Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria

ABSTRACT Two-component sensory (TCS) systems link microbial physiology to the environment and thus may play key roles in biogeochemical cycles. In this study, we surveyed the TCS systems of 328 diverse marine bacterial species. We identified lifestyle traits such as copiotrophy and diazotrophy that...

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Autores principales:	Noelle A. Held, Matthew R. McIlvin, Dawn M. Moran, Michael T. Laub, Mak A. Saito
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	biogeochemistry cell signaling gene regulation marine microbiology proteomics regulatory network Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/60baea8761ea4d23b08d41fd33c59272
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spelling	oai:doaj.org-article:60baea8761ea4d23b08d41fd33c592722021-12-02T19:46:18ZUnique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria10.1128/mSystems.00317-182379-5077https://doaj.org/article/60baea8761ea4d23b08d41fd33c592722019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00317-18https://doaj.org/toc/2379-5077ABSTRACT Two-component sensory (TCS) systems link microbial physiology to the environment and thus may play key roles in biogeochemical cycles. In this study, we surveyed the TCS systems of 328 diverse marine bacterial species. We identified lifestyle traits such as copiotrophy and diazotrophy that are associated with larger numbers of TCS system genes within the genome. We compared marine bacterial species with 1,152 reference bacterial species from a variety of habitats and found evidence of extra response regulators in marine genomes. Examining the location of TCS genes along the circular bacterial genome, we also found that marine bacteria have a large number of “orphan” genes, as well as many hybrid histidine kinases. The prevalence of “extra” response regulators, orphan genes, and hybrid TCS systems suggests that marine bacteria break with traditional understanding of how TCS systems operate. These trends suggest prevalent regulatory networking, which may allow coordinated physiological responses to multiple environmental signals and may represent a specific adaptation to the marine environment. We examine phylogenetic and lifestyle traits that influence the number and structure of two-component systems in the genome, finding, for example, that a lack of two-component systems is a hallmark of oligotrophy. Finally, in an effort to demonstrate the importance of TCS systems to marine biogeochemistry, we examined the distribution of Prochlorococcus/Synechococcus response regulator PMT9312_0717 in metaproteomes of the tropical South Pacific. We found that this protein’s abundance is related to phosphate concentrations, consistent with a putative role in phosphate regulation. IMPORTANCE Marine microbes must manage variation in their chemical, physical, and biological surroundings. Because they directly link bacterial physiology to environmental changes, TCS systems are crucial to the bacterial cell. This study surveyed TCS systems in a large number of marine bacteria and identified key phylogenetic and lifestyle patterns in environmental sensing. We found evidence that, in comparison with bacteria as a whole, marine organisms have irregular TCS system constructs which might represent an adaptation specific to the marine environment. Additionally, we demonstrate the biogeochemical relevance of TCS systems by correlating the presence of the PMT9312_0717 response regulator protein to phosphate concentrations in the South Pacific. We highlight that despite their potential ecological and biogeochemical relevance, TCS systems have been understudied in the marine ecosystem. This report expands our understanding of the breadth of bacterial TCS systems and how marine bacteria have adapted to survive in their unique environment.Noelle A. HeldMatthew R. McIlvinDawn M. MoranMichael T. LaubMak A. SaitoAmerican Society for Microbiologyarticlebiogeochemistrycell signalinggene regulationmarine microbiologyproteomicsregulatory networkMicrobiologyQR1-502ENmSystems, Vol 4, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	biogeochemistry cell signaling gene regulation marine microbiology proteomics regulatory network Microbiology QR1-502
spellingShingle	biogeochemistry cell signaling gene regulation marine microbiology proteomics regulatory network Microbiology QR1-502 Noelle A. Held Matthew R. McIlvin Dawn M. Moran Michael T. Laub Mak A. Saito Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria
description	ABSTRACT Two-component sensory (TCS) systems link microbial physiology to the environment and thus may play key roles in biogeochemical cycles. In this study, we surveyed the TCS systems of 328 diverse marine bacterial species. We identified lifestyle traits such as copiotrophy and diazotrophy that are associated with larger numbers of TCS system genes within the genome. We compared marine bacterial species with 1,152 reference bacterial species from a variety of habitats and found evidence of extra response regulators in marine genomes. Examining the location of TCS genes along the circular bacterial genome, we also found that marine bacteria have a large number of “orphan” genes, as well as many hybrid histidine kinases. The prevalence of “extra” response regulators, orphan genes, and hybrid TCS systems suggests that marine bacteria break with traditional understanding of how TCS systems operate. These trends suggest prevalent regulatory networking, which may allow coordinated physiological responses to multiple environmental signals and may represent a specific adaptation to the marine environment. We examine phylogenetic and lifestyle traits that influence the number and structure of two-component systems in the genome, finding, for example, that a lack of two-component systems is a hallmark of oligotrophy. Finally, in an effort to demonstrate the importance of TCS systems to marine biogeochemistry, we examined the distribution of Prochlorococcus/Synechococcus response regulator PMT9312_0717 in metaproteomes of the tropical South Pacific. We found that this protein’s abundance is related to phosphate concentrations, consistent with a putative role in phosphate regulation. IMPORTANCE Marine microbes must manage variation in their chemical, physical, and biological surroundings. Because they directly link bacterial physiology to environmental changes, TCS systems are crucial to the bacterial cell. This study surveyed TCS systems in a large number of marine bacteria and identified key phylogenetic and lifestyle patterns in environmental sensing. We found evidence that, in comparison with bacteria as a whole, marine organisms have irregular TCS system constructs which might represent an adaptation specific to the marine environment. Additionally, we demonstrate the biogeochemical relevance of TCS systems by correlating the presence of the PMT9312_0717 response regulator protein to phosphate concentrations in the South Pacific. We highlight that despite their potential ecological and biogeochemical relevance, TCS systems have been understudied in the marine ecosystem. This report expands our understanding of the breadth of bacterial TCS systems and how marine bacteria have adapted to survive in their unique environment.
format	article
author	Noelle A. Held Matthew R. McIlvin Dawn M. Moran Michael T. Laub Mak A. Saito
author_facet	Noelle A. Held Matthew R. McIlvin Dawn M. Moran Michael T. Laub Mak A. Saito
author_sort	Noelle A. Held
title	Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria
title_short	Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria
title_full	Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria
title_fullStr	Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria
title_full_unstemmed	Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria
title_sort	unique patterns and biogeochemical relevance of two-component sensing in marine bacteria
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/60baea8761ea4d23b08d41fd33c59272
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_version_	1718376029164142592

Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria

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