The energy-conserving electron transfer system used by Desulfovibrio alaskensis strain G20 during pyruvate fermentation involves reduction of endogenously formed fumarate and cytoplasmic and membrane-bound complexes, Hdr-Flox and Rnf.
The adaptation capability of Desulfovibrio to natural fluctuations in electron acceptor availability was evaluated by studying Desulfovibrio alaskensis strain G20 under varying respiratory, fermentative and methanogenic coculture conditions in chemostats. Transition from lactate to pyruvate in coculture resulted in a dramatic shift in the population structure and closer interspecies cell-to-cell interactions. Lower methane production rates in coculture than predicted from pyruvate input was attributed to redirection of electron flow to fumarate reduction. Without a methanogenic partner, accumulation of H₂and formate resulted in greater succinate production. Comparative transcript and gene fitness analysis in concert with physiological data of G20 wildtype and mutants demonstrated that pyruvate fermentation involves respiration of cytoplasmically formed fumarate using cytoplasmic and membrane-bound energy-conserving complexes, Rnf, Hdr-Flox-1 and Hmc. At the low H₂/formate levels maintained in coculture, Rnf likely functions as proton-pumping ferredoxin (Fd): type-I cytochrome c oxidoreductase, which transitions to a proton-pumping Fd(red):  nicotinamide adenine dinucleotide (NAD⁺) oxidoreductase at high H₂/formate levels during fermentation in monoculture. Hdr-Flox-1 is postulated to recycle Fd(red) via a flavin-based electron bifurcation involving NADH, Fdox and the thiol/disulphide-containing DsrC. In a menaquinone (MQ)-based electron confurcation reaction, the high-molecular-weight cytochrome-c₃complex, Hmc, is proposed to then couple DsrC(red) and periplasmic H₂/formate oxidation using the MQ pool to fuel a membrane-bound fumarate reductase.
Department of Civil and Environmental Engineering, University of Washington, Seattle, WA, 98195, USA.
Birte
B
Meyer
Jennifer V
JV
Kuehl
Morgan N
MN
Price
Jayashree
J
Ray
Adam M
AM
Deutschbauer
Adam P
AP
Arkin
David A
DA
Stahl
D002462:Cell Membrane / Q000378:metabolism; D003593:Cytoplasm / Q000378:metabolism; D003901:Desulfovibrio / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D004579:Electron Transport; D005285:Fermentation; D005561:Formates / Q000378:metabolism; D005650:Fumarates / Q000378:metabolism*; D015870:Gene Expression; D019344:Lactic Acid / Q000378:metabolism; D026901:Membrane Transport Proteins / Q000378:metabolism; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000378:metabolism; D017494:Proton Pumps / Q000378:metabolism; D019289:Pyruvic Acid / Q000378:metabolism*
D005561:Formates; D005650:Fumarates; D026901:Membrane Transport Proteins; D017494:Proton Pumps; C030544:formic acid; D019344:Lactic Acid; D019289:Pyruvic Acid; D010088:Oxidoreductases