Bloom of a denitrifying methanotroph, 'Candidatus Methylomirabilis limnetica', in a deep stratified lake.

Jon S Graf,Marcel M M Kuypers,Jana Milucka,Carsten J Schubert,Daniela Tienken,Andreas Brand,Magdalena J Mayr,Philipp F Hach,Hannah K Marchant

doi:10.1111/1462-2920.14285

Abstract

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.

Highlights

Temperate lakes are environments with intense methane cycling
‘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
We give a genomic description of this new putative species ‘Candidatus Methylomirabilis limnetica’, infer its in situ activity from metatranscriptomics and describe the biogeochemical conditions during the sampling period that presumably led to the bloom of this bacterium

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). 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. The reconstructed genome encoded a complete pathway for methane oxidation, and an incomplete denitrification pathway, including two putative nitric oxide dismutase genes. ‘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

Introduction

Results and discussion

Experimental procedures