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Despite the versatile metabolic flexibility of Methanosarcinales, no member of this order has been shown to use formate for methanogenesis. In the present study, we identified a cytosolic formate dehydrogenase (FdhAB) present in several Methanosarcinales, likely acquired by independent horizontal gene transfers after an early evolutionary loss, encouraging re\u2010evaluation of our understanding of formate utilization in Methanosarcinales. To explore whether formate\u2010dependent (methyl\u2010reducing or CO\n                    <jats:sub>2<\/jats:sub>\n                    \u2010reducing) methanogenesis can occur in Methanosarcinales, we engineered two different strains of\n                    <jats:italic>Methanosarcina acetivorans<\/jats:italic>\n                    by functionally expressing FdhAB from\n                    <jats:italic>Methanosarcina barkeri<\/jats:italic>\n                    in\u00a0\n                    <jats:italic>M.\u2009acetivorans<\/jats:italic>\n                    . In the first strain,\n                    <jats:italic>fdhAB<\/jats:italic>\n                    was integrated into the\n                    <jats:italic>N<\/jats:italic>\n                    <jats:sup>5<\/jats:sup>\n                    \u2010methyl\u2010 tetrahydrosarcinapterin:coenzyme M methyltransferase (\n                    <jats:italic>mtr<\/jats:italic>\n                    ) operon, making it capable of growing by reducing methanol with electrons from formate. In the second strain,\n                    <jats:italic>fdhAB<\/jats:italic>\n                    was integrated into the F\n                    <jats:sub>420<\/jats:sub>\n                    \u2010reducing hydrogenase (\n                    <jats:italic>frh<\/jats:italic>\n                    ) operon, instead of the\n                    <jats:italic>mtr<\/jats:italic>\n                    operon, enabling its growth with formate as the only source of carbon and energy after adaptive laboratory evolution. In this strain, one CO\n                    <jats:sub>2<\/jats:sub>\n                    is reduced to one methane with electrons from oxidizing four formate to four CO\n                    <jats:sub>2<\/jats:sub>\n                    , a metabolism reported only in methanogens without cytochromes. Although methanogens without cytochromes typically utilize flavin\u2010based electron bifurcation to generate the ferredoxins needed for CO\n                    <jats:sub>2<\/jats:sub>\n                    activation, we hypothesize that, in our engineered strains, reduced ferredoxins are obtained via the\n                    <jats:italic>Rhodobacter<\/jats:italic>\n                    nitrogen fixation complex complex running in reverse. Our work demonstrates formate\u2010dependent methyl\u2010reducing and CO\n                    <jats:sub>2<\/jats:sub>\n                    \u2010reducing methanogenesis in\n                    <jats:italic>M.\u2009acetivorans<\/jats:italic>\n                    that is enabled by the flexible nature of the microbe working in tandem with the nurturing provided.\n                  <\/jats:p>","DOI":"10.1111\/febs.17409","type":"journal-article","created":{"date-parts":[[2025,1,31]],"date-time":"2025-01-31T04:04:37Z","timestamp":1738296277000},"page":"2251-2271","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Nature\n                    <scp>AND<\/scp>\n                    nurture: enabling formate\u2010dependent growth in\n                    <i>Methanosarcina 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