Metagenomic Insight into Environmentally Challenged Methane-Fed Microbial Communities
In this study, we aimed to investigate, through high-resolution metagenomics and metatranscriptomics, the composition and the trajectories of microbial communities originating from a natural sample, fed exclusively with methane, over 14 weeks of laboratory incubation. This study builds on our prior...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2020-10-01
|
Series: | Microorganisms |
Subjects: | |
Online Access: | https://www.mdpi.com/2076-2607/8/10/1614 |
_version_ | 1797550380014370816 |
---|---|
author | Yue Zheng Huan Wang Zheng Yu Fauzi Haroon Maria E. Hernández Ludmila Chistoserdova |
author_facet | Yue Zheng Huan Wang Zheng Yu Fauzi Haroon Maria E. Hernández Ludmila Chistoserdova |
author_sort | Yue Zheng |
collection | DOAJ |
description | In this study, we aimed to investigate, through high-resolution metagenomics and metatranscriptomics, the composition and the trajectories of microbial communities originating from a natural sample, fed exclusively with methane, over 14 weeks of laboratory incubation. This study builds on our prior data, suggesting that multiple functional guilds feed on methane, likely through guild-to-guild carbon transfer, and potentially through intraguild and intraspecies interactions. We observed that, under two simulated dioxygen partial pressures—low versus high—community trajectories were different, with considerable variability among the replicates. In all microcosms, four major functional guilds were prominently present, representing <i>Methylococcaceae</i> (the true methanotrophs), <i>Methylophilaceae</i> (the nonmethanotrophic methylotrophs), Burkholderiales, and Bacteroidetes. Additional functional guilds were detected in multiple samples, such as members of Opitutae, as well as the predatory species, suggesting additional complexity for methane-oxidizing communities. Metatranscriptomic analysis suggested simultaneous expression of the two alternative types of methanol dehydrogenases in both <i>Methylococcaceae</i> and <i>Methylophilaceae</i>, while high expression of the oxidative/nitrosative stress response genes suggested competition for dioxygen among the community members. The transcriptomic analysis further suggested that Burkholderiales likely feed on acetate that is produced by <i>Methylococcaceae</i> under hypoxic conditions, while Bacteroidetes likely feed on biopolymers produced by both <i>Methylococcaceae</i> and <i>Methylophilaceae</i>. |
first_indexed | 2024-03-10T15:28:27Z |
format | Article |
id | doaj.art-4127b3d10e614506847d9b1bd9069d3a |
institution | Directory Open Access Journal |
issn | 2076-2607 |
language | English |
last_indexed | 2024-03-10T15:28:27Z |
publishDate | 2020-10-01 |
publisher | MDPI AG |
record_format | Article |
series | Microorganisms |
spelling | doaj.art-4127b3d10e614506847d9b1bd9069d3a2023-11-20T17:51:56ZengMDPI AGMicroorganisms2076-26072020-10-01810161410.3390/microorganisms8101614Metagenomic Insight into Environmentally Challenged Methane-Fed Microbial CommunitiesYue Zheng0Huan Wang1Zheng Yu2Fauzi Haroon3Maria E. Hernández4Ludmila Chistoserdova5CAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, ChinaCAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, ChinaDepartment of Chemical Engineering, University of Washington, Seattle, WA 98195, USADepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USADepartment of Chemical Engineering, University of Washington, Seattle, WA 98195, USADepartment of Chemical Engineering, University of Washington, Seattle, WA 98195, USAIn this study, we aimed to investigate, through high-resolution metagenomics and metatranscriptomics, the composition and the trajectories of microbial communities originating from a natural sample, fed exclusively with methane, over 14 weeks of laboratory incubation. This study builds on our prior data, suggesting that multiple functional guilds feed on methane, likely through guild-to-guild carbon transfer, and potentially through intraguild and intraspecies interactions. We observed that, under two simulated dioxygen partial pressures—low versus high—community trajectories were different, with considerable variability among the replicates. In all microcosms, four major functional guilds were prominently present, representing <i>Methylococcaceae</i> (the true methanotrophs), <i>Methylophilaceae</i> (the nonmethanotrophic methylotrophs), Burkholderiales, and Bacteroidetes. Additional functional guilds were detected in multiple samples, such as members of Opitutae, as well as the predatory species, suggesting additional complexity for methane-oxidizing communities. Metatranscriptomic analysis suggested simultaneous expression of the two alternative types of methanol dehydrogenases in both <i>Methylococcaceae</i> and <i>Methylophilaceae</i>, while high expression of the oxidative/nitrosative stress response genes suggested competition for dioxygen among the community members. The transcriptomic analysis further suggested that Burkholderiales likely feed on acetate that is produced by <i>Methylococcaceae</i> under hypoxic conditions, while Bacteroidetes likely feed on biopolymers produced by both <i>Methylococcaceae</i> and <i>Methylophilaceae</i>.https://www.mdpi.com/2076-2607/8/10/1614methanotrophic communitiesmicrocosm incubationmetagenomicsmetatranscriptomics<i>Methylococcaceae</i><i>Methylophilaceae</i> |
spellingShingle | Yue Zheng Huan Wang Zheng Yu Fauzi Haroon Maria E. Hernández Ludmila Chistoserdova Metagenomic Insight into Environmentally Challenged Methane-Fed Microbial Communities Microorganisms methanotrophic communities microcosm incubation metagenomics metatranscriptomics <i>Methylococcaceae</i> <i>Methylophilaceae</i> |
title | Metagenomic Insight into Environmentally Challenged Methane-Fed Microbial Communities |
title_full | Metagenomic Insight into Environmentally Challenged Methane-Fed Microbial Communities |
title_fullStr | Metagenomic Insight into Environmentally Challenged Methane-Fed Microbial Communities |
title_full_unstemmed | Metagenomic Insight into Environmentally Challenged Methane-Fed Microbial Communities |
title_short | Metagenomic Insight into Environmentally Challenged Methane-Fed Microbial Communities |
title_sort | metagenomic insight into environmentally challenged methane fed microbial communities |
topic | methanotrophic communities microcosm incubation metagenomics metatranscriptomics <i>Methylococcaceae</i> <i>Methylophilaceae</i> |
url | https://www.mdpi.com/2076-2607/8/10/1614 |
work_keys_str_mv | AT yuezheng metagenomicinsightintoenvironmentallychallengedmethanefedmicrobialcommunities AT huanwang metagenomicinsightintoenvironmentallychallengedmethanefedmicrobialcommunities AT zhengyu metagenomicinsightintoenvironmentallychallengedmethanefedmicrobialcommunities AT fauziharoon metagenomicinsightintoenvironmentallychallengedmethanefedmicrobialcommunities AT mariaehernandez metagenomicinsightintoenvironmentallychallengedmethanefedmicrobialcommunities AT ludmilachistoserdova metagenomicinsightintoenvironmentallychallengedmethanefedmicrobialcommunities |