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...
Main Authors: | , , , , , , , |
---|---|
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 |
_version_ | 1819261351573323776 |
---|---|
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. |
first_indexed | 2024-12-23T19:40:25Z |
format | Article |
id | doaj.art-fd7f387516644ef49e3ed47f50aa28d0 |
institution | Directory Open Access Journal |
issn | 2049-2618 |
language | English |
last_indexed | 2024-12-23T19:40:25Z |
publishDate | 2018-01-01 |
publisher | BMC |
record_format | Article |
series | Microbiome |
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 |
work_keys_str_mv | AT deepakkumaresan aerobicproteobacterialmethylotrophsinmovilecavegenomicandmetagenomicanalyses AT jasonstephenson aerobicproteobacterialmethylotrophsinmovilecavegenomicandmetagenomicanalyses AT andrewcdoxey aerobicproteobacterialmethylotrophsinmovilecavegenomicandmetagenomicanalyses AT hinabandukwala aerobicproteobacterialmethylotrophsinmovilecavegenomicandmetagenomicanalyses AT elliotbrooks aerobicproteobacterialmethylotrophsinmovilecavegenomicandmetagenomicanalyses AT alexandrahillebrandvoiculescu aerobicproteobacterialmethylotrophsinmovilecavegenomicandmetagenomicanalyses AT andrewswhiteley aerobicproteobacterialmethylotrophsinmovilecavegenomicandmetagenomicanalyses AT jcolinmurrell aerobicproteobacterialmethylotrophsinmovilecavegenomicandmetagenomicanalyses |