Formate-limited growth of Methanobacterium formicium in steady-state cultures

Chua, Han Bing; Robinson, John P.

doi:10.1007/bf00408027

Cited by 21 publications

(10 citation statements)

References 8 publications

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“…If increased fdhCAB transcription is a survival response of cells growing on H 2 plus CO 2 faced with an H 2 limitation, then transcription of the hydrogenase-encoding genes might increase in formate-growing cells faced with a formate limitation. This can be investigated directly by using formate to limit growth in a continuous culture system (8). The fdh transcripts are, however, present only at low levels in M. thermoformicicum cells growing on H 2 plus CO 2 under conditions of excess H 2 , whereas the frh, mvh, and mth transcripts are present at relatively high levels in M. thermoformicicum cells growing with excess formate (Fig.…”

Section: Discussionmentioning

confidence: 99%

Growth- and substrate-dependent transcription of the formate dehydrogenase (fdhCAB) operon in Methanobacterium thermoformicicum Z-245

Nölling

Reeve

1997

J Bacteriol

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The formate dehydrogenase-encoding fdhCAB operon and flanking genes have been cloned and sequenced from Methanobacterium thermoformicicum Z-245. fdh transcription was shown to be initiated 21 bp upstream from fdhC, although most fdh transcripts terminated or were processed between fdhC and fdhA. The resulting fdhC, fdhAB, and fdhCAB transcripts were present at all growth stages in cells growing on formate but were barely detectable during early exponential growth on H 2 plus CO 2 . The levels of the fdh transcripts did, however, increase dramatically in cells growing on H 2 plus CO 2 , coincident with the decrease in the growth rate and the onset of constant methanogenesis that occurred when culture densities reached an optical density at 600 nm of ϳ0.5. The mth transcript that encodes the H 2 -dependent methenyl-H 4 MPT reductase (MTH) and the frh and mvh transcripts that encode the coenzyme F 420 -reducing (FRH) and nonreducing (MVH) hydrogenases, respectively, were also present in cells growing on formate, consistent with the synthesis of three hydrogenases, MTH, FRH, and MVH, in the absence of exogenously supplied H 2 . Reducing the H 2 supply to M. thermoformicicum cells growing on H 2 plus CO 2 reduced the growth rate and CH 4 production but increased frh and fdh transcription and also increased transcription of the mtd, mer, and mcr genes that encode enzymes that catalyze steps 4, 5, and 7, respectively, in the pathway of CO 2 reduction to CH 4 . Reducing the H 2 supply to a level insufficient for growth resulted in the disappearance of all methane gene transcripts except the mcr transcript, which increased. Regions flanking the fdhCAB operon in M. thermoformicicum Z-245 were used as probes to clone the homologous region from the Methanobacterium thermoautotrophicum ⌬H genome. Sequencing revealed the presence of very similar genes except that the genome of M. thermoautotrophicum, a methanogen incapable of growth on formate, lacked the fdhCAB operon.Methanobacterium thermoautotrophicum ⌬H and Methanobacterium thermoformicicum Z-245 are very closely related, thermophilic methanogens that could be considered members of the same species (16,23,41). However, M. thermoautotrophicum grows only by the H 2 -dependent reduction of CO 2 to CH 4 (9, 39), whereas M. thermoformicicum is more metabolically versatile and can also catabolize formate to CH 4 and therefore can grow in the absence of exogenously supplied H 2 . The availability of H 2 determines which of two intersecting pathways of CO 2 reduction to CH 4 is employed by M. thermoautotrophicum (20, 39). When excess H 2 is available, the mth and mrt genes are transcribed, resulting in the synthesis of the H 2 -dependent N 5 ,N 10 -methenyltetrahydromethanopterin (methenyl-H 4 MPT) reductase (MTH) and methyl coenzyme M reductase (MR) II, respectively, that catalyze steps 4 and 7 in the seven-step pathway of CO 2 reduction to CH 4 (5, 25, 27, 49). However, under H 2 -limited growth conditions, these steps are catalyzed by the reduced coenzyme F 420 -dependent N 5...

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Section: Discussionmentioning

confidence: 99%

Growth- and substrate-dependent transcription of the formate dehydrogenase (fdhCAB) operon in Methanobacterium thermoformicicum Z-245

Nölling

Reeve

1997

J Bacteriol

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“…(12) and (13)] requires the total dissipation ( D : ' / r A x ) g r , which includes the growth-associated and maintenance-associated dissipation [Eq. (11)]. In a previous article2' a simple correlation has been provided for (D:'/rAx)gr.…”

Section: In This Equation ( D : ' / F -A~)~~ Is the Gibbs Energy Reqmentioning

confidence: 99%

“…(1) and (11) to give the correlation [Eq. (17)] which allows for heterotrophic growth the estimation of the total dissipationlc-mole biomass as a function of (1) growth rate…”

Section: The Combined Correlation For Me (For Aerobic/anaerobic Growtmentioning

confidence: 99%

A thermodynamically based correlation for maintenance gibbs energy requirements in aerobic and anaerobic chemotrophic growth

Tijhuis

Loosdrecht

Heijnen

1993

Biotech & Bioengineering

246

238

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A thermodynamic framework has been provided for the description of maintenance requirements of microorganisms. The central parameter is the biomass specific Gibbs energy consumption for maintenance, m(E) (kJ/C-mol biomass . h). A large set of data has been used including (i) a large range of different organisms (bacteria, yeasts, plant cells), (ii) mixed cultures, (iii) heterotrophic and autotrophic growth, (iv) growth under aerobic and anaerobic conditions, and (v) a large temperature range (5-75 degrees C). It appears that only the temperature has a major influence, with an energy of activation of 69 kJ/mol. Different electron donors or electron acceptors only show a very minor influence on m(E). On the basis of the data set, temperature correlations of m(E) have been derived for aerobic and anaerobic growth. The generalized concept for maintenance Gibbs energy is used to establish a correlation which allows the estimation of the biomass yield on electron donor as a function of C-source, electron donor, electron acceptor, N source, growth rate, and temperature. The advantage of using the m(E) parameter over other maintenance-related parameters (like mu(e), m(O2), m(D), gamma(D)m(D)) is discussed.

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“…A Y CH4 max of ϳ7 g DW mol Ϫ1 of methane, which was adopted when growth proceeded at p H2 Ͼ 12 kPa, has as yet not been reported for M. thermautotrophicus. Importantly, the existence of the two distinct, hydrogen-dependent Y CH4 max values is predicted from a theoretical analysis of the process of methanogenesis presented in in the supplemental material (2). The analysis suggests Y CH4 max values of 3.1 to 3.7 and 6.1 to 7.4 g DW mol of methane Ϫ1 for growth below and above p H2 ϳ 12 kPa, respectively.…”

Section: Discussionmentioning

confidence: 91%

“…Unfortunately, the mechanistic meaning of the maintenance coefficient concept is not very clear either, being often simply defined as "any diversion of energy from growth to non-growth reactions" (22). A theoretical analysis of the process of methane formation suggests that the governing factor in "maintenance" is likely to be proton leakage or proton slippage (see the supplemental material [2). The effect of the uncoupler TCS on the growth behavior (Fig.…”

Section: Discussionmentioning

confidence: 99%

Coupling ofMethanothermobacter thermautotrophicusMethane Formation and Growth in Fed-Batch and Continuous Cultures under Different H₂Gassing Regimens

Poorter

Geerts

Keltjens

2007

Appl Environ Microbiol

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In nature, H 2 -and CO 2 -utilizing methanogenic archaea have to couple the processes of methanogenesis and autotrophic growth under highly variable conditions with respect to the supply and concentration of their energy source, hydrogen. To study the hydrogen-dependent coupling between methanogenesis and growth, Methanothermobacter thermautotrophicus was cultured in a fed-batch fermentor and in a chemostat under different 80% H 2 -20% CO 2 gassing regimens while we continuously monitored the dissolved hydrogen partial pressures (p H2 ). In the fed-batch system, in which the conditions continuously changed the uptake rates by the growing biomass, the organism displayed a complex and yet defined growth behavior, comprising the consecutive lag, exponential, and linear growth phases. It was found that the in situ hydrogen concentration affected the coupling between methanogenesis and growth in at least two respects. (i) The microorganism could adopt two distinct theoretical maximal growth yields (Y CH4 max ), notably approximately 3 and 7 g (dry weight) of methane formed mol ؊1 , for growth under low (p H2 < 12 kPa)-and high-hydrogen conditions, respectively. The distinct values can be understood from a theoretical analysis of the process of methanogenesis presented in the supplemental material associated with this study. (ii) The in situ hydrogen concentration affected the "specific maintenance" requirements or, more likely, the degree of proton leakage and proton slippage processes. At low p H2 values, the "specific maintenance" diminished and the specific growth yields approached Y CH4 max , indicating that growth and methanogenesis became fully coupled.Most methanogenic archaea, including the Methanothermobacter thermautrophicus used in the present study, derive their energy for autotrophic growth from the H 2 -dependent reduction of CO 2 into methane. The pathways of methane formation, CO 2 fixation, and ATP synthesis are highly conserved among the different H 2 -utilizing (hydrogenotrophic) methanogens (for reviews, see references 5, 6, 9, and 32 and additional information in the supplemental material). Nevertheless, different species display remarkable differences in specific growth yields (Y CH4 ), i.e., the amount of biomass formed per mole of methane produced at a given growth condition (Table 1). Y CH4 values can be variable for a given species. Even maximal growth yields (Y CH4 max ) seem to differ. Y CH4 max represents the theoretical maximal growth yield that would be obtained if methanogenesis and growth are fully coupled.Methanogens have to couple the processes of energy generation (methanogenesis) and biomass formation under highly diverse concentrations of their energy source, hydrogen. In environments such as anaerobic sediments and sewage digestors, hydrogen formed by obligate proton reducers is available at only very low levels (11, 37). In contrast, hydrogen concentrations can be high at sites where methanogens obtain the gas from H 2 -producing fermentative microorganisms (29, 37). Under labo...

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Formate-limited growth of Methanobacterium formicium in steady-state cultures

Cited by 21 publications

References 8 publications

Growth- and substrate-dependent transcription of the formate dehydrogenase (fdhCAB) operon in Methanobacterium thermoformicicum Z-245

Growth- and substrate-dependent transcription of the formate dehydrogenase (fdhCAB) operon in Methanobacterium thermoformicicum Z-245

A thermodynamically based correlation for maintenance gibbs energy requirements in aerobic and anaerobic chemotrophic growth

Coupling ofMethanothermobacter thermautotrophicusMethane Formation and Growth in Fed-Batch and Continuous Cultures under Different H₂Gassing Regimens

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Formate-limited growth of Methanobacterium formicium in steady-state cultures

Cited by 21 publications

References 8 publications

Growth- and substrate-dependent transcription of the formate dehydrogenase (fdhCAB) operon in Methanobacterium thermoformicicum Z-245

Growth- and substrate-dependent transcription of the formate dehydrogenase (fdhCAB) operon in Methanobacterium thermoformicicum Z-245

A thermodynamically based correlation for maintenance gibbs energy requirements in aerobic and anaerobic chemotrophic growth

Coupling ofMethanothermobacter thermautotrophicusMethane Formation and Growth in Fed-Batch and Continuous Cultures under Different H2Gassing Regimens

Contact Info

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Resources

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Coupling ofMethanothermobacter thermautotrophicusMethane Formation and Growth in Fed-Batch and Continuous Cultures under Different H₂Gassing Regimens