Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments

Abstract Microbial methane oxidation is a major biofilter preventing larger emissions of this powerful greenhouse gas from marine coastal areas into the atmosphere. In these zones, various electron acceptors such as sulfate, metal oxides, nitrate, or oxygen can be used. However, the key microbial pl...

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Main Authors: Paula Dalcin Martins, Anniek deJong, Wytze K. Lenstra, Niels A. G. M. vanHelmond, Caroline P. Slomp, Mike S. M. Jetten, Cornelia U. Welte, Olivia Rasigraf
Format: Article
Language:English
Published: Wiley 2021-02-01
Series:MicrobiologyOpen
Subjects:
Online Access:https://doi.org/10.1002/mbo3.1175
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author Paula Dalcin Martins
Anniek deJong
Wytze K. Lenstra
Niels A. G. M. vanHelmond
Caroline P. Slomp
Mike S. M. Jetten
Cornelia U. Welte
Olivia Rasigraf
author_facet Paula Dalcin Martins
Anniek deJong
Wytze K. Lenstra
Niels A. G. M. vanHelmond
Caroline P. Slomp
Mike S. M. Jetten
Cornelia U. Welte
Olivia Rasigraf
author_sort Paula Dalcin Martins
collection DOAJ
description Abstract Microbial methane oxidation is a major biofilter preventing larger emissions of this powerful greenhouse gas from marine coastal areas into the atmosphere. In these zones, various electron acceptors such as sulfate, metal oxides, nitrate, or oxygen can be used. However, the key microbial players and mechanisms of methane oxidation are poorly understood. In this study, we inoculated a bioreactor with methane‐ and iron‐rich sediments from the Bothnian Sea to investigate microbial methane and iron cycling under low oxygen concentrations. Using metagenomics, we investigated shifts in microbial community composition after approximately 2.5 years of bioreactor operation. Marker genes for methane and iron cycling, as well as respiratory and fermentative metabolism, were identified and used to infer putative microbial metabolism. Metagenome‐assembled genomes representing novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria were recovered and revealed a potential for methane oxidation, organic matter degradation, and iron cycling, respectively. This work brings new hypotheses on the identity and metabolic versatility of microorganisms that may be members of such functional guilds in coastal marine sediments and highlights that microorganisms potentially composing the methane biofilter in these sediments may be more diverse than previously appreciated.
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spelling doaj.art-afa942d1036a40148b0ef10622ae65a02022-12-21T20:47:30ZengWileyMicrobiologyOpen2045-88272021-02-01101n/an/a10.1002/mbo3.1175Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sedimentsPaula Dalcin Martins0Anniek deJong1Wytze K. Lenstra2Niels A. G. M. vanHelmond3Caroline P. Slomp4Mike S. M. Jetten5Cornelia U. Welte6Olivia Rasigraf7Department of Microbiology Radboud University Nijmegen Nijmegen The NetherlandsDepartment of Microbiology Radboud University Nijmegen Nijmegen The NetherlandsNetherlands Earth System Science Centre (NESSC) Utrecht The NetherlandsNetherlands Earth System Science Centre (NESSC) Utrecht The NetherlandsNetherlands Earth System Science Centre (NESSC) Utrecht The NetherlandsDepartment of Microbiology Radboud University Nijmegen Nijmegen The NetherlandsDepartment of Microbiology Radboud University Nijmegen Nijmegen The NetherlandsDepartment of Microbiology Radboud University Nijmegen Nijmegen The NetherlandsAbstract Microbial methane oxidation is a major biofilter preventing larger emissions of this powerful greenhouse gas from marine coastal areas into the atmosphere. In these zones, various electron acceptors such as sulfate, metal oxides, nitrate, or oxygen can be used. However, the key microbial players and mechanisms of methane oxidation are poorly understood. In this study, we inoculated a bioreactor with methane‐ and iron‐rich sediments from the Bothnian Sea to investigate microbial methane and iron cycling under low oxygen concentrations. Using metagenomics, we investigated shifts in microbial community composition after approximately 2.5 years of bioreactor operation. Marker genes for methane and iron cycling, as well as respiratory and fermentative metabolism, were identified and used to infer putative microbial metabolism. Metagenome‐assembled genomes representing novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria were recovered and revealed a potential for methane oxidation, organic matter degradation, and iron cycling, respectively. This work brings new hypotheses on the identity and metabolic versatility of microorganisms that may be members of such functional guilds in coastal marine sediments and highlights that microorganisms potentially composing the methane biofilter in these sediments may be more diverse than previously appreciated.https://doi.org/10.1002/mbo3.1175Bothnian Seacoastal sedimentsiron cyclinglow oxygenmethane oxidationmethanotrophs
spellingShingle Paula Dalcin Martins
Anniek deJong
Wytze K. Lenstra
Niels A. G. M. vanHelmond
Caroline P. Slomp
Mike S. M. Jetten
Cornelia U. Welte
Olivia Rasigraf
Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments
MicrobiologyOpen
Bothnian Sea
coastal sediments
iron cycling
low oxygen
methane oxidation
methanotrophs
title Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments
title_full Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments
title_fullStr Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments
title_full_unstemmed Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments
title_short Enrichment of novel Verrucomicrobia, Bacteroidetes, and Krumholzibacteria in an oxygen‐limited methane‐ and iron‐fed bioreactor inoculated with Bothnian Sea sediments
title_sort enrichment of novel verrucomicrobia bacteroidetes and krumholzibacteria in an oxygen limited methane and iron fed bioreactor inoculated with bothnian sea sediments
topic Bothnian Sea
coastal sediments
iron cycling
low oxygen
methane oxidation
methanotrophs
url https://doi.org/10.1002/mbo3.1175
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