Anaerobic methanotroph ‘Candidatus Methanoperedens nitroreducens’ has a pleomorphic life cycle

‘ Candidatus Methanoperedens’ are anaerobic methanotrophic (ANME) archaea with global importance to methane cycling. Here meta-omics and fluorescence in situ hybridization (FISH) were applied to characterize a bioreactor dominated by ‘ Candidatus Methanoperedens nitroreducens’ performing anaerobic methane oxidation coupled to nitrate reduction. Unexpectedly, FISH revealed the stable co-existence of two ‘Ca . M. nitroreducens’ morphotypes: the archetypal coccobacilli microcolonies and previously unreported planktonic rods. Metagenomic analysis showed that the ‘ Ca . M. nitroreducens’ morphotypes were genomically identical but had distinct gene expression profiles for proteins associated with carbon metabolism, motility and cell division. In addition, a third distinct phenotype was observed, with some coccobacilli ‘ Ca . M. nitroreducens’ storing carbon as polyhydroxyalkanoates. The phenotypic variation of ‘ Ca . M. nitroreducens’ probably aids their survival and dispersal in the face of sub-optimal environmental conditions. These findings further demonstrate the remarkable ability of members of the ‘ Ca . Methanoperedens’ to adapt to their environment. Anaerobic methanotrophic archaea (ANME) are globally distributed methane consumers for which pure cultures are lacking. Here the authors use multi-omics and FISH on a bioreactor enrichment to reveal metabolically and morphologically distinct life stages in a single ANME lineage.