title: Syntrophic growth of Desulfovibrio alaskensis requires genes for H2 and formate metabolism as well as those for flagellum and biofilm formation.
abstract: In anaerobic environments, mutually beneficial metabolic interactions between microorganisms (syntrophy) are essential for oxidation of organic matter to carbon dioxide and methane. Syntrophic interactions typically involve a microorganism degrading an organic compound to primary fermentation by-products and sources of electrons (i.e., formate, hydrogen, or nanowires) and a partner producing methane or respiring the electrons via alternative electron accepting processes. Using a transposon gene mutant library of the sulfate-reducing Desulfovibrio alaskensis G20, we screened for mutants incapable of serving as the electron-accepting partner of the butyrate-oxidizing bacterium, Syntrophomonas wolfei. A total of 17 gene mutants of D. alaskensis were identified as incapable of serving as the electron-accepting partner. The genes identified predominantly fell into three categories: membrane surface assembly, flagellum-pilus synthesis, and energy metabolism. Among these genes required to serve as the electron-accepting partner, the glycosyltransferase, pilus assembly protein (tadC), and flagellar biosynthesis protein showed reduced biofilm formation, suggesting that each of these components is involved in cell-to-cell interactions. Energy metabolism genes encoded proteins primarily involved in H2 uptake and electron cycling, including a rhodanese-containing complex that is phylogenetically conserved among sulfate-reducing Deltaproteobacteria. Utilizing an mRNA sequencing approach, analysis of transcript abundance in wild-type axenic and cocultures confirmed that genes identified as important for serving as the electron-accepting partner were more highly expressed under syntrophic conditions. The results imply that sulfate-reducing microorganisms require flagellar and outer membrane components to effectively couple to their syntrophic partners; furthermore, H2 metabolism is essential for syntrophic growth of D. alaskensis G20.
authors.affiliation: Department of Microbiology and Plant Biology, The University of Oklahoma, Norman, Oklahoma, USA Institute for Energy and the Environment, The University of Oklahoma, Norman, Oklahoma, USA krumholz@ou.edu.
authors.forename: Lee R
authors.initials: LR
authors.lastname: Krumholz
authors.affiliation: Department of Microbiology and Plant Biology, The University of Oklahoma, Norman, Oklahoma, USA.
authors.forename: Peter
authors.initials: P
authors.lastname: Bradstock
authors.affiliation: Department of Earth and Environmental Science, University of Michigan, Ann Arbor, Michigan, USA.
authors.forename: Cody S
authors.initials: CS
authors.lastname: Sheik
authors.affiliation: Department of Microbiology and Plant Biology, The University of Oklahoma, Norman, Oklahoma, USA.
authors.forename: Yiwei
authors.initials: Y
authors.lastname: Diao
authors.affiliation: Department of Microbiology and Plant Biology, The University of Oklahoma, Norman, Oklahoma, USA.
authors.forename: Ozcan
authors.initials: O
authors.lastname: Gazioglu
authors.affiliation: Department of Civil and Environmental Engineering, Rensselaer Polytechnic Institute, Troy, New York, USA.
authors.forename: Yuri
authors.initials: Y
authors.lastname: Gorby
authors.affiliation: Department of Microbiology and Plant Biology, The University of Oklahoma, Norman, Oklahoma, USA.
authors.forename: Michael J
authors.initials: MJ
authors.lastname: McInerney
mesh_terms: D018441:Biofilms / Q000254:growth & development*; D000068016:Eubacteriales / Q000254:growth & development / Q000378:metabolism / Q000502:physiology*; D004251:DNA Transposable Elements; D003901:Desulfovibrio / Q000235:genetics / Q000254:growth & development / Q000378:metabolism / Q000502:physiology*; D004734:Energy Metabolism; D005407:Flagella / Q000502:physiology*; D005561:Formates / Q000378:metabolism*; D005798:Genes, Bacterial; D006859:Hydrogen / Q000378:metabolism*; D056265:Microbial Interactions; D016254:Mutagenesis, Insertional; D009930:Organic Chemicals / Q000378:metabolism; D013559:Symbiosis
chemical_list: D004251:DNA Transposable Elements; D005561:Formates; D009930:Organic Chemicals; C030544:formic acid; D006859:Hydrogen