Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses

Abstract Background Movile Cave (Mangalia, Romania) is a unique ecosystem where the food web is sustained by microbial primary production, analogous to deep-sea hydrothermal vents. Specifically, chemoautotrophic microbes deriving energy from the oxidation of hydrogen sulphide and methane form the ba...

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Main Authors: Deepak Kumaresan, Jason Stephenson, Andrew C. Doxey, Hina Bandukwala, Elliot Brooks, Alexandra Hillebrand-Voiculescu, Andrew S. Whiteley, J Colin Murrell
Format: Article
Language:English
Published: BMC 2018-01-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-017-0383-2
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author Deepak Kumaresan
Jason Stephenson
Andrew C. Doxey
Hina Bandukwala
Elliot Brooks
Alexandra Hillebrand-Voiculescu
Andrew S. Whiteley
J Colin Murrell
author_facet Deepak Kumaresan
Jason Stephenson
Andrew C. Doxey
Hina Bandukwala
Elliot Brooks
Alexandra Hillebrand-Voiculescu
Andrew S. Whiteley
J Colin Murrell
author_sort Deepak Kumaresan
collection DOAJ
description Abstract Background Movile Cave (Mangalia, Romania) is a unique ecosystem where the food web is sustained by microbial primary production, analogous to deep-sea hydrothermal vents. Specifically, chemoautotrophic microbes deriving energy from the oxidation of hydrogen sulphide and methane form the basis of the food web. Results Here, we report the isolation of the first methane-oxidizing bacterium from the Movile Cave ecosystem, Candidatus Methylomonas sp. LWB, a new species and representative of Movile Cave microbial mat samples. While previous research has suggested a prevalence of anoxic conditions in deeper lake water and sediment, using small-scale shotgun metagenome sequencing, we show that metabolic genes encoding enzymes for aerobic methylotrophy are prevalent in sediment metagenomes possibly indicating the presence of microoxic conditions. Moreover, this study also indicates that members within the family Gallionellaceae (Sideroxydans and Gallionella) were the dominant taxa within the sediment microbial community, thus suggesting a major role for microaerophilic iron-oxidising bacteria in nutrient cycling within the Movile Cave sediments. Conclusions In this study, based on phylogenetic and metabolic gene surveys of metagenome sequences, the possibility of aerobic microbial processes (i.e., methylotrophy and iron oxidation) within the sediment is indicated. We also highlight significant gaps in our knowledge on biogeochemical cycles within the Movile Cave ecosystem, and the need to further investigate potential feedback mechanisms between microbial communities in both lake sediment and lake water.
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spelling doaj.art-fd7f387516644ef49e3ed47f50aa28d02022-12-21T17:33:40ZengBMCMicrobiome2049-26182018-01-016111010.1186/s40168-017-0383-2Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analysesDeepak Kumaresan0Jason Stephenson1Andrew C. Doxey2Hina Bandukwala3Elliot Brooks4Alexandra Hillebrand-Voiculescu5Andrew S. Whiteley6J Colin Murrell7School of Environmental Sciences, University of East AngliaSchool of Life Sciences, University of WarwickDepartment of Biology, University of WaterlooDepartment of Biology, University of WaterlooSchool of Environmental Sciences, University of East AngliaDepartment of Biospeleology and Karst Edaphobiology, Emil Racovita Institute of SpeleologyUWA School of Agriculture and Environment, University of Western AustraliaSchool of Environmental Sciences, University of East AngliaAbstract Background Movile Cave (Mangalia, Romania) is a unique ecosystem where the food web is sustained by microbial primary production, analogous to deep-sea hydrothermal vents. Specifically, chemoautotrophic microbes deriving energy from the oxidation of hydrogen sulphide and methane form the basis of the food web. Results Here, we report the isolation of the first methane-oxidizing bacterium from the Movile Cave ecosystem, Candidatus Methylomonas sp. LWB, a new species and representative of Movile Cave microbial mat samples. While previous research has suggested a prevalence of anoxic conditions in deeper lake water and sediment, using small-scale shotgun metagenome sequencing, we show that metabolic genes encoding enzymes for aerobic methylotrophy are prevalent in sediment metagenomes possibly indicating the presence of microoxic conditions. Moreover, this study also indicates that members within the family Gallionellaceae (Sideroxydans and Gallionella) were the dominant taxa within the sediment microbial community, thus suggesting a major role for microaerophilic iron-oxidising bacteria in nutrient cycling within the Movile Cave sediments. Conclusions In this study, based on phylogenetic and metabolic gene surveys of metagenome sequences, the possibility of aerobic microbial processes (i.e., methylotrophy and iron oxidation) within the sediment is indicated. We also highlight significant gaps in our knowledge on biogeochemical cycles within the Movile Cave ecosystem, and the need to further investigate potential feedback mechanisms between microbial communities in both lake sediment and lake water.http://link.springer.com/article/10.1186/s40168-017-0383-2Movile caveMethylotrophic bacteriaOne-carbon metabolismMethaneMethanotrophsExtreme ecosystem
spellingShingle Deepak Kumaresan
Jason Stephenson
Andrew C. Doxey
Hina Bandukwala
Elliot Brooks
Alexandra Hillebrand-Voiculescu
Andrew S. Whiteley
J Colin Murrell
Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses
Microbiome
Movile cave
Methylotrophic bacteria
One-carbon metabolism
Methane
Methanotrophs
Extreme ecosystem
title Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses
title_full Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses
title_fullStr Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses
title_full_unstemmed Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses
title_short Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses
title_sort aerobic proteobacterial methylotrophs in movile cave genomic and metagenomic analyses
topic Movile cave
Methylotrophic bacteria
One-carbon metabolism
Methane
Methanotrophs
Extreme ecosystem
url http://link.springer.com/article/10.1186/s40168-017-0383-2
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