The <italic toggle="yes">Azospirillum brasilense</italic> Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism

ABSTRACT Bacterial chemotaxis affords motile bacteria the ability to navigate the environment to locate niches for growth and survival. At the molecular level, chemotaxis depends on chemoreceptor signaling arrays that interact with cytoplasmic proteins to control the direction of movement. In Azospi...

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Autores principales:	Elena E. Ganusova, Lam T. Vo, Paul E. Abraham, Lindsey O’Neal Yoder, Robert L. Hettich, Gladys Alexandre
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Azospirillum chemotaxis nitrate assimilation nitrogen fixation RpoN metabolomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ea09864df79d45c091ed900dd2b19131
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spelling	oai:doaj.org-article:ea09864df79d45c091ed900dd2b191312021-12-02T18:20:19ZThe <italic toggle="yes">Azospirillum brasilense</italic> Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism10.1128/mSystems.01354-202379-5077https://doaj.org/article/ea09864df79d45c091ed900dd2b191312021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01354-20https://doaj.org/toc/2379-5077ABSTRACT Bacterial chemotaxis affords motile bacteria the ability to navigate the environment to locate niches for growth and survival. At the molecular level, chemotaxis depends on chemoreceptor signaling arrays that interact with cytoplasmic proteins to control the direction of movement. In Azospirillum brasilense, chemotaxis is mediated by two distinct chemotaxis pathways: Che1 and Che4. Both Che1 and Che4 are critical in the A. brasilense free-living and plant-associated lifestyles. Here, we use whole-cell proteomics and metabolomics to characterize the role of chemotaxis in A. brasilense physiology. We found that mutants lacking CheA1 or CheA4 or both are affected in nonchemotaxis functions, including major changes in transcription, signaling transport, and cell metabolism. We identify specific effects of CheA1 and CheA4 on nitrogen metabolism, including nitrate assimilation and nitrogen fixation, that may depend, at least, on the transcriptional control of rpoN, which encodes RpoN, a global regulator of metabolism, including nitrogen. Consistent with proteomics, the abundance of several nitrogenous compounds (purines, pyrimidines, and amino acids) changed in the metabolomes of the chemotaxis mutants relative to the parental strain. Further, we uncover novel, and yet uncharacterized, layers of transcriptional and posttranscriptional control of nitrogen metabolism regulators. Together, our data reveal roles for CheA1 and CheA4 in linking chemotaxis and nitrogen metabolism, likely through control of global regulatory networks. IMPORTANCE Bacterial chemotaxis is widespread in bacteria, increasing competitiveness in diverse environments and mediating associations with eukaryotic hosts ranging from commensal to beneficial and pathogenic. In most bacteria, chemotaxis signaling is tightly linked to energy metabolism, with this coupling occurring through the sensory input of several energy-sensing chemoreceptors. Here, we show that in A. brasilense the chemotaxis proteins have key roles in modulating nitrogen metabolism, including nitrate assimilation and nitrogen fixation, through novel and yet unknown regulations. These results are significant given that A. brasilense is a model bacterium for plant growth promotion and free-living nitrogen fixation and is used as a bio-inoculant for cereal crops. Chemotaxis signaling in A. brasilense thus links locomotor behaviors to nitrogen metabolism, allowing cells to continuously and reciprocally adjust metabolism and chemotaxis signaling as they navigate gradients.Elena E. GanusovaLam T. VoPaul E. AbrahamLindsey O’Neal YoderRobert L. HettichGladys AlexandreAmerican Society for MicrobiologyarticleAzospirillumchemotaxisnitrate assimilationnitrogen fixationRpoNmetabolomicsMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Azospirillum chemotaxis nitrate assimilation nitrogen fixation RpoN metabolomics Microbiology QR1-502
spellingShingle	Azospirillum chemotaxis nitrate assimilation nitrogen fixation RpoN metabolomics Microbiology QR1-502 Elena E. Ganusova Lam T. Vo Paul E. Abraham Lindsey O’Neal Yoder Robert L. Hettich Gladys Alexandre The <italic toggle="yes">Azospirillum brasilense</italic> Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism
description	ABSTRACT Bacterial chemotaxis affords motile bacteria the ability to navigate the environment to locate niches for growth and survival. At the molecular level, chemotaxis depends on chemoreceptor signaling arrays that interact with cytoplasmic proteins to control the direction of movement. In Azospirillum brasilense, chemotaxis is mediated by two distinct chemotaxis pathways: Che1 and Che4. Both Che1 and Che4 are critical in the A. brasilense free-living and plant-associated lifestyles. Here, we use whole-cell proteomics and metabolomics to characterize the role of chemotaxis in A. brasilense physiology. We found that mutants lacking CheA1 or CheA4 or both are affected in nonchemotaxis functions, including major changes in transcription, signaling transport, and cell metabolism. We identify specific effects of CheA1 and CheA4 on nitrogen metabolism, including nitrate assimilation and nitrogen fixation, that may depend, at least, on the transcriptional control of rpoN, which encodes RpoN, a global regulator of metabolism, including nitrogen. Consistent with proteomics, the abundance of several nitrogenous compounds (purines, pyrimidines, and amino acids) changed in the metabolomes of the chemotaxis mutants relative to the parental strain. Further, we uncover novel, and yet uncharacterized, layers of transcriptional and posttranscriptional control of nitrogen metabolism regulators. Together, our data reveal roles for CheA1 and CheA4 in linking chemotaxis and nitrogen metabolism, likely through control of global regulatory networks. IMPORTANCE Bacterial chemotaxis is widespread in bacteria, increasing competitiveness in diverse environments and mediating associations with eukaryotic hosts ranging from commensal to beneficial and pathogenic. In most bacteria, chemotaxis signaling is tightly linked to energy metabolism, with this coupling occurring through the sensory input of several energy-sensing chemoreceptors. Here, we show that in A. brasilense the chemotaxis proteins have key roles in modulating nitrogen metabolism, including nitrate assimilation and nitrogen fixation, through novel and yet unknown regulations. These results are significant given that A. brasilense is a model bacterium for plant growth promotion and free-living nitrogen fixation and is used as a bio-inoculant for cereal crops. Chemotaxis signaling in A. brasilense thus links locomotor behaviors to nitrogen metabolism, allowing cells to continuously and reciprocally adjust metabolism and chemotaxis signaling as they navigate gradients.
format	article
author	Elena E. Ganusova Lam T. Vo Paul E. Abraham Lindsey O’Neal Yoder Robert L. Hettich Gladys Alexandre
author_facet	Elena E. Ganusova Lam T. Vo Paul E. Abraham Lindsey O’Neal Yoder Robert L. Hettich Gladys Alexandre
author_sort	Elena E. Ganusova
title	The <italic toggle="yes">Azospirillum brasilense</italic> Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism
title_short	The <italic toggle="yes">Azospirillum brasilense</italic> Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism
title_full	The <italic toggle="yes">Azospirillum brasilense</italic> Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism
title_fullStr	The <italic toggle="yes">Azospirillum brasilense</italic> Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism
title_full_unstemmed	The <italic toggle="yes">Azospirillum brasilense</italic> Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism
title_sort	<italic toggle="yes">azospirillum brasilense</italic> core chemotaxis proteins chea1 and chea4 link chemotaxis signaling with nitrogen metabolism
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/ea09864df79d45c091ed900dd2b19131
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The <italic toggle="yes">Azospirillum brasilense</italic> Core Chemotaxis Proteins CheA1 and CheA4 Link Chemotaxis Signaling with Nitrogen Metabolism

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