A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in <italic toggle="yes">Methylobacter</italic>

ABSTRACT Methylobacter species, members of the Methylococcales, have recently emerged as some of the globally widespread, cosmopolitan species that play a key role in the environmental consumption of methane across gradients of dioxygen tensions. In this work, we approached the question of how Methy...

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Autores principales:	Zheng Yu, Mitchell Pesesky, Lei Zhang, Jing Huang, Mari Winkler, Ludmila Chistoserdova
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	hypoxia Methylobacter tundripaludum nitric oxide hybrid cluster protein quorum sensing tundrenone Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/69ecf7b466dc414f85e90c7c0e1f2c66
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spelling	oai:doaj.org-article:69ecf7b466dc414f85e90c7c0e1f2c662021-12-02T18:25:17ZA Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in <italic toggle="yes">Methylobacter</italic>10.1128/mSystems.00770-192379-5077https://doaj.org/article/69ecf7b466dc414f85e90c7c0e1f2c662020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00770-19https://doaj.org/toc/2379-5077ABSTRACT Methylobacter species, members of the Methylococcales, have recently emerged as some of the globally widespread, cosmopolitan species that play a key role in the environmental consumption of methane across gradients of dioxygen tensions. In this work, we approached the question of how Methylobacter copes with hypoxia, via laboratory manipulation. Through comparative transcriptomics of cultures grown under high dioxygen partial pressure versus cultures exposed to hypoxia, we identified a gene cluster encoding a hybrid cluster protein along with sensing and regulatory functions. Through mutant analysis, we demonstrated that this gene cluster is involved in the hypoxia stress response. Through additional transcriptomic analyses, we uncovered a complex interconnection between the NO-mediated stress response, quorum sensing, the secondary metabolite tundrenone, and methanol dehydrogenase functions. This novel and complex hypoxia stress response system is so far unique to Methylobacter species, and it may play a role in the environmental fitness of these organisms and in their cosmopolitan environmental distribution. IMPORTANCE Here, we describe a novel and complex hypoxia response system in a methanotrophic bacterium that involves modules of central carbon metabolism, denitrification, quorum sensing, and a secondary metabolite, tundrenone. This intricate stress response system, so far unique to Methylobacter species, may be responsible for the persistence and activity of these species across gradients of dioxygen tensions and for the cosmopolitan distribution of these organisms in freshwater and soil environments in the Northern Hemisphere, including the fast-melting permafrosts.Zheng YuMitchell PeseskyLei ZhangJing HuangMari WinklerLudmila ChistoserdovaAmerican Society for MicrobiologyarticlehypoxiaMethylobacter tundripaludumnitric oxidehybrid cluster proteinquorum sensingtundrenoneMicrobiologyQR1-502ENmSystems, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	hypoxia Methylobacter tundripaludum nitric oxide hybrid cluster protein quorum sensing tundrenone Microbiology QR1-502
spellingShingle	hypoxia Methylobacter tundripaludum nitric oxide hybrid cluster protein quorum sensing tundrenone Microbiology QR1-502 Zheng Yu Mitchell Pesesky Lei Zhang Jing Huang Mari Winkler Ludmila Chistoserdova A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in <italic toggle="yes">Methylobacter</italic>
description	ABSTRACT Methylobacter species, members of the Methylococcales, have recently emerged as some of the globally widespread, cosmopolitan species that play a key role in the environmental consumption of methane across gradients of dioxygen tensions. In this work, we approached the question of how Methylobacter copes with hypoxia, via laboratory manipulation. Through comparative transcriptomics of cultures grown under high dioxygen partial pressure versus cultures exposed to hypoxia, we identified a gene cluster encoding a hybrid cluster protein along with sensing and regulatory functions. Through mutant analysis, we demonstrated that this gene cluster is involved in the hypoxia stress response. Through additional transcriptomic analyses, we uncovered a complex interconnection between the NO-mediated stress response, quorum sensing, the secondary metabolite tundrenone, and methanol dehydrogenase functions. This novel and complex hypoxia stress response system is so far unique to Methylobacter species, and it may play a role in the environmental fitness of these organisms and in their cosmopolitan environmental distribution. IMPORTANCE Here, we describe a novel and complex hypoxia response system in a methanotrophic bacterium that involves modules of central carbon metabolism, denitrification, quorum sensing, and a secondary metabolite, tundrenone. This intricate stress response system, so far unique to Methylobacter species, may be responsible for the persistence and activity of these species across gradients of dioxygen tensions and for the cosmopolitan distribution of these organisms in freshwater and soil environments in the Northern Hemisphere, including the fast-melting permafrosts.
format	article
author	Zheng Yu Mitchell Pesesky Lei Zhang Jing Huang Mari Winkler Ludmila Chistoserdova
author_facet	Zheng Yu Mitchell Pesesky Lei Zhang Jing Huang Mari Winkler Ludmila Chistoserdova
author_sort	Zheng Yu
title	A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in <italic toggle="yes">Methylobacter</italic>
title_short	A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in <italic toggle="yes">Methylobacter</italic>
title_full	A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in <italic toggle="yes">Methylobacter</italic>
title_fullStr	A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in <italic toggle="yes">Methylobacter</italic>
title_full_unstemmed	A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in <italic toggle="yes">Methylobacter</italic>
title_sort	complex interplay between nitric oxide, quorum sensing, and the unique secondary metabolite tundrenone constitutes the hypoxia response in <italic toggle="yes">methylobacter</italic>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/69ecf7b466dc414f85e90c7c0e1f2c66
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A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in <italic toggle="yes">Methylobacter</italic>

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