Quorum Quenching of <named-content content-type="genus-species">Nitrobacter winogradskyi</named-content> Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification

ABSTRACT Quorum sensing (QS) is a widespread process in bacteria used to coordinate gene expression with cell density, diffusion dynamics, and spatial distribution through the production of diffusible chemical signals. To date, most studies on QS have focused on model bacteria that are amenable to g...

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Autores principales:	Brett L. Mellbye, Andrew T. Giguere, Peter J. Bottomley, Luis A. Sayavedra-Soto
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Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
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spelling	oai:doaj.org-article:e4f69e9d967648f1bcdb4a5bd15cb8552021-11-15T15:50:16ZQuorum Quenching of <named-content content-type="genus-species">Nitrobacter winogradskyi</named-content> Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification10.1128/mBio.01753-162150-7511https://doaj.org/article/e4f69e9d967648f1bcdb4a5bd15cb8552016-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01753-16https://doaj.org/toc/2150-7511ABSTRACT Quorum sensing (QS) is a widespread process in bacteria used to coordinate gene expression with cell density, diffusion dynamics, and spatial distribution through the production of diffusible chemical signals. To date, most studies on QS have focused on model bacteria that are amenable to genetic manipulation and capable of high growth rates, but many environmentally important bacteria have been overlooked. For example, representatives of proteobacteria that participate in nitrification, the aerobic oxidation of ammonia to nitrate via nitrite, produce QS signals called acyl-homoserine lactones (AHLs). Nitrification emits nitrogen oxide gases (NO, NO2, and N2O), which are potentially hazardous compounds that contribute to global warming. Despite considerable interest in nitrification, the purpose of QS in the physiology/ecology of nitrifying bacteria is poorly understood. Through a quorum quenching approach, we investigated the role of QS in a well-studied AHL-producing nitrite oxidizer, Nitrobacter winogradskyi. We added a recombinant AiiA lactonase to N. winogradskyi cultures to degrade AHLs to prevent their accumulation and to induce a QS-negative phenotype and then used mRNA sequencing (mRNA-Seq) to identify putative QS-controlled genes. Our transcriptome analysis showed that expression of nirK and nirK cluster genes (ncgABC) increased up to 19.9-fold under QS-proficient conditions (minus active lactonase). These data led to us to query if QS influenced nitrogen oxide gas fluxes in N. winogradskyi. Production and consumption of NOx increased and production of N2O decreased under QS-proficient conditions. Quorum quenching transcriptome approaches have broad potential to identify QS-controlled genes and phenotypes in organisms that are not genetically tractable. IMPORTANCE Bacterial cell-cell signaling, or quorum sensing (QS), is a method of bacterial communication and gene regulation that is well studied in bacteria. However, little is known about the purpose of QS in many environmentally important bacteria. Here, we demonstrate quorum quenching coupled with mRNA-Seq to identify QS-controlled genes and phenotypes in Nitrobacter winogradskyi, a nitrite-oxidizing bacterium. Nitrite oxidizers play an important role in the nitrogen cycle though their participation in nitrification, the aerobic oxidation of ammonia to nitrate via nitrite. Our quorum quenching approach revealed that QS influences production and consumption of environmentally important nitrogen oxide gases (NO, NO2, and N2O) in N. winogradskyi. This study demonstrated a novel technique for studying QS in difficult-to-work-with microorganisms and showed that nitrite oxidizers might also contribute to nitrification-dependent production of nitrogen oxide gases that contribute to global warming.Brett L. MellbyeAndrew T. GiguerePeter J. BottomleyLuis A. Sayavedra-SotoAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 5 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Brett L. Mellbye Andrew T. Giguere Peter J. Bottomley Luis A. Sayavedra-Soto Quorum Quenching of <named-content content-type="genus-species">Nitrobacter winogradskyi</named-content> Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification
description	ABSTRACT Quorum sensing (QS) is a widespread process in bacteria used to coordinate gene expression with cell density, diffusion dynamics, and spatial distribution through the production of diffusible chemical signals. To date, most studies on QS have focused on model bacteria that are amenable to genetic manipulation and capable of high growth rates, but many environmentally important bacteria have been overlooked. For example, representatives of proteobacteria that participate in nitrification, the aerobic oxidation of ammonia to nitrate via nitrite, produce QS signals called acyl-homoserine lactones (AHLs). Nitrification emits nitrogen oxide gases (NO, NO2, and N2O), which are potentially hazardous compounds that contribute to global warming. Despite considerable interest in nitrification, the purpose of QS in the physiology/ecology of nitrifying bacteria is poorly understood. Through a quorum quenching approach, we investigated the role of QS in a well-studied AHL-producing nitrite oxidizer, Nitrobacter winogradskyi. We added a recombinant AiiA lactonase to N. winogradskyi cultures to degrade AHLs to prevent their accumulation and to induce a QS-negative phenotype and then used mRNA sequencing (mRNA-Seq) to identify putative QS-controlled genes. Our transcriptome analysis showed that expression of nirK and nirK cluster genes (ncgABC) increased up to 19.9-fold under QS-proficient conditions (minus active lactonase). These data led to us to query if QS influenced nitrogen oxide gas fluxes in N. winogradskyi. Production and consumption of NOx increased and production of N2O decreased under QS-proficient conditions. Quorum quenching transcriptome approaches have broad potential to identify QS-controlled genes and phenotypes in organisms that are not genetically tractable. IMPORTANCE Bacterial cell-cell signaling, or quorum sensing (QS), is a method of bacterial communication and gene regulation that is well studied in bacteria. However, little is known about the purpose of QS in many environmentally important bacteria. Here, we demonstrate quorum quenching coupled with mRNA-Seq to identify QS-controlled genes and phenotypes in Nitrobacter winogradskyi, a nitrite-oxidizing bacterium. Nitrite oxidizers play an important role in the nitrogen cycle though their participation in nitrification, the aerobic oxidation of ammonia to nitrate via nitrite. Our quorum quenching approach revealed that QS influences production and consumption of environmentally important nitrogen oxide gases (NO, NO2, and N2O) in N. winogradskyi. This study demonstrated a novel technique for studying QS in difficult-to-work-with microorganisms and showed that nitrite oxidizers might also contribute to nitrification-dependent production of nitrogen oxide gases that contribute to global warming.
format	article
author	Brett L. Mellbye Andrew T. Giguere Peter J. Bottomley Luis A. Sayavedra-Soto
author_facet	Brett L. Mellbye Andrew T. Giguere Peter J. Bottomley Luis A. Sayavedra-Soto
author_sort	Brett L. Mellbye
title	Quorum Quenching of <named-content content-type="genus-species">Nitrobacter winogradskyi</named-content> Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification
title_short	Quorum Quenching of <named-content content-type="genus-species">Nitrobacter winogradskyi</named-content> Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification
title_full	Quorum Quenching of <named-content content-type="genus-species">Nitrobacter winogradskyi</named-content> Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification
title_fullStr	Quorum Quenching of <named-content content-type="genus-species">Nitrobacter winogradskyi</named-content> Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification
title_full_unstemmed	Quorum Quenching of <named-content content-type="genus-species">Nitrobacter winogradskyi</named-content> Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification
title_sort	quorum quenching of <named-content content-type="genus-species">nitrobacter winogradskyi</named-content> suggests that quorum sensing regulates fluxes of nitrogen oxide(s) during nitrification
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/e4f69e9d967648f1bcdb4a5bd15cb855
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Quorum Quenching of <named-content content-type="genus-species">Nitrobacter winogradskyi</named-content> Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification

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