Syntrophic growth of Desulfovibrio alaskensis requires genes for H2 and formate metabolism as well as those for flagellum and biofilm formation

• Published in: Applied and Environmental Microbiology 2015-04, Vol.81 (7), p.2339-2348
• Main Authors: Krumholz, Lee R, Bradstock, Peter, Sheik, Cody S, Diao, Yiwei, Gazioglu, Ozcan, Gorby, Yuri, McInerney, Michael J
• Format: Article
• Language: English
• Subjects: Biofilms - growth & development; Clostridiales - growth & development; Clostridiales - metabolism; Clostridiales - physiology; Desulfovibrio; Desulfovibrio - genetics; Desulfovibrio - growth & development; Desulfovibrio - metabolism; Desulfovibrio - physiology; DNA Transposable Elements; Energy Metabolism; Flagella - physiology; Formates - metabolism; Genes, Bacterial; Hydrogen - metabolism; Microbial Ecology; Microbial Interactions; Mutagenesis, Insertional; Organic Chemicals - metabolism; Symbiosis; Syntrophomonas wolfei
• ISSN: 0099-2240; 1098-5336; 1098-6596
• DOI: 10.1128/AEM.03358-14

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.