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Abstract:
In marine sediments the anaerobic oxidation of methane with sulfate as electron
acceptor (AOM) is responsible for the removal of a major part of the greenhouse gas
methane. AOM is performed by consortia of anaerobic methane-oxidizing archaea
(ANME) and their specific partner bacteria. The physiology of these organisms is poorly
understood, which is due to their slow growth with doubling times in the order of
months and the phylogenetic diversity in natural and
in vitro
AOM enrichments. Here
we study sediment-free long-term AOM enrichments that were cultivated from seep
sediments sampled off the Italian Island Elba (20◦C; hereon called E20) and from
hot vents of the Guaymas Basin, Gulf of California, cultivated at 37◦C (G37) or at 50◦C (G50). These enrichments were dominated by consortia of ANME-2 archaea and Seep-SRB2 partner bacteria (E20) or by ANME-1, forming consortia with Seep-SRB2
bacteria (G37) or with bacteria of the HotSeep-1 cluster (G50). We investigate lipid
membrane compositions as possible factors for the different temperature affinities
of the different ANME clades and show autotrophy as characteristic feature for
both ANME clades and their partner bacteria. Although in the absence of additional
substrates methane formation was not observed, methanogenesis from methylated
substrates (methanol and methylamine) could be quickly stimulated in the E20 and
the G37 enrichment. Responsible for methanogenesis are archaea from the genus
Methanohalophilus
and Methanococcoides, which are minor community members
during AOM (1–7h of archaeal 16S rRNA gene amplicons). In the same two cultures
also sulfur disproportionation could be quickly stimulated by addition of zero-valent
colloidal sulfur. The isolated partner bacteria are likewise minor community members
(1–9h of bacterial 16S rRNA gene amplicons), whereas the dominant partner bacteria
(Seep-SRB1a, Seep-SRB2, or HotSeep-1) did not grow on elemental sulfur. Our results
support a functioning of AOM as syntrophic interaction of obligate methanotrophic
archaea that transfer non-molecular reducing equivalents (i.e., via direct interspecies
electron transfer) to obligate sulfate-reducing partner bacteria. Additional katabolic
processes in these enrichments but also in sulfate methane interfaces are likely
performed by minor community members.
