Structural Basis of Hydrogenotrophic Methanogenesis

Abstract

Most methanogenic archaea use the rudimentary hydrogenotrophic pathway—from CO2 and H2 to methane—as the terminal step of microbial biomass degradation in anoxic habitats. The barely exergonic process that just conserves sufficient energy for a modest lifestyle involves chemically challenging reactions catalyzed by complex enzyme machineries with unique metal-containing cofactors. The basic strategy of the methanogenic energy metabolism is to covalently bind C1 species to the C1 carriers methanofuran, tetrahydromethanopterin, and coenzyme M at different oxidation states. The four reduction reactions from CO2 to methane involve one molybdopterin-based two-electron reduction, two coenzyme F420–based hydride transfers, and one coenzyme F430–based radical process. For energy conservation, one ion-gradient-forming methyl transfer reaction is sufficient, albeit supported by a sophisticated energy-coupling process termed flavin-based electron bifurcation for driving the endergonic CO2 reduction and fixation. Here, we review the knowledge about the structure-based catalytic mechanism of each enzyme of hydrogenotrophic methanogenesis. Expected final online publication date for the Annual Review of Microbiology, Volume 74 is September 8, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Three-megadalton complex of methanogenic electron-bifurcating and CO 2 -fixing enzymes

“…Microbial Protein Structure Group, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany. 2 Redox and Metalloprotein Research Group, Max Planck Institute of Biophysics, 60438 Frankfurt am Main, Germany. 3 Core Facility for Mass Spectrometry and Proteomics, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany.…”

Iron corrosion by methanogenic archaea characterized by stable isotope effects and crust mineralogy

“…In hydrogenotrophic methanogenesis, water is the source of hydrogen in methane for most reactions converting CO 2 to methane. This includes the reduction of methenyltetrahydromethanopterin (methenyl-H 4 MPT) to methylene-H 4 MPT, and of methylene-H 4 MPT to methyl-H 4 MPT, reactions mediated by hydride transfer from reduced coenzyme F 420 (Shima et al, 2020). Although regeneration of F 420 H 2 is catalysed by a hydrogenase, this reaction is subjected to isotope exchange with H 2 O hydrogen (Löffler et al, 2019).…”

“…Although regeneration of F 420 H 2 is catalysed by a hydrogenase, this reaction is subjected to isotope exchange with H 2 O hydrogen (Löffler et al, 2019). H 2 is used directly as a reactant only by H 2 -forming methylene-H 4 MPT dehydrogenase, which is expressed particularly under Ni-limiting conditions (Shima et al, 2020). However, even this reaction, which also involves a hydride transfer, is affected by isotope exchange with water (Klein et al, 1995).…”

A paean to the ineffable Marjory Stephenson

“…However, analysis of clostridial hydrogenase II revealed that it contained no nickel and only iron. These two classes of enzyme differ phylogenetically [42] and to this was added a third broad class of iron-only hydrogenases found so far exclusively in certain methanogenic archaea [43]. The hydrogenases of clostridia and single-celled eukarya such as Chlamydomonas reinhardtii have in common that they lack [NiFe]-hydrogenases.…”