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Shotgun metagenomic sequencing from Manao-Pee cave, Thailand, reveals insight into the microbial community structure and its metabolic potential

BACKGROUND: Due to the cave oligotrophic environment, this habitat presents a challenge for microorganisms to colonize and thrive. However, it has been well documented that microorganisms play important roles in cave development. Survival of microbes in this unique habitat likely involves a broad ra...

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Autores principales: Wiseschart, Apirak, Mhuantong, Wuttichai, Tangphatsornruang, Sithichoke, Chantasingh, Duriya, Pootanakit, Kusol
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6598295/
https://www.ncbi.nlm.nih.gov/pubmed/31248378
http://dx.doi.org/10.1186/s12866-019-1521-8
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author Wiseschart, Apirak
Mhuantong, Wuttichai
Tangphatsornruang, Sithichoke
Chantasingh, Duriya
Pootanakit, Kusol
author_facet Wiseschart, Apirak
Mhuantong, Wuttichai
Tangphatsornruang, Sithichoke
Chantasingh, Duriya
Pootanakit, Kusol
author_sort Wiseschart, Apirak
collection PubMed
description BACKGROUND: Due to the cave oligotrophic environment, this habitat presents a challenge for microorganisms to colonize and thrive. However, it has been well documented that microorganisms play important roles in cave development. Survival of microbes in this unique habitat likely involves a broad range of adaptive capabilities. Recently, cave microbiomes all over the world are of great scientific interest. However, the majority of investigations focused mostly on small subunit ribosomal RNA (16S rRNA) gene, leaving the ecological role of the microbial community largely unknown. Here, we are particularly interested in exploring the taxonomic composition and metabolic potential of microorganisms in soil from Manao-Pee cave, a subterranean limestone cave in the western part of Thailand, by using high-throughput shotgun metagenomic sequencing. RESULTS: From taxonomic composition analysis using ribosomal RNA genes (rRNA), the results confirmed that Actinobacteria (51.2%) and Gammaproteobacteria (24.4%) were the dominant bacterial groups in the cave soil community. Metabolic potential analysis, based on six functional modules of the Kyoto Encyclopedia of Genes and Genomes (KEGG) database, revealed that functional genes involved in microbial metabolisms are highly represented in this community (40.6%). To better understand how microbes thrive under unfavorable cave condition, we focused on microbial energy metabolism. The results showed that microbial genes involved in oxidative phosphorylation were the most dominant (28.8%) in Manao-Pee cave, and were followed by methane metabolism (20.5%), carbon fixation (16.0%), nitrogen metabolism (14.7%), and sulfur metabolism (6.3%). In addition, microbial genes involved in xenobiotic biodegradation (26 pathways) and in production of secondary metabolites (27 pathways) were also identified. CONCLUSION: In addition to providing information on microbial diversity, we also gained insights into microbial adaptations and survival strategies under cave conditions. Based on rRNA genes, the results revealed that bacteria belonging to the Actinobacteria and Gammaproteobacteria were the most abundant in this community. From metabolic potential analysis, energy and nutrient sources that sustain diverse microbial population in this community might be atmospheric gases (methane, carbon dioxide, nitrogen), inorganic sulfur, and xenobiotic compounds. In addition, the presence of biosynthetic pathways of secondary metabolites suggested that they might play important ecological roles in the cave microbiome. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12866-019-1521-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-65982952019-07-11 Shotgun metagenomic sequencing from Manao-Pee cave, Thailand, reveals insight into the microbial community structure and its metabolic potential Wiseschart, Apirak Mhuantong, Wuttichai Tangphatsornruang, Sithichoke Chantasingh, Duriya Pootanakit, Kusol BMC Microbiol Research Article BACKGROUND: Due to the cave oligotrophic environment, this habitat presents a challenge for microorganisms to colonize and thrive. However, it has been well documented that microorganisms play important roles in cave development. Survival of microbes in this unique habitat likely involves a broad range of adaptive capabilities. Recently, cave microbiomes all over the world are of great scientific interest. However, the majority of investigations focused mostly on small subunit ribosomal RNA (16S rRNA) gene, leaving the ecological role of the microbial community largely unknown. Here, we are particularly interested in exploring the taxonomic composition and metabolic potential of microorganisms in soil from Manao-Pee cave, a subterranean limestone cave in the western part of Thailand, by using high-throughput shotgun metagenomic sequencing. RESULTS: From taxonomic composition analysis using ribosomal RNA genes (rRNA), the results confirmed that Actinobacteria (51.2%) and Gammaproteobacteria (24.4%) were the dominant bacterial groups in the cave soil community. Metabolic potential analysis, based on six functional modules of the Kyoto Encyclopedia of Genes and Genomes (KEGG) database, revealed that functional genes involved in microbial metabolisms are highly represented in this community (40.6%). To better understand how microbes thrive under unfavorable cave condition, we focused on microbial energy metabolism. The results showed that microbial genes involved in oxidative phosphorylation were the most dominant (28.8%) in Manao-Pee cave, and were followed by methane metabolism (20.5%), carbon fixation (16.0%), nitrogen metabolism (14.7%), and sulfur metabolism (6.3%). In addition, microbial genes involved in xenobiotic biodegradation (26 pathways) and in production of secondary metabolites (27 pathways) were also identified. CONCLUSION: In addition to providing information on microbial diversity, we also gained insights into microbial adaptations and survival strategies under cave conditions. Based on rRNA genes, the results revealed that bacteria belonging to the Actinobacteria and Gammaproteobacteria were the most abundant in this community. From metabolic potential analysis, energy and nutrient sources that sustain diverse microbial population in this community might be atmospheric gases (methane, carbon dioxide, nitrogen), inorganic sulfur, and xenobiotic compounds. In addition, the presence of biosynthetic pathways of secondary metabolites suggested that they might play important ecological roles in the cave microbiome. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12866-019-1521-8) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-27 /pmc/articles/PMC6598295/ /pubmed/31248378 http://dx.doi.org/10.1186/s12866-019-1521-8 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Wiseschart, Apirak
Mhuantong, Wuttichai
Tangphatsornruang, Sithichoke
Chantasingh, Duriya
Pootanakit, Kusol
Shotgun metagenomic sequencing from Manao-Pee cave, Thailand, reveals insight into the microbial community structure and its metabolic potential
title Shotgun metagenomic sequencing from Manao-Pee cave, Thailand, reveals insight into the microbial community structure and its metabolic potential
title_full Shotgun metagenomic sequencing from Manao-Pee cave, Thailand, reveals insight into the microbial community structure and its metabolic potential
title_fullStr Shotgun metagenomic sequencing from Manao-Pee cave, Thailand, reveals insight into the microbial community structure and its metabolic potential
title_full_unstemmed Shotgun metagenomic sequencing from Manao-Pee cave, Thailand, reveals insight into the microbial community structure and its metabolic potential
title_short Shotgun metagenomic sequencing from Manao-Pee cave, Thailand, reveals insight into the microbial community structure and its metabolic potential
title_sort shotgun metagenomic sequencing from manao-pee cave, thailand, reveals insight into the microbial community structure and its metabolic potential
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6598295/
https://www.ncbi.nlm.nih.gov/pubmed/31248378
http://dx.doi.org/10.1186/s12866-019-1521-8
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