The Relationship Between Microbial Community Structures and Environmental Parameters Revealed by Metagenomic Analysis of Hot Spring Water in the Kirishima Area, Japan

Diverse microorganisms specifically inhabit extreme environments, such as hot springs and deep-sea hydrothermal vents. To test the hypothesis that the microbial community structure is predictable based on environmental factors characteristic of such extreme environments, we conducted correlation ana...

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Main Authors: Eri Nishiyama, Koichi Higashi, Hiroshi Mori, Konomi Suda, Hitomi Nakamura, Soichi Omori, Shigenori Maruyama, Yuichi Hongoh, Ken Kurokawa
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-12-01
Series:Frontiers in Bioengineering and Biotechnology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fbioe.2018.00202/full
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author Eri Nishiyama
Eri Nishiyama
Koichi Higashi
Hiroshi Mori
Konomi Suda
Hitomi Nakamura
Soichi Omori
Shigenori Maruyama
Yuichi Hongoh
Ken Kurokawa
author_facet Eri Nishiyama
Eri Nishiyama
Koichi Higashi
Hiroshi Mori
Konomi Suda
Hitomi Nakamura
Soichi Omori
Shigenori Maruyama
Yuichi Hongoh
Ken Kurokawa
author_sort Eri Nishiyama
collection DOAJ
description Diverse microorganisms specifically inhabit extreme environments, such as hot springs and deep-sea hydrothermal vents. To test the hypothesis that the microbial community structure is predictable based on environmental factors characteristic of such extreme environments, we conducted correlation analyses of microbial taxa/functions and environmental factors using metagenomic and 61 types of physicochemical data of water samples from nine hot springs in the Kirishima area (Kyusyu, Japan), where hot springs with diverse chemical properties are distributed in a relatively narrow area. Our metagenomic analysis revealed that the samples can be classified into two major types dominated by either phylum Crenarchaeota or phylum Aquificae. The correlation analysis showed that Crenarchaeota dominated in nutrient-rich environments with high concentrations of ions and total carbons, whereas Aquificae dominated in nutrient-poor environments with low ion concentrations. These environmental factors were also important explanatory variables in the generalized linear models constructed to predict the abundances of Crenarchaeota or Aquificae. Functional enrichment analysis of genes also revealed that the separation of the two major types is primarily attributable to genes involved in autotrophic carbon fixation, sulfate metabolism and nitrate reduction. Our results suggested that Aquificae and Crenarchaeota play a vital role in the Kirishima hot spring water ecosystem through their metabolic pathways adapted to each environment. Our findings provide a basis to predict microbial community structures in hot springs from environmental parameters, and also provide clues for the exploration of biological resources in extreme environments.
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spelling doaj.art-c513a4f941a445bfa90ffd3880485e4c2022-12-21T22:48:23ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852018-12-01610.3389/fbioe.2018.00202419710The Relationship Between Microbial Community Structures and Environmental Parameters Revealed by Metagenomic Analysis of Hot Spring Water in the Kirishima Area, JapanEri Nishiyama0Eri Nishiyama1Koichi Higashi2Hiroshi Mori3Konomi Suda4Hitomi Nakamura5Soichi Omori6Shigenori Maruyama7Yuichi Hongoh8Ken Kurokawa9Biotechnological Research Support Division, FASMAC Co. Ltd, Kanagawa, JapanDepartment of Biological Information, Tokyo Institute of Technology, Tokyo, JapanCenter for Information Biology, National Institute of Genetics, Shizuoka, JapanCenter for Information Biology, National Institute of Genetics, Shizuoka, JapanInstitute for Geo-Resources and Environment, National Institute of Advanced Industrial Science and Technology, Ibaraki, JapanDepartment of Solid Earth Geochemistry, Japan Agency for Marine-Earth Science and Technology, Yokosuka, JapanFaculty of Liberal Arts, The Open University of Japan, Chiba, JapanDepartment of Earth and Planetary Sciences, Tokyo Institute of Technology, Tokyo, JapanSchool of Life Science and Technology, Tokyo Institute of Technology, Tokyo, JapanCenter for Information Biology, National Institute of Genetics, Shizuoka, JapanDiverse microorganisms specifically inhabit extreme environments, such as hot springs and deep-sea hydrothermal vents. To test the hypothesis that the microbial community structure is predictable based on environmental factors characteristic of such extreme environments, we conducted correlation analyses of microbial taxa/functions and environmental factors using metagenomic and 61 types of physicochemical data of water samples from nine hot springs in the Kirishima area (Kyusyu, Japan), where hot springs with diverse chemical properties are distributed in a relatively narrow area. Our metagenomic analysis revealed that the samples can be classified into two major types dominated by either phylum Crenarchaeota or phylum Aquificae. The correlation analysis showed that Crenarchaeota dominated in nutrient-rich environments with high concentrations of ions and total carbons, whereas Aquificae dominated in nutrient-poor environments with low ion concentrations. These environmental factors were also important explanatory variables in the generalized linear models constructed to predict the abundances of Crenarchaeota or Aquificae. Functional enrichment analysis of genes also revealed that the separation of the two major types is primarily attributable to genes involved in autotrophic carbon fixation, sulfate metabolism and nitrate reduction. Our results suggested that Aquificae and Crenarchaeota play a vital role in the Kirishima hot spring water ecosystem through their metabolic pathways adapted to each environment. Our findings provide a basis to predict microbial community structures in hot springs from environmental parameters, and also provide clues for the exploration of biological resources in extreme environments.https://www.frontiersin.org/article/10.3389/fbioe.2018.00202/fullextreme environmentsenvironmental parametersmicroorganismsmetagenomehot springs
spellingShingle Eri Nishiyama
Eri Nishiyama
Koichi Higashi
Hiroshi Mori
Konomi Suda
Hitomi Nakamura
Soichi Omori
Shigenori Maruyama
Yuichi Hongoh
Ken Kurokawa
The Relationship Between Microbial Community Structures and Environmental Parameters Revealed by Metagenomic Analysis of Hot Spring Water in the Kirishima Area, Japan
Frontiers in Bioengineering and Biotechnology
extreme environments
environmental parameters
microorganisms
metagenome
hot springs
title The Relationship Between Microbial Community Structures and Environmental Parameters Revealed by Metagenomic Analysis of Hot Spring Water in the Kirishima Area, Japan
title_full The Relationship Between Microbial Community Structures and Environmental Parameters Revealed by Metagenomic Analysis of Hot Spring Water in the Kirishima Area, Japan
title_fullStr The Relationship Between Microbial Community Structures and Environmental Parameters Revealed by Metagenomic Analysis of Hot Spring Water in the Kirishima Area, Japan
title_full_unstemmed The Relationship Between Microbial Community Structures and Environmental Parameters Revealed by Metagenomic Analysis of Hot Spring Water in the Kirishima Area, Japan
title_short The Relationship Between Microbial Community Structures and Environmental Parameters Revealed by Metagenomic Analysis of Hot Spring Water in the Kirishima Area, Japan
title_sort relationship between microbial community structures and environmental parameters revealed by metagenomic analysis of hot spring water in the kirishima area japan
topic extreme environments
environmental parameters
microorganisms
metagenome
hot springs
url https://www.frontiersin.org/article/10.3389/fbioe.2018.00202/full
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