Cargando…

Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities

Methanotrophic verrucomicrobia of the order Methylacidiphilales are known as extremely acidophilic, thermophilic or mesophilic bacteria that inhabit acidic geothermal ecosystems. The occurrence of verrucomicrobial methanotrophs in other types of acidic environments remains an open question. Notably,...

Descripción completa

Detalles Bibliográficos
Autores principales: Dedysh, Svetlana N., Beletsky, Alexey V., Ivanova, Anastasia A., Danilova, Olga V., Begmatov, Shahjahon, Kulichevskaya, Irina S., Mardanov, Andrey V., Ravin, Nikolai V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8706344/
https://www.ncbi.nlm.nih.gov/pubmed/34946166
http://dx.doi.org/10.3390/microorganisms9122566
_version_ 1784622169879216128
author Dedysh, Svetlana N.
Beletsky, Alexey V.
Ivanova, Anastasia A.
Danilova, Olga V.
Begmatov, Shahjahon
Kulichevskaya, Irina S.
Mardanov, Andrey V.
Ravin, Nikolai V.
author_facet Dedysh, Svetlana N.
Beletsky, Alexey V.
Ivanova, Anastasia A.
Danilova, Olga V.
Begmatov, Shahjahon
Kulichevskaya, Irina S.
Mardanov, Andrey V.
Ravin, Nikolai V.
author_sort Dedysh, Svetlana N.
collection PubMed
description Methanotrophic verrucomicrobia of the order Methylacidiphilales are known as extremely acidophilic, thermophilic or mesophilic bacteria that inhabit acidic geothermal ecosystems. The occurrence of verrucomicrobial methanotrophs in other types of acidic environments remains an open question. Notably, Methylacidiphilales-affiliated 16S rRNA gene sequences are commonly retrieved from acidic (pH 3.5–5.5) peatlands. In this study, we compared the patterns of verrucomicrobial diversity in four acidic raised bogs and six neutral fens located in European North Russia. Methylacidiphilales-like 16S rRNA gene reads displaying 83–86% similarity to 16S rRNA gene sequences of currently described verrucomicrobial methanotrophs were recovered exclusively from raised bogs. Laboratory incubation of peat samples with 10% methane for 3 weeks resulted in the pronounced increase of a relative abundance of alphaproteobacterial methanotrophs, while no response was detected for Methylacidiphilales-affiliated bacteria. Three metagenome-assembled genomes (MAGs) of peat-inhabiting Methylacidiphilales bacteria were reconstructed and examined for the presence of genes encoding methane monooxygenase enzymes and autotrophic carbon fixation pathways. None of these genomic determinants were detected in assembled MAGs. Metabolic reconstructions predicted a heterotrophic metabolism, with a potential to hydrolyze several plant-derived polysaccharides. As suggested by our analysis, peat-inhabiting representatives of the Methylacidiphilales are acidophilic aerobic heterotrophs, which comprise a sister family of the methanotrophic Methylacidiphilaceae.
format Online
Article
Text
id pubmed-8706344
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-87063442021-12-25 Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities Dedysh, Svetlana N. Beletsky, Alexey V. Ivanova, Anastasia A. Danilova, Olga V. Begmatov, Shahjahon Kulichevskaya, Irina S. Mardanov, Andrey V. Ravin, Nikolai V. Microorganisms Article Methanotrophic verrucomicrobia of the order Methylacidiphilales are known as extremely acidophilic, thermophilic or mesophilic bacteria that inhabit acidic geothermal ecosystems. The occurrence of verrucomicrobial methanotrophs in other types of acidic environments remains an open question. Notably, Methylacidiphilales-affiliated 16S rRNA gene sequences are commonly retrieved from acidic (pH 3.5–5.5) peatlands. In this study, we compared the patterns of verrucomicrobial diversity in four acidic raised bogs and six neutral fens located in European North Russia. Methylacidiphilales-like 16S rRNA gene reads displaying 83–86% similarity to 16S rRNA gene sequences of currently described verrucomicrobial methanotrophs were recovered exclusively from raised bogs. Laboratory incubation of peat samples with 10% methane for 3 weeks resulted in the pronounced increase of a relative abundance of alphaproteobacterial methanotrophs, while no response was detected for Methylacidiphilales-affiliated bacteria. Three metagenome-assembled genomes (MAGs) of peat-inhabiting Methylacidiphilales bacteria were reconstructed and examined for the presence of genes encoding methane monooxygenase enzymes and autotrophic carbon fixation pathways. None of these genomic determinants were detected in assembled MAGs. Metabolic reconstructions predicted a heterotrophic metabolism, with a potential to hydrolyze several plant-derived polysaccharides. As suggested by our analysis, peat-inhabiting representatives of the Methylacidiphilales are acidophilic aerobic heterotrophs, which comprise a sister family of the methanotrophic Methylacidiphilaceae. MDPI 2021-12-11 /pmc/articles/PMC8706344/ /pubmed/34946166 http://dx.doi.org/10.3390/microorganisms9122566 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Dedysh, Svetlana N.
Beletsky, Alexey V.
Ivanova, Anastasia A.
Danilova, Olga V.
Begmatov, Shahjahon
Kulichevskaya, Irina S.
Mardanov, Andrey V.
Ravin, Nikolai V.
Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities
title Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities
title_full Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities
title_fullStr Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities
title_full_unstemmed Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities
title_short Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities
title_sort peat-inhabiting verrucomicrobia of the order methylacidiphilales do not possess methanotrophic capabilities
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8706344/
https://www.ncbi.nlm.nih.gov/pubmed/34946166
http://dx.doi.org/10.3390/microorganisms9122566
work_keys_str_mv AT dedyshsvetlanan peatinhabitingverrucomicrobiaoftheordermethylacidiphilalesdonotpossessmethanotrophiccapabilities
AT beletskyalexeyv peatinhabitingverrucomicrobiaoftheordermethylacidiphilalesdonotpossessmethanotrophiccapabilities
AT ivanovaanastasiaa peatinhabitingverrucomicrobiaoftheordermethylacidiphilalesdonotpossessmethanotrophiccapabilities
AT danilovaolgav peatinhabitingverrucomicrobiaoftheordermethylacidiphilalesdonotpossessmethanotrophiccapabilities
AT begmatovshahjahon peatinhabitingverrucomicrobiaoftheordermethylacidiphilalesdonotpossessmethanotrophiccapabilities
AT kulichevskayairinas peatinhabitingverrucomicrobiaoftheordermethylacidiphilalesdonotpossessmethanotrophiccapabilities
AT mardanovandreyv peatinhabitingverrucomicrobiaoftheordermethylacidiphilalesdonotpossessmethanotrophiccapabilities
AT ravinnikolaiv peatinhabitingverrucomicrobiaoftheordermethylacidiphilalesdonotpossessmethanotrophiccapabilities