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...

Full description

Bibliographic Details
Main Authors: Yue Zheng, Huan Wang, Zheng Yu, Fauzi Haroon, Maria E. Hernández, Ludmila Chistoserdova
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