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      Crenothrix are major methane consumers in stratified lakes

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          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 N 2O. 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.

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          Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage.

          Anaerobic oxidation of methane (AOM) is critical for controlling the flux of methane from anoxic environments. AOM coupled to iron, manganese and sulphate reduction have been demonstrated in consortia containing anaerobic methanotrophic (ANME) archaea. More recently it has been shown that the bacterium Candidatus 'Methylomirabilis oxyfera' can couple AOM to nitrite reduction through an intra-aerobic methane oxidation pathway. Bioreactors capable of AOM coupled to denitrification have resulted in the enrichment of 'M. oxyfera' and a novel ANME lineage, ANME-2d. However, as 'M. oxyfera' can independently couple AOM to denitrification, the role of ANME-2d in the process is unresolved. Here, a bioreactor fed with nitrate, ammonium and methane was dominated by a single ANME-2d population performing nitrate-driven AOM. Metagenomic, single-cell genomic and metatranscriptomic analyses combined with bioreactor performance and (13)C- and (15)N-labelling experiments show that ANME-2d is capable of independent AOM through reverse methanogenesis using nitrate as the terminal electron acceptor. Comparative analyses reveal that the genes for nitrate reduction were transferred laterally from a bacterial donor, suggesting selection for this novel process within ANME-2d. Nitrite produced by ANME-2d is reduced to dinitrogen gas through a syntrophic relationship with an anaerobic ammonium-oxidizing bacterium, effectively outcompeting 'M. oxyfera' in the system. We propose the name Candidatus 'Methanoperedens nitroreducens' for the ANME-2d population and the family Candidatus 'Methanoperedenaceae' for the ANME-2d lineage. We predict that 'M. nitroreducens' and other members of the 'Methanoperedenaceae' have an important role in linking the global carbon and nitrogen cycles in anoxic environments.
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            Methane emissions from lakes: Dependence of lake characteristics, two regional assessments, and a global estimate

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              Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage

              Bacteria in the 16S rRNA clade SAR86 are among the most abundant uncultivated constituents of microbial assemblages in the surface ocean for which little genomic information is currently available. Bioinformatic techniques were used to assemble two nearly complete genomes from marine metagenomes and single-cell sequencing provided two more partial genomes. Recruitment of metagenomic data shows that these SAR86 genomes substantially increase our knowledge of non-photosynthetic bacteria in the surface ocean. Phylogenomic analyses establish SAR86 as a basal and divergent lineage of γ-proteobacteria, and the individual genomes display a temperature-dependent distribution. Modestly sized at 1.25–1.7 Mbp, the SAR86 genomes lack several pathways for amino-acid and vitamin synthesis as well as sulfate reduction, trends commonly observed in other abundant marine microbes. SAR86 appears to be an aerobic chemoheterotroph with the potential for proteorhodopsin-based ATP generation, though the apparent lack of a retinal biosynthesis pathway may require it to scavenge exogenously-derived pigments to utilize proteorhodopsin. The genomes contain an expanded capacity for the degradation of lipids and carbohydrates acquired using a wealth of tonB-dependent outer membrane receptors. Like the abundant planktonic marine bacterial clade SAR11, SAR86 exhibits metabolic streamlining, but also a distinct carbon compound specialization, possibly avoiding competition.
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                Author and article information

                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group
                1751-7362
                1751-7370
                September 2017
                06 June 2017
                1 September 2017
                : 11
                : 9
                : 2124-2140
                Affiliations
                [1 ]Department of Surface Waters—Research and Management, Eawag, Swiss Federal Institute of Aquatic Science and Technology , Kastanienbaum, Switzerland
                [2 ]Institute of Biogeochemistry and Pollutant Dynamics, ETH Zurich, Department of Environmental Systems Science, Swiss Federal Institute of Technology , Zurich, Switzerland
                [3 ]Department of Biogeochemistry, Max Planck Institute for Marine Microbiology , Bremen, Germany
                [4 ]Department of Chemistry and Bioscience, Center for Microbial Communities, Aalborg University , Aalborg, Denmark
                [5 ]Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry meets Microbiology, University of Vienna , Vienna, Austria
                Author notes
                [* ]Department of Biogeochemistry, Max Planck Institute for Marine Microbiology , Celsiusstrasse 1, Bremen 28359, Germany. E-mail: jmilucka@ 123456mpi-bremen.de
                [6]

                These two authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0001-7029-1972
                http://orcid.org/0000-0002-6151-190X
                http://orcid.org/0000-0002-9778-7684
                Article
                ismej201777
                10.1038/ismej.2017.77
                5563964
                28585934
                5e559547-8546-46e2-acf0-bacdc8cef1df
                Copyright © 2017 The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 04 November 2016
                : 13 April 2017
                : 21 April 2017
                Categories
                Original Article

                Microbiology & Virology
                Microbiology & Virology

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