The electron transfer system of syntrophically grown Desulfovibrio vulgaris.
Interspecies hydrogen transfer between organisms producing and consuming hydrogen promotes the decomposition of organic matter in most anoxic environments. Although syntrophic coupling between hydrogen producers and consumers is a major feature of the carbon cycle, mechanisms for energy recovery at the extremely low free energies of reactions typical of these anaerobic communities have not been established. In this study, comparative transcriptional analysis of a model sulfate-reducing microbe, Desulfovibrio vulgaris Hildenborough, suggested the use of alternative electron transfer systems dependent on growth modality. During syntrophic growth on lactate with a hydrogenotrophic methanogen, numerous genes involved in electron transfer and energy generation were upregulated in D. vulgaris compared with their expression in sulfate-limited monocultures. In particular, genes coding for the putative membrane-bound Coo hydrogenase, two periplasmic hydrogenases (Hyd and Hyn), and the well-characterized high-molecular-weight cytochrome (Hmc) were among the most highly expressed and upregulated genes. Additionally, a predicted operon containing genes involved in lactate transport and oxidation exhibited upregulation, further suggesting an alternative pathway for electrons derived from lactate oxidation during syntrophic growth. Mutations in a subset of genes coding for Coo, Hmc, Hyd, and Hyn impaired or severely limited syntrophic growth but had little effect on growth via sulfate respiration. These results demonstrate that syntrophic growth and sulfate respiration use largely independent energy generation pathways and imply that to understand microbial processes that sustain nutrient cycling, lifestyles not captured in pure culture must be considered.
Walker
Christopher B
CB
Department of Civil and Environmental Engineering, University of Washington, 302 More Hall, Box 352700. Seattle, WA 98195-2700, USA.
He
Zhili
Z
Yang
Zamin K
ZK
Ringbauer
Joseph A
JA
He
Qiang
Q
Zhou
Jizhong
J
Voordouw
Gerrit
G
Wall
Judy D
JD
Arkin
Adam P
AP
Hazen
Terry C
TC
Stolyar
Sergey
S
Stahl
David A
DA
D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D018533:Biomass; D003470:Culture Media; D016969:Desulfovibrio vulgaris / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism; D004579:Electron Transport; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial; D006859:Hydrogen / Q000378:metabolism; D019344:Lactic Acid / Q000378:metabolism; D017017:Methanococcus / Q000145:classification / Q000254:growth & development; D009154:Mutation; D010084:Oxidation-Reduction; D013431:Sulfates / Q000378:metabolism*
D001426:Bacterial Proteins; D003470:Culture Media; D013431:Sulfates; D019344:Lactic Acid; D006859:Hydrogen