A Model <italic toggle="yes">Roseobacter</italic>, <named-content content-type="genus-species">Ruegeria pomeroyi</named-content> DSS-3, Employs a Diffusible Killing Mechanism To Eliminate Competitors

ABSTRACT The Roseobacter clade is a group of alphaproteobacteria that have diverse metabolic and regulatory capabilities. They are abundant in marine environments and have a substantial role in marine ecology and biogeochemistry. However, interactions between roseobacters and other bacterioplankton...

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Autores principales:	Garrett C. Sharpe, Scott M. Gifford, Alecia N. Septer
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	competition marine bacteria roseobacters gamma-butyrolactone roseobacter Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/92a3d7106bb14ef9a385306051270ddb
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spelling	oai:doaj.org-article:92a3d7106bb14ef9a385306051270ddb2021-12-02T18:15:46ZA Model <italic toggle="yes">Roseobacter</italic>, <named-content content-type="genus-species">Ruegeria pomeroyi</named-content> DSS-3, Employs a Diffusible Killing Mechanism To Eliminate Competitors10.1128/mSystems.00443-202379-5077https://doaj.org/article/92a3d7106bb14ef9a385306051270ddb2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00443-20https://doaj.org/toc/2379-5077ABSTRACT The Roseobacter clade is a group of alphaproteobacteria that have diverse metabolic and regulatory capabilities. They are abundant in marine environments and have a substantial role in marine ecology and biogeochemistry. However, interactions between roseobacters and other bacterioplankton have not been extensively explored. In this study, we identify a killing mechanism in the model roseobacter Ruegeria pomeroyi DSS-3 by coculturing it with a group of phylogenetically diverse bacteria. The killing mechanism is diffusible and occurs when cells are grown both on surfaces and in suspension and is dependent on cell density. A screen of random transposon mutants revealed that the killing phenotype, as well as resistance to killing, require genes within an ∼8-kb putative gamma-butyrolactone synthesis gene cluster, which resembles similar pheromone-sensing systems in actinomycetes that regulate secondary metabolite production, including antimicrobials. Transcriptomics revealed the gene cluster is highly upregulated in wild-type DSS-3 compared to a nonkiller mutant when grown in liquid coculture with a roseobacter target. Our findings show that R. pomeroyi has the capability to eliminate closely and distantly related competitors, providing a mechanism to alter the community structure and function in its native habitats. IMPORTANCE Bacteria carry out critical ecological and biogeochemical processes and form the foundations of ecosystems. Identifying the factors that influence microbial community composition and the functional capabilities encoded within them is key to predicting how microbes impact an ecosystem. Because microorganisms must compete for limited space and nutrients to promote their own propagation, they have evolved diverse mechanisms to outcompete or kill competitors. However, the genes and regulatory strategies that promote such competitive abilities are largely underexplored, particularly in free-living marine bacteria. Here, genetics and omics techniques are used to investigate how a model marine bacterium is capable of quickly eliminating natural competitors in coculture. We determined that a previously uncharacterized horizontally acquired gene cluster is required for this bacterium to kill diverse competitors. This work represents an important step toward understanding the mechanisms bacterial populations can use to become dominant members in marine microbial communities.Garrett C. SharpeScott M. GiffordAlecia N. SepterAmerican Society for Microbiologyarticlecompetitionmarine bacteriaroseobactersgamma-butyrolactoneroseobacterMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	competition marine bacteria roseobacters gamma-butyrolactone roseobacter Microbiology QR1-502
spellingShingle	competition marine bacteria roseobacters gamma-butyrolactone roseobacter Microbiology QR1-502 Garrett C. Sharpe Scott M. Gifford Alecia N. Septer A Model <italic toggle="yes">Roseobacter</italic>, <named-content content-type="genus-species">Ruegeria pomeroyi</named-content> DSS-3, Employs a Diffusible Killing Mechanism To Eliminate Competitors
description	ABSTRACT The Roseobacter clade is a group of alphaproteobacteria that have diverse metabolic and regulatory capabilities. They are abundant in marine environments and have a substantial role in marine ecology and biogeochemistry. However, interactions between roseobacters and other bacterioplankton have not been extensively explored. In this study, we identify a killing mechanism in the model roseobacter Ruegeria pomeroyi DSS-3 by coculturing it with a group of phylogenetically diverse bacteria. The killing mechanism is diffusible and occurs when cells are grown both on surfaces and in suspension and is dependent on cell density. A screen of random transposon mutants revealed that the killing phenotype, as well as resistance to killing, require genes within an ∼8-kb putative gamma-butyrolactone synthesis gene cluster, which resembles similar pheromone-sensing systems in actinomycetes that regulate secondary metabolite production, including antimicrobials. Transcriptomics revealed the gene cluster is highly upregulated in wild-type DSS-3 compared to a nonkiller mutant when grown in liquid coculture with a roseobacter target. Our findings show that R. pomeroyi has the capability to eliminate closely and distantly related competitors, providing a mechanism to alter the community structure and function in its native habitats. IMPORTANCE Bacteria carry out critical ecological and biogeochemical processes and form the foundations of ecosystems. Identifying the factors that influence microbial community composition and the functional capabilities encoded within them is key to predicting how microbes impact an ecosystem. Because microorganisms must compete for limited space and nutrients to promote their own propagation, they have evolved diverse mechanisms to outcompete or kill competitors. However, the genes and regulatory strategies that promote such competitive abilities are largely underexplored, particularly in free-living marine bacteria. Here, genetics and omics techniques are used to investigate how a model marine bacterium is capable of quickly eliminating natural competitors in coculture. We determined that a previously uncharacterized horizontally acquired gene cluster is required for this bacterium to kill diverse competitors. This work represents an important step toward understanding the mechanisms bacterial populations can use to become dominant members in marine microbial communities.
format	article
author	Garrett C. Sharpe Scott M. Gifford Alecia N. Septer
author_facet	Garrett C. Sharpe Scott M. Gifford Alecia N. Septer
author_sort	Garrett C. Sharpe
title	A Model <italic toggle="yes">Roseobacter</italic>, <named-content content-type="genus-species">Ruegeria pomeroyi</named-content> DSS-3, Employs a Diffusible Killing Mechanism To Eliminate Competitors
title_short	A Model <italic toggle="yes">Roseobacter</italic>, <named-content content-type="genus-species">Ruegeria pomeroyi</named-content> DSS-3, Employs a Diffusible Killing Mechanism To Eliminate Competitors
title_full	A Model <italic toggle="yes">Roseobacter</italic>, <named-content content-type="genus-species">Ruegeria pomeroyi</named-content> DSS-3, Employs a Diffusible Killing Mechanism To Eliminate Competitors
title_fullStr	A Model <italic toggle="yes">Roseobacter</italic>, <named-content content-type="genus-species">Ruegeria pomeroyi</named-content> DSS-3, Employs a Diffusible Killing Mechanism To Eliminate Competitors
title_full_unstemmed	A Model <italic toggle="yes">Roseobacter</italic>, <named-content content-type="genus-species">Ruegeria pomeroyi</named-content> DSS-3, Employs a Diffusible Killing Mechanism To Eliminate Competitors
title_sort	model <italic toggle="yes">roseobacter</italic>, <named-content content-type="genus-species">ruegeria pomeroyi</named-content> dss-3, employs a diffusible killing mechanism to eliminate competitors
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/92a3d7106bb14ef9a385306051270ddb
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A Model <italic toggle="yes">Roseobacter</italic>, <named-content content-type="genus-species">Ruegeria pomeroyi</named-content> DSS-3, Employs a Diffusible Killing Mechanism To Eliminate Competitors

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