Crenothrix are major methane consumers in stratified lakes

Kirsten Oswald,Carsten J Schubert,Daniela Tienken,Marcel Mm Kuypers,Bernhard Wehrli,Holger Daims,Jana Milucka,Michael Wagner,Jon S Graf,Andreas Brand,Mads Albertsen,Sten Littmann

doi:10.1038/ismej.2017.77

Abstract

Methane-oxidizing bacteria represent a major biological sink for methane and are thus Earth’s natural protection against this potent greenhouse gas. Here we show that in two stratified freshwater lakes a substantial part of upward-diffusing methane was oxidized by filamentous gamma-proteobacteria related to Crenothrix polyspora. These filamentous bacteria have been known as contaminants of drinking water supplies since 1870, but their role in the environmental methane removal has remained unclear. While oxidizing methane, these organisms were assigned an ‘unusual’ methane monooxygenase (MMO), which was only distantly related to ‘classical’ MMO of gamma-proteobacterial methanotrophs. We now correct this assignment and show that Crenothrix encode a typical gamma-proteobacterial PmoA. Stable isotope labeling in combination swith single-cell imaging mass spectrometry revealed methane-dependent growth of the lacustrine Crenothrix with oxygen as well as under oxygen-deficient conditions. Crenothrix genomes encoded pathways for the respiration of oxygen as well as for the reduction of nitrate to N2O. The observed abundance and planktonic growth of Crenothrix suggest that these methanotrophs can act as a relevant biological sink for methane in stratified lakes and should be considered in the context of environmental removal of methane.

Highlights

Freshwater lakes represent large natural sources of methane and contribute more to methane emissions than the oceans despite their comparably smaller area (Bastviken et al, 2004)
We investigated the occurrence and involve- Methane oxidation rates were measured in incubament of these filamentous bacteria in methane tions set up in October 2014, with water from the 7 m oxidation at and below the oxyclines of Lake Rotsee depth, and from 8 m depth
In Lake Zug, the fila- Figures 1d–f). This is much lower than the overall ments were shorter but more consistent in terms of contribution of Crenothrix in Lake Rotsee, which is length, reaching an average length and width of ca. largely due to their lower abundance

Summary

Introduction

Freshwater lakes represent large natural sources of methane and contribute more to methane emissions than the oceans despite their comparably smaller area (Bastviken et al, 2004). Methane-derived carbon by Crenothrix filaments was Overall, in all analyzed incubations from both lakes comparable to that of ‘classical’ unicellular gammatotal Crenothix biovolumes increased over time MOB (13C enrichment of 22 ± 4.8 at % and 29 ± 4.1 at (Supplementary Figure 4b).

Results

Conclusion