Oral Presentation Australian Microbial Ecology 2022

Discovery of a pleomorphic life cycle in the anaerobic methanotroph ‘Candidatus Methanoperedens nitroreducens’ (#5)

Simon J McIlroy 1 , Andy O Leu 1 , Xueqin Zhang 2 , Rhys Newell 1 , Ben J Woodcroft 1 , Zhiguo Yuan 2 , Shihu Hu 2 , Gene W Tyson 1
  1. Centre for Microbiome Research, Queensland University of Technology, Brisbane, QLD, Australia
  2. Australian Centre for Water and Environmental Biotechnology (ACWEB), Faculty of Engineering, Architecture and Information Technology, University of Queensland, Brisbane, QLD, Australia

Methanoperedenaceae are uncultured anaerobic methanotrophic (ANME) archaea with global importance to methane cycling that are typically found in freshwater sediments. The Methanoperedenaceae are metabolically diverse, with several bioreactor enrichment studies demonstrating their ability to couple the anaerobic oxidation of methane (AOM) to the direct reduction of nitrate and metal oxides as terminal electron acceptors (TEAs)1-4. Comparative genomic analyses recently revealed several species have acquired additional terminal reductases through lateral gene transfer (LGT) events, giving them the genetic potential to utilise selenate, arsenate and elemental sulfur as TEAs5. Interestingly, despite only being reported to grow as microcolonies within flocs, the majority of metagenome assembled genomes (MAGs) for the family possess genes for archaellum5, suggesting a previously undocumented biphasic motile lifestyle for these microorganisms. In the presented study, meta-omics and fluorescence in situ hybridisation (FISH) were applied to characterise a bioreactor dominated by the type species ‘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 the ‘Ca. M. nitroreducens’ likely aids in their survival and dispersal in the face of sub-optimal environmental conditions. The potential ability of ‘Ca. M. nitroreducens’ to immediately respond to fluctuations in their environment, coupled with the reported ability of the Methanoperedenaceae to readily adapt through LGT, likely underpins the success of the family in a range of freshwater environments.

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