Reverse Methanogenesis and Respiration in Methanotrophic Archaea

Abstract

Anaerobic oxidation of methane (AOM) is catalyzed by anaerobic methane-oxidizing archaea (ANME) via a reverse and modified methanogenesis pathway. Methanogens can also reverse the methanogenesis pathway to oxidize methane, but only during net methane production (i.e., "trace methane oxidation"). In turn, ANME can produce methane, but only during net methane oxidation (i.e., enzymatic back flux). Net AOM is exergonic when coupled to an external electron acceptor such as sulfate (ANME-1, ANME-2abc, and ANME-3), nitrate (ANME-2d), or metal (oxides). In this review, the reversibility of the methanogenesis pathway and essential differences between ANME and methanogens are described by combining published information with domain based (meta)genome comparison of archaeal methanotrophs and selected archaea. These differences include abundances and special structure of methyl coenzyme M reductase and of multiheme cytochromes and the presence of menaquinones or methanophenazines. ANME-2a and ANME-2d can use electron acceptors other than sulfate or nitrate for AOM, respectively. Environmental studies suggest that ANME-2d are also involved in sulfate-dependent AOM. ANME-1 seem to use a different mechanism for disposal of electrons and possibly are less versatile in electron acceptors use than ANME-2. Future research will shed light on the molecular basis of reversal of the methanogenic pathway and electron transfer in different ANME types.

Figure 1

Phylogenetic tree of full length archaeal 16S rRNA sequences showing all methanotrophic clades so far described (grey) and other archaeal clades used in our domain based (meta)genome comparison (black). The tree was constructed with the ARB software package (version arb-6.0.1.rev12565) [49] using 2800 sequences from the SILVA SSURef NR 99 database (release 119.1) [50]. Trees were calculated by maximum likelihood analysis (RAxML, PHYML) and the ARB neighbor-joining method with terminal filtering and the Jukes-Cantor correction. Resulting trees were compared manually and a consensus tree was constructed. Sulfolobales as outgroup was removed after tree calculations. The scale bar represents the percentage of changes per nucleotide position.

Figure 2

Hydrogenotrophic methanogenesis in cytochrome containing Methanosarcina barkeri. Black lines represent presence of conversions. See Table 3 for nomenclature.

Figure 3

Methylotrophic methanogenesis in cytochrome containing Methanosarcina barkeri. Black lines represent presence of conversions and red lines indicate reversal of the hydrogenotrophic methanogenic pathway. See Table 3 for nomenclature.

Figure 4

Methanotrophic pathway during S-AOM by ANME-2a [42]. Red lines indicate reversal of the hydrogenotrophic methanogenic pathway. See Table 3 for nomenclature.

Figure 5

Methanotrophic pathway during N-AOM by “Ca. M. nitroreducens” MPEBLZ (ANME-2d) [43]. Red lines indicate reversal of the hydrogenotrophic methanogenic pathway. See Table 3 for nomenclature.

Figure 6

Methanotrophic pathway during S-AOM by ANME-1 [40, 41]. Red lines indicate reversal of the hydrogenotrophic methanogenic pathway, grey lines represent absence of conversions, and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway. See Table 3 for nomenclature.