Bloom of a denitrifying methanotroph, ‘Candidatus Methylomirabilis limnetica’, in a deep stratified lake

• Published in: Environmental microbiology Vol. 20; no. 7; pp. 2598 - 2614
• Main Authors: Graf, Jon S., Mayr, Magdalena J., Marchant, Hannah K., Tienken, Daniela, Hach, Philipp F., Brand, Andreas, Schubert, Carsten J., Kuypers, Marcel M. M., Milucka, Jana
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01-07-2018; Wiley Subscription Services, Inc
• Subjects: Adaptation; Anoxia; Bacteria; Blooms; Candidatus Methylomirabilis; Denitrification; Freshwater; Freshwater lakes; Gene sequencing; Genes; Genomes; Inland water environment; Methane; Methanotrophic bacteria; Microorganisms; New species; Niches; Nitric oxide; Nitrogen cycle; Oxidation; Redundancy; Streamlining
• ISSN: 1462-2912; 1462-2920
• DOI: 10.1111/1462-2920.14285

Summary
Methanotrophic bacteria represent an important biological filter regulating methane emissions into the atmosphere. Planktonic methanotrophic communities in freshwater lakes are typically dominated by aerobic gamma‐proteobacteria, with a contribution from alpha‐proteobacterial methanotrophs and the NC10 bacteria. The NC10 clade encompasses methanotrophs related to ‘Candidatus Methylomirabilis oxyfera’, which oxidize methane using a unique pathway of denitrification that tentatively produces N2 and O2 from nitric oxide (NO). Here, we describe a new species of the NC10 clade, ‘Ca. Methylomirabilis limnetica’, which dominated the planktonic microbial community in the anoxic depths of the deep stratified Lake Zug in two consecutive years, comprising up to 27% of the total bacterial population. Gene transcripts assigned to ‘Ca. M. limnetica’ constituted up to one third of all metatranscriptomic sequences in situ. The reconstructed genome encoded a complete pathway for methane oxidation, and an incomplete denitrification pathway, including two putative nitric oxide dismutase genes. The genome of ‘Ca. M. limnetica’ exhibited features possibly related to genome streamlining (i.e. less redundancy of key metabolic genes) and adaptation to its planktonic habitat (i.e. gas vesicle genes). We speculate that ‘Ca. M. limnetica’ temporarily bloomed in the lake during non‐steady‐state conditions suggesting a niche for NC10 bacteria in the lacustrine methane and nitrogen cycle.