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Dispensable Methanogenic Energy Metabolism in a Methanogenic Archaeon

ABSTRACT: Biogenic methane formation, methanogenesis, a key process in the global carbon cycle is the only energy metabolism known to sustain growth of the microorganisms employing it, the methanogenic archaea. All known methanogenic pathways converge at the methane-liberating step where also the terminal electron acceptor of methanogenic respiration, the heterodisulfide of coenzyme M and coenzyme B is formed. Carbon monoxide (CO) utilization of Methanosarcina acetivorans is unique in that the organism can shift from methanogenesis towards acetogenesis. Here, we show that M. acetivorans can dispense of methanogenesis for energy conservation completely. By disrupting the methanogenic pathway through targeted mutagenesis, followed by adaptive evolution, a strain capable of sustained growth by CO-dependent acetogenesis was created. Still, a minute flux through the methane-liberating reaction remained essential, which was attributed to the involvement of the heterodisulfide in at least one essential anabolic reaction. Genomic and proteomic analysis showed that substantial metabolic rewiring had occurred in the strain. Most notably, heterodisulfide reductase, the terminal respiratory oxidoreductase was eliminated to funnel the heterodisulfide towards anabolism. These results suggest that the metabolic flexibility of “methanogenic” archaea is much greater than anticipated and open avenues for probing the mechanism of energetic coupling and the crosstalk between catabolism and anabolism.

INSTRUMENT(S): Q Exactive HF

ORGANISM(S): Methanosarcina Acetivorans

SUBMITTER: Nico Jehmlich

LAB HEAD: Nico Jehmlich

PROVIDER: PXD022016 | Pride | 2021-10-05

REPOSITORIES: Pride

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Project description:Methanogenesis allows methanogenic archaea (methanogens) to generate cellular energy for their growth while producing methane. Hydrogenotrophic methanogens thrive on carbon dioxide and molecular hydrogen as sole carbon and energy sources. Thermophilic and hydrogenotrophic Methanothermobacter spp. have been recognized as robust biocatalysts for a circular carbon economy and are now applied in power-to-gas technology. Here, we generated the first manually curated genome-scale metabolic reconstruction for three Methanothermobacter spp.. We investigated differences in growth performance and gas consumption/production of three wild-type strains and one genetically engineered strain in two independent quadruplicate chemostat bioreactor experiments: 1) with molecular hydrogen and carbon dioxide; and 2) with sodium formate. In the first experiment, we found the highest methane production rate for Methanothermobacter thermautotrophicus ΔH, while Methanothermobacter marburgensis Marburg reached the highest biomass growth rate. We collected statistically reliable transcriptomics and proteomics data sets from these steady-state bioreactors, which we integrated within our genome-scale metabolic models. The implementation of an pan-model that contains combined reactions from all three microbes allowed us to perform an interspecies comparison of the complete omics data set. While the observed differences in the growth behavior cannot be fully explained, the comparison enabled us to identify crucial differences in growth-related pathways, such as formate anabolism. In the second experiment, we found stable growth with a M. thermautotrophicus ΔH plasmid-carrying strain on formate with similar performance parameters compared to wild-type Methanothermobacter thermautotrophicus Z-245. The results of the two studies demonstrate the advantages of an integrative approach using fermentation and omics data with genome-scale modeling for the investigation of lesser studied metabolisms, and the biotechnological potential of Methanothermobacter spp. as production platform hosts.

Project description:(iMTD22IC) This model is described in these articles: Casini, I., McCubbin, T., Esquivel-Elizondo, S., Luque, G.G., Evseeva, D., Fink, C., Beblawy, S., Youngblut, N.D., Aristilde, L., Huson, D., Drager, A., Ley, R., Marcellin, E., Angenent, L.T., Molitor, B. 2023. An integrated systems biology approach reveals differences in formate metabolism in the genus Methanothermobacter. Iscience, 26(10). Casini, I., McCubbin, T., Esquivel-Elizondo, S., Luque, G.G., Evseeva, D., Fink, C., Beblawy, S., Youngblut, N.D., Aristilde, L., Huson, D., Drager, A., Ley, R., Marcellin, E., Angenent, L.T., Molitor, B. 2022. An integrated systems-biology platform for power-to-gas technology. bioRxiv, 2022.12.30.522236. Methanogenesis allows methanogenic archaea (methanogens) to generate cellular energy for their growth while producing methane. Hydrogenotrophic methanogens thrive on carbon dioxide and molecular hydrogen as sole carbon and energy sources. Thermophilic and hydrogenotrophic Methanothermobacter spp. have been recognized as robust biocatalysts for a circular carbon economy and are now applied in power-to-gas technology. Here, we generated the first manually curated genome-scale metabolic reconstruction for three Methanothermobacter spp.. We investigated differences in growth performance of three wild-type strains and one genetically engineered strain in two independent chemostat bioreactor experiments, first, with molecular hydrogen and carbon dioxide, and second, with sodium formate. In the first experiment, we found the highest methane production rate for Methanothermobacter thermautotrophicus ΔH, while Methanothermobacter marburgensis Marburg reached the highest biomass growth rate. Transcriptomics and proteomics data sets from these steady-state bioreactors, in combination with the implementation of a pan-model that contains combined reactions from all three microbes, allowed us to perform an interspecies comparison. While the observed differences in the growth behavior cannot be fully explained, the comparison enabled us to identify crucial differences in growth-related pathways such as formate anabolism. In the second experiment, we found stable growth with a M. thermautotrophicus ΔH plasmid-carrying strain on formate with similar performance parameters compared to wild-type Methanothermobacter thermautotrophicus Z-245. The results of the two studies demonstrate the advantages of an integrative approach combining fermentation and omics data with genome-scale modeling to reveal knowledge gaps of archaeal metabolisms and the biotechnological potential of Methanothermobacter spp. as production platform hosts.

Project description:This model is described in these articles: Casini, I., McCubbin, T., Esquivel-Elizondo, S., Luque, G.G., Evseeva, D., Fink, C., Beblawy, S., Youngblut, N.D., Aristilde, L., Huson, D., Drager, A., Ley, R., Marcellin, E., Angenent, L.T., Molitor, B. 2023. An integrated systems biology approach reveals differences in formate metabolism in the genus Methanothermobacter. Iscience, 26(10). Casini, I., McCubbin, T., Esquivel-Elizondo, S., Luque, G.G., Evseeva, D., Fink, C., Beblawy, S., Youngblut, N.D., Aristilde, L., Huson, D., Drager, A., Ley, R., Marcellin, E., Angenent, L.T., Molitor, B. 2022. An integrated systems-biology platform for power-to-gas technology. bioRxiv, 2022.12.30.522236. Methanogenesis allows methanogenic archaea (methanogens) to generate cellular energy for their growth while producing methane. Hydrogenotrophic methanogens thrive on carbon dioxide and molecular hydrogen as sole carbon and energy sources. Thermophilic and hydrogenotrophic Methanothermobacter spp. have been recognized as robust biocatalysts for a circular carbon economy and are now applied in power-to-gas technology. Here, we generated the first manually curated genome-scale metabolic reconstruction for three Methanothermobacter spp.. We investigated differences in growth performance of three wild-type strains and one genetically engineered strain in two independent chemostat bioreactor experiments, first, with molecular hydrogen and carbon dioxide, and second, with sodium formate. In the first experiment, we found the highest methane production rate for Methanothermobacter thermautotrophicus ΔH, while Methanothermobacter marburgensis Marburg reached the highest biomass growth rate. Transcriptomics and proteomics data sets from these steady-state bioreactors, in combination with the implementation of a pan-model that contains combined reactions from all three microbes, allowed us to perform an interspecies comparison. While the observed differences in the growth behavior cannot be fully explained, the comparison enabled us to identify crucial differences in growth-related pathways such as formate anabolism. In the second experiment, we found stable growth with a M. thermautotrophicus ΔH plasmid-carrying strain on formate with similar performance parameters compared to wild-type Methanothermobacter thermautotrophicus Z-245. The results of the two studies demonstrate the advantages of an integrative approach combining fermentation and omics data with genome-scale modeling to reveal knowledge gaps of archaeal metabolisms and the biotechnological potential of Methanothermobacter spp. as production platform hosts.

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	181207_M42_rep1.raw	Raw
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	181207_M42_rep4.raw	Raw
	181207_M42_rep5.raw	Raw

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Dispensable Methanogenic Energy Metabolism in a Methanogenic Archaeon

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