Evidence that the AlgI/AlgJ gene cassette, required for O-acetylation of Pseudomonas aeruginosa alginate, evolved by lateral gene transfer

dc.contributor.authorFranklin, Michael J.
dc.contributor.authorDouthit, Stephanie Ann
dc.contributor.authorMcClure, Marcella A.
dc.date.accessioned2017-07-20T17:50:56Z
dc.date.available2017-07-20T17:50:56Z
dc.date.issued2004-07
dc.description.abstractPseudomonas aeruginosa strains, isolated from chronically infected patients with cystic fibrosis, produce the O-acetylated extracellular polysaccharide, alginate, giving these strains a mucoid phenotype. O acetylation of alginate plays an important role in the ability of mucoid P. aeruginosa to form biofilms and to resist complement-mediated phagocytosis. The O-acetylation process is complex, requiring a protein with seven transmembrane domains (AlgI), a type II membrane protein (AlgJ), and a periplasmic protein (AlgF). The cellular localization of these proteins suggests a model wherein alginate is modified at the polymer level after the transport of O-acetyl groups to the periplasm. Here, we demonstrate that this mechanism for polysaccharide esterification may be common among bacteria, since AlgI homologs linked to type II membrane proteins are found in a variety of gram-positive and gram-negative bacteria. In some cases, genes for these homologs have been incorporated into polysaccharide biosynthetic operons other than for alginate biosynthesis. The phylogenies of AlgI do not correlate with the phylogeny of the host bacteria, based on 16S rRNA analysis. The algI homologs and the gene for their adjacent type II membrane protein present a mosaic pattern of gene arrangement, suggesting that individual components of the multigene cassette, as well as the entire cassette, evolved by lateral gene transfer. AlgJ and the other type II membrane proteins, although more diverged than AlgI, contain conserved motifs, including a motif surrounding a highly conserved histidine residue, which is required for alginate O-acetylation activity by AlgJ. The AlgI homologs also contain an ordered series of motifs that included conserved amino acid residues in the cytoplasmic domain CD-4; the transmembrane domains TM-C, TM-D, and TM-E; and the periplasmic domain PD-3. Site-directed mutagenesis studies were used to identify amino acids important for alginate O-acetylation activity, including those likely required for (i) the interaction of AlgI with the O-acetyl precursor in the cytoplasm, (ii) the export of the O-acetyl group across the cytoplasmic membrane, and (iii) the transfer of the O-acetyl group to a periplasmic protein or to alginate. These results indicate that AlgI belongs to a family of membrane proteins required for modification of polysaccharides and that a mechanism requiring an AlgI homolog and a type II membrane protein has evolved by lateral gene transfer for the esterification of many bacterial extracellular polysaccharides.en_US
dc.identifier.citationFranklin MJ, Douthit SA, McClure MA, "Evidence that the AlgI/AlgJ gene cassette, required for O-acetylation of Pseudomonas aeruginosa alginate, evolved by lateral gene transfer," J Bacteriol, 2004 186(14):4759-4773en_US
dc.identifier.issn0021-9193
dc.identifier.urihttps://scholarworks.montana.edu/handle/1/13374
dc.titleEvidence that the AlgI/AlgJ gene cassette, required for O-acetylation of Pseudomonas aeruginosa alginate, evolved by lateral gene transferen_US
dc.typeArticleen_US
mus.citation.extentfirstpage4759en_US
mus.citation.extentlastpage4773en_US
mus.citation.issue14en_US
mus.citation.journaltitleJournal of Bacteriologyen_US
mus.citation.volume186en_US
mus.data.thumbpage7en_US
mus.identifier.categoryEngineering & Computer Scienceen_US
mus.identifier.doi10.1128/jb.186.14.4759-4773.2004en_US
mus.relation.collegeCollege of Engineeringen_US
mus.relation.departmentCenter for Biofilm Engineering.en_US
mus.relation.departmentChemical & Biological Engineering.en_US
mus.relation.departmentChemical Engineering.en_US
mus.relation.departmentMicrobiology & Immunology.en_US
mus.relation.researchgroupCenter for Biofilm Engineering.en_US
mus.relation.universityMontana State University - Bozemanen_US

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