A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in Methylobacter
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 howMethylobacter 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.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 toMethylobacterspecies, may be responsible for the persistence and activity ofmore »
- Authors:
-
[2];
- Central South Univ., Hunan (China); Univ. of Washington, Seattle, WA (United States)
- Univ. of Washington, Seattle, WA (United States)
- Central South Univ., Hunan (China)
- Publication Date:
- Research Org.:
- Univ. of Washington, Seattle, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1626185
- Grant/Contract Number:
- SC0016224
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mSystems
- Additional Journal Information:
- Journal Volume: 5; Journal Issue: 1; Journal ID: ISSN 2379-5077
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology; hypoxia; Methylobacter tundripaludum; nitric oxide; hybrid cluster protein; quorum sensing; tundrenone
Citation Formats
Yu, Zheng, Pesesky, Mitchell, Zhang, Lei, Huang, Jing, Winkler, Mari, and Chistoserdova, Ludmila. A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in Methylobacter. United States: N. p., 2020.
Web. doi:10.1128/msystems.00770-19.
Yu, Zheng, Pesesky, Mitchell, Zhang, Lei, Huang, Jing, Winkler, Mari, & Chistoserdova, Ludmila. A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in Methylobacter. United States. https://doi.org/10.1128/msystems.00770-19
Yu, Zheng, Pesesky, Mitchell, Zhang, Lei, Huang, Jing, Winkler, Mari, and Chistoserdova, Ludmila. Tue .
"A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in Methylobacter". United States. https://doi.org/10.1128/msystems.00770-19. https://www.osti.gov/servlets/purl/1626185.
@article{osti_1626185,
title = {A Complex Interplay between Nitric Oxide, Quorum Sensing, and the Unique Secondary Metabolite Tundrenone Constitutes the Hypoxia Response in Methylobacter},
author = {Yu, Zheng and Pesesky, Mitchell and Zhang, Lei and Huang, Jing and Winkler, Mari and Chistoserdova, Ludmila},
abstractNote = {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 howMethylobacter 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.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 toMethylobacterspecies, 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.},
doi = {10.1128/msystems.00770-19},
journal = {mSystems},
number = 1,
volume = 5,
place = {United States},
year = {Tue Jan 21 00:00:00 EST 2020},
month = {Tue Jan 21 00:00:00 EST 2020}
}
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Cited by: 9 works
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Figures / Tables:
FIG 1: Heat map depicting differential expression of select genes in M. tundripaludum 31/32 under oxic (1 h) and increasingly hypoxic (24 and 48 h) conditions (experiments 1A and B). A single replicate for each experiment is shown. Complete transcriptomics data, including additional replicates, are presented in Tables S1 andmore »
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Metagenomic Binning Recovers a Transcriptionally Active Gammaproteobacterium Linking Methanotrophy to Partial Denitrification in an Anoxic Oxygen Minimum Zone
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