Formate-driven growth coupled with H(2) production.
Although a common reaction in anaerobic environments, the conversion of formate and water to bicarbonate and H(2) (with a change in Gibbs free energy of ΔG° = +1.3 kJ mol(-1)) has not been considered energetic enough to support growth of microorganisms. Recently, experimental evidence for growth on formate was reported for syntrophic communities of Moorella sp. strain AMP and a hydrogen-consuming Methanothermobacter species and of Desulfovibrio sp. strain G11 and Methanobrevibacter arboriphilus strain AZ. The basis of the sustainable growth of the formate-users is explained by H(2) consumption by the methanogens, which lowers the H(2) partial pressure, thus making the pathway exergonic. However, it has not been shown that a single strain can grow on formate by catalysing its conversion to bicarbonate and H(2). Here we report that several hyperthermophilic archaea belonging to the Thermococcus genus are capable of formate-oxidizing, H(2)-producing growth. The actual ΔG values for the formate metabolism are calculated to range between -8 and -20 kJ mol(-1) under the physiological conditions where Thermococcus onnurineus strain NA1 are grown. Furthermore, we detected ATP synthesis in the presence of formate as a sole energy source. Gene expression profiling and disruption identified the gene cluster encoding formate hydrogen lyase, cation/proton antiporter and formate transporter, which were responsible for the growth of T. onnurineus NA1 on formate. This work shows formate-driven growth by a single microorganism with protons as the electron acceptor, and reports the biochemical basis of this ability.
Kim
Yun Jae
YJ
Korea Ocean Research & Development Institute, PO Box 29, Ansan 425-600, Korea.
Lee
Hyun Sook
HS
Kim
Eun Sook
ES
Bae
Seung Seob
SS
Lim
Jae Kyu
JK
Matsumi
Rie
R
Lebedinsky
Alexander V
AV
Sokolova
Tatyana G
TG
Kozhevnikova
Darya A
DA
Cha
Sun-Shin
SS
Kim
Sang-Jin
SJ
Kwon
Kae Kyoung
KK
Imanaka
Tadayuki
T
Atomi
Haruyuki
H
Bonch-Osmolovskaya
Elizaveta A
EA
Lee
Jung-Hyun
JH
Kang
Sung Gyun
SG
D000255:Adenosine Triphosphate / Q000032:analysis / Q000096:biosynthesis; D000693:Anaerobiosis; D055162:Biocatalysis; D002245:Carbon Dioxide / Q000378:metabolism; D004583:Electrons; D005560:Formate Dehydrogenases; D005561:Formates / Q000378:metabolism*; D020869:Gene Expression Profiling; D019848:Gene Expression Regulation, Archaeal / Q000235:genetics; D006859:Hydrogen / Q000378:metabolism*; D006864:Hydrogenase; D008190:Lyases / Q000378:metabolism; D008954:Models, Biological; D009097:Multienzyme Complexes; D005810:Multigene Family / Q000235:genetics; D010084:Oxidation-Reduction; D010313:Partial Pressure; D011522:Protons; D020133:Reverse Transcriptase Polymerase Chain Reaction; D019712:Thermococcus / Q000145:classification / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism*; D014867:Water / Q000378:metabolism
D005561:Formates; D009097:Multienzyme Complexes; D011522:Protons; D014867:Water; C030544:formic acid; D002245:Carbon Dioxide; D006859:Hydrogen; D000255:Adenosine Triphosphate; D006864:Hydrogenase; D005560:Formate Dehydrogenases; C054017:formate hydrogenlyase; D008190:Lyases