the Water Processor Assembly (WPA) which together recycles wastewater from human urine and recovered humidity from the ISS atmosphere. These wastewaters and various process streams are continually inoculated with microorganisms primarily arising from the space crew microbiome. Biofilm-related fouling has been encountered and addressed in spacecraft in low Earth orbit, including ISS and the Russian Mir Space Station. However, planned future missions beyond low Earth orbit to the Moon and Mars present additional challenges, as resupplying spare parts or support materials would be impractical and the mission timeline would be in the order of years in the case of a mission to Mars. In addition, future missions are expected to include a period of dormancy in which the WRS would be unused for an extended duration. The concepts developed in this review arose from a workshop including NASA personnel and representatives with biofilm expertise from a wide range of industrial and academic backgrounds. Here, we address current strategies that are employed on Earth for biofilm control, including antifouling coatings and biocides and mechanisms for mitigating biofilm growth and damage. These ideas are presented in the context of their applicability to spaceflight and identify proposed new topics of biofilm control that need to be addressed in order to facilitate future extended, crewed, spaceflight missions.
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    Carbon-dependent chromate toxicity mechanism in an environmental Arthrobacter isolate
    (2018-08) Field, Erin K.; Blaskovich, John P.; Peyton, Brent M.; Gerlach, Robin
    Arthrobacter spp. are widespread in soil systems and well-known for their Cr(VI) reduction capabilities making them attractive candidates for in situ bioremediation efforts. Cellulose drives carbon flow in soil systems; yet, most laboratory studies evaluate Arthrobacter-Cr(VI) interactions solely with nutrient-rich media or glucose. This study aims to determine how various cellulose degradation products and biostimulation substrates influence Cr(VI) toxicity, reduction, and microbial growth of an environmental Arthrobacter sp. isolate. Laboratory culture-based studies suggest there is a carbon-dependent Cr(VI) toxicity mechanism that affects subsequent Cr(VI) reduction by strain LLW01. Strain LLW01 could only grow in the presence of, and reduce, 50 μM Cr(VI) when glucose or lactate were provided. Compared to lactate, Cr(VI) was at least 30-fold and 10-fold more toxic when ethanol or butyrate was the sole carbon source, respectively. The addition of sulfate mitigated toxicity somewhat, but had no effect on the extent of Cr(VI) reduction. Cell viability studies indicated that a small fraction of cells were viable after 8 days suggesting cell growth and subsequent Cr(VI) reduction may resume. These results suggest when designing bioremediation strategies with Arthrobacter spp. such as strain LLW01, carbon sources such as glucose and lactate should be considered over ethanol and butyrate.
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    Influence of carbon sources and electron shuttles on ferric iron reduction by Cellulomonas sp. strain ES6
    (2011-09) Gerlach, Robin; Field, E. K.; Viamajala, Sridhar; Peyton, Brent M.; Apel, William A.; Cunningham, Alfred B.
    Microbially reduced iron minerals can reductively transform a variety of contaminants including heavy metals, radionuclides, chlorinated aliphatics, and nitroaromatics. A number of Cellulomonas spp. strains, including strain ES6, isolated from aquifer samples obtained at the U.S. Department of Energy’s Hanford site in Washington, have been shown to be capable of reducing Cr(VI), TNT, natural organic matter, and soluble ferric iron [Fe(III)]. This research investigated the ability of Cellulomonas sp. strain ES6 to reduce solid phase and dissolved Fe(III) utilizing different carbon sources and various electron shuttling compounds. Results suggest that Fe(III) reduction by and growth of strain ES6 was dependent upon the type of electron donor, the form of iron present, and the presence of synthetic or natural organic matter, such as anthraquinone-2,6-disulfonate (AQDS) or humic substances. This research suggests that Cellulomonas sp. strain ES6 could play a significant role in metal reduction in the Hanford subsurface and that the choice of carbon source and organic matter addition can allow for independent control of growth and iron reduction activity.
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    Permeable reactive biobarriers for in-situ Cr(VI) reduction: Bench scale tests using Cellulomonas sp. strain ES6
    (2008-12) Viamajala, Sridhar; Peyton, Brent M.; Gerlach, Robin; Vaideeswaran, S.; Apel, William A.; Petersen, James N.
    Chromate (Cr(VI)) reduction studies were performed in bench scale flow columns using the fermentative subsurface isolate Cellulomonas sp. strain ES6. In these tests, columns packed with either quartz sand or hydrous ferric oxide (HFO)-coated quartz sand, were inoculated with strain ES6 and fed nutrients to stimulate growth before nutrient-free Cr(VI) solutions were injected. Results show that in columns containing quartz sand, a continuous inflow of 2 mg/L Cr(VI) was reduced to below detection limits in the effluent for durations of up to 5.7 residence times after nutrient injection was discontinued proving the ability of strain ES6 to reduce chromate in the absence of an external electron donor. In the HFO-containing columns, Cr(VI) reduction was significantly prolonged and effluent Cr(VI) concentrations remained below detectable levels for periods of up to 66 residence times after nutrient injection was discontinued. Fe was detected in the effluent of the HFOcontaining columns throughout the period of Cr(VI)removal indicating that the insoluble Fe(III) bearing solids were being continuously reduced to form soluble Fe(II) resulting in prolonged abiotic Cr(VI) reduction. Thus, growth of Cellulomonas within the soil columns resulted in formation of permeable reactive barriers that could reduce Cr(VI) and Fe(III) for extended periods even in the absence of external electron donors. Other bioremediation systems employing Fe(II)-mediated reactions require a continuous presence of external nutrients to regenerate Fe(II). After depletion of nutrients, contaminant removal within these systems occurs by reaction with surface-associated Fe(II) that can rapidly become inaccessible due to formation of crystalline Fe-minerals or other precipitates. The ability of fermentative organisms like Cellulomonas to reduce metals without continuous nutrient supply in the subsurface offers a viable and economical alternative technology for in situ remediation of Cr(VI)-contaminated groundwater through formation of permeable reactive biobarriers (PRBB).
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    Application of molecular techniques to elucidate the influence of cellulosic waste on the bacterial community structure at a simulated low level waste site
    (2010-03) Field, E. K.; D'Imperio, Seth; Miller, A. R.; VanEngelen, Michael R.; Gerlach, Robin; Lee, Brady D.; Apel, William A.; Peyton, Brent M.
    Low-level radioactive waste sites, including those at various U.S. Department of Energy (DOE) sites, frequently contain cellulosic waste in the form of paper towels, cardboard boxes, or wood contaminated with heavy metals and radionuclides such as chromium and uranium. To understand how the soil microbial community is influenced by the presence of cellulosic waste products, multiple soil samples were obtained from a non-radioactive model low-level waste test pit at the Idaho National Laboratory. Samples were analyzed using 16S rRNA gene clone libraries and 16S rRNA gene microarray (PhyloChip) analyses. Both methods revealed changes in the bacterial community structure with depth. In all samples, the PhyloChip detected significantly more Operational Taxonomic Units (OTUs), and therefore relative diversity, than the clone libraries. Diversity indices suggest that diversity is lowest in the Fill (F) and Fill Waste (FW) layers and greater in the Wood Waste (WW) and Waste Clay (WC) layers. Principal coordinates analysis and lineage specific analysis determined that Bacteroidetes and Actinobacteria phyla account for most of the significant differences observed between the layers. The decreased diversity in the FW layer and increased members of families containing known cellulose degrading microorganisms suggests the FW layer is an enrichment environment for these organisms. These results suggest that the presence of the cellulosic material significantly influences the bacterial community structure in a stratified soil system.
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    UO2+2 speciation determines uranium toxicity and bioaccumulation in an environmental Pseudomonas sp. isolate
    (2010-04) VanEngelen, Michael R.; Field, E. K.; Gerlach, Robin; Lee, Brady D.; Apel, William A.; Peyton, Brent M.
    In the present study, experiments were performed to investigate how representative cellulosic breakdown products, when serving as growth substrates under aerobic conditions, affect hexavalent uranyl cation (UO2+2 ) toxicity and bioaccumulation within a Pseudomonas sp. isolate (designated isolate A). Isolate A taken from the Cold Test Pit South (CTPS) region of the Idaho National Laboratory (INL), Idaho Falls, ID, USA. The INL houses low-level uranium-contaminated cellulosic material and understanding how this material, and specifically its breakdown products, affect U-bacterial interactions is important for understanding UO2+2 fate and mobility. Toxicity was modeled using a generalized Monod expression. Butyrate, dextrose, ethanol, and lactate served as growth substrates. The potential contribution of bicarbonate species present in high concentrations was also investigated and compared with toxicity and bioaccumulation patterns seen in low-bicarbonate conditions. Isolate A was significantly more sensitive to UO2+2 and accumulated significantly more UO2+2 in low-bicarbonate concentrations. In addition, UO2+2 growth inhibition and bioaccumulation varied depending on the growth substrate. In the presence of high bicarbonate concentrations, sensitivity to UO2+2 inhibition was greatly mitigated, and did not vary between the four substrates tested. The extent of UO2+2 accumulation was also diminished. The observed patterns were related to UO2+2 aqueous complexation, as predicted by MINTEQ (ver. 2.52) (Easton, PA, USA). In the low- bicarbonate medium, the presence of positively charged and unstable UO2+2 -hydroxide complexes explained both the greater sensitivity of isolate A to UO2+2, and the ability of isolate A to accumulate significant amounts of UO2+2 . The exclusive presence of negatively charged and stable UO2+2 -carbonate complexes in the high bi-carbonate medium explained the diminished sensitivity of isolate A to UO2+2 toxicity, and limited ability of isolate A to accumulate UO2+2 .
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    Uranium exerts acute toxicity by binding to pyrroloquinoline quinone cofactor
    (2010-12) VanEngelen, Michael R.; Szilagyi, Robert K.; Gerlach, Robin; Lee, Brady D.; Apel, William A.; Peyton, Brent M.
    Uranium as an environmental contaminant has been shown to be toxic to eukaryotes and prokaryotes; however, no specific mechanisms of uranium toxicity have been proposed so far. Here a combination of in vivo, in vitro, and in silico studies are presented describing direct inhibition of pyrroloquinoline quinone (PQQ)-dependent growth and metabolism by uranyl cations. Electrospray-ionization mass spectroscopy, UV-vis optical spectroscopy, competitive Ca2+/uranyl binding studies, relevant crystal structures, and molecular modeling unequivocally indicate the preferred binding of uranyl simultaneously to the carboxyl oxygen, pyridine nitrogen, and quinone oxygen of the PQQmolecule. The observed toxicity patterns are consistent with the biotic ligand model of acute metal toxicity. In addition to the environmental implications, this work represents the first proposed molecular mechanism of uranium toxicity in bacteria, and has relevance for uranium toxicity in many living systems.
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    Multiple mechanisms of uranium immobilization by Cellulomonas sp. strain ES6
    (2011-02) Sivaswamy, V.; Boyanov, M. I.; Peyton, Brent M.; Viamajala, Sridhar; Gerlach, Robin; Apel, William A.; Sani, Rajesh K.; Dohnalkova, Alice; Kemner, K. M.; Borch, Thomas
    Removal of hexavalent uranium (U(VI)) from aqueous solution was studied using a gram-positive facultative anaerobe, Cellulomonas sp. strain ES6, under anaerobic, non-growth conditions in bicarbonate and PIPES buffers.Inorganic phosphate was released by cells during the experiments providing ligands for formation of insoluble U(VI) phosphates. Phosphate release was most probably the result of anaerobic hydrolysis of intracellular polyphosphates accumulated by ES6 during aerobic growth. Microbial reduction of U(VI) to U(IV) was also observed. However, the relative magnitudes of U(VI) removal by abiotic (phosphate-based) precipitation and microbial reduction depended on the buffer chemistry. In bicarbonate buffer, X-ray absorption fine structure (XAFS) spectroscopy showed that U in the solid phase was present primarily as a non-uraninite U(IV) phase, whereas in PIPES buffer, U precipitates consisted primarily of U(VI)-phosphate. In both bicarbonate and PIPES buffer, net release of cellular phosphate was measured to be lower than that observed in U-free controls suggesting simultaneous precipitation of U and PO₄³⠻. In PIPES, U(VI) phosphates formed a significant portion of U precipitates and mass balance estimates of U and P along with XAFS data corroborate this hypothesis. High-resolution transmission electron microscopy (HR-TEM) and energy dispersive X-ray spectroscopy (EDS) of samples from PIPES treatments indeed showed both extracellular and intracellular accumulation of U solids with nanometer sized lath structures that contained U and P. In bicarbonate, however, more phosphate was removed than required to stoichiometrically balance the U(VI)/U(IV) fraction determined by XAFS, suggesting that U(IV) precipitated together with phosphate in this system. When anthraquinone-2,6-disulfonate (AQDS), a known electron shuttle, was added to the experimental reactors, the dominant removal mechanism in both buffers was reduction to a non-uraninite U(IV) phase.Uranium immobilization by abiotic precipitation or microbial reduction has been extensively reported; however, the present work suggests that strain ES6 can remove U(VI) from solution simultaneously through precipitation with phosphate ligands and microbial reduction, depending on the environmental conditions. Cellulomonadaceae are environmentally relevant subsurface bacteria and here, for the first time, the presence of multiple U immobilization mechanisms within one organism is reported using Cellulomonas sp. strain ES6
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    Influence of carbon sources and electron shuttles on ferric iron reduction by Cellulomonas sp. strain ES6
    (2011-09) Gerlach, Robin; Field, E. K.; Viamajala, Sridhar; Peyton, Brent M.; Apel, William A.; Cunningham, Alfred B.
    Microbially reduced iron minerals can reductively transform a variety of contaminants including heavy metals, radionuclides, chlorinated aliphatics, and nitroaromatics. A number of Cellulomonas spp. strains, including strain ES6, isolated from aquifer samples obtained at the U.S. Department of Energy’s Hanford site in Washington, have been shown to be capable of reducing Cr(VI), TNT, natural organic matter, and soluble ferric iron [Fe(III)]. This research investigated the ability of Cellulomonas sp. strain ES6 to reduce solid phase and dissolved Fe(III) utilizing different carbon sources and various electron shuttling compounds. Results suggest that Fe(III) reduction by and growth of strain ES6 was dependent upon the type of electron donor, the form of iron present, and the presence of synthetic or natural organic matter, such as anthraquinone-2,6-disulfonate (AQDS) or humic substances. This research suggests that Cellulomonas sp. strain ES6 could play a significant role in metal reduction in the Hanford subsurface and that the choice of carbon source and organic matter addition can allow for independent control of growth and iron reduction activity.
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