The Unconventional Cytoplasmic Sensing Mechanism for Ethanol Chemotaxis in <named-content content-type="genus-species">Bacillus subtilis</named-content>

ABSTRACT Motile bacteria sense chemical gradients using chemoreceptors, which consist of distinct sensing and signaling domains. The general model is that the sensing domain binds the chemical and the signaling domain induces the tactic response. Here, we investigated the unconventional sensing mech...

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Autores principales:	Payman Tohidifar, Girija A. Bodhankar, Sichong Pei, C. Keith Cassidy, Hanna E. Walukiewicz, George W. Ordal, Phillip J. Stansfeld, Christopher V. Rao
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	chemotaxis Bacillus subtilis ethanol sensing cytoplasmic sensing chemoreceptor molecular dynamics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/063646b204624a6a963f9fa7b1e17a7b
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spelling	oai:doaj.org-article:063646b204624a6a963f9fa7b1e17a7b2021-11-15T16:19:08ZThe Unconventional Cytoplasmic Sensing Mechanism for Ethanol Chemotaxis in <named-content content-type="genus-species">Bacillus subtilis</named-content>10.1128/mBio.02177-202150-7511https://doaj.org/article/063646b204624a6a963f9fa7b1e17a7b2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02177-20https://doaj.org/toc/2150-7511ABSTRACT Motile bacteria sense chemical gradients using chemoreceptors, which consist of distinct sensing and signaling domains. The general model is that the sensing domain binds the chemical and the signaling domain induces the tactic response. Here, we investigated the unconventional sensing mechanism for ethanol taxis in Bacillus subtilis. Ethanol and other short-chain alcohols are attractants for B. subtilis. Two chemoreceptors, McpB and HemAT, sense these alcohols. In the case of McpB, the signaling domain directly binds ethanol. We were further able to identify a single amino acid residue, Ala431, on the cytoplasmic signaling domain of McpB that, when mutated to serine, reduces taxis to alcohols. Molecular dynamics simulations suggest that the conversion of Ala431 to serine increases coiled-coil packing within the signaling domain, thereby reducing the ability of ethanol to bind between the helices of the signaling domain. In the case of HemAT, the myoglobin-like sensing domain binds ethanol, likely between the helices encapsulating the heme group. Aside from being sensed by an unconventional mechanism, ethanol also differs from many other chemoattractants because it is not metabolized by B. subtilis and is toxic. We propose that B. subtilis uses ethanol and other short-chain alcohols to locate prey, namely, alcohol-producing microorganisms. IMPORTANCE Ethanol is a chemoattractant for Bacillus subtilis even though it is not metabolized and inhibits growth. B. subtilis likely uses ethanol to find ethanol-fermenting microorganisms to utilize as prey. Two chemoreceptors sense ethanol: HemAT and McpB. HemAT’s myoglobin-like sensing domain directly binds ethanol, but the heme group is not involved. McpB is a transmembrane receptor consisting of an extracellular sensing domain and a cytoplasmic signaling domain. While most attractants bind the extracellular sensing domain, we found that ethanol directly binds between intermonomer helices of the cytoplasmic signaling domain of McpB, using a mechanism akin to those identified in many mammalian ethanol-binding proteins. Our results indicate that the sensory repertoire of chemoreceptors extends beyond the sensing domain and can directly involve the signaling domain.Payman TohidifarGirija A. BodhankarSichong PeiC. Keith CassidyHanna E. WalukiewiczGeorge W. OrdalPhillip J. StansfeldChristopher V. RaoAmerican Society for MicrobiologyarticlechemotaxisBacillus subtilisethanol sensingcytoplasmic sensingchemoreceptormolecular dynamicsMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	chemotaxis Bacillus subtilis ethanol sensing cytoplasmic sensing chemoreceptor molecular dynamics Microbiology QR1-502
spellingShingle	chemotaxis Bacillus subtilis ethanol sensing cytoplasmic sensing chemoreceptor molecular dynamics Microbiology QR1-502 Payman Tohidifar Girija A. Bodhankar Sichong Pei C. Keith Cassidy Hanna E. Walukiewicz George W. Ordal Phillip J. Stansfeld Christopher V. Rao The Unconventional Cytoplasmic Sensing Mechanism for Ethanol Chemotaxis in <named-content content-type="genus-species">Bacillus subtilis</named-content>
description	ABSTRACT Motile bacteria sense chemical gradients using chemoreceptors, which consist of distinct sensing and signaling domains. The general model is that the sensing domain binds the chemical and the signaling domain induces the tactic response. Here, we investigated the unconventional sensing mechanism for ethanol taxis in Bacillus subtilis. Ethanol and other short-chain alcohols are attractants for B. subtilis. Two chemoreceptors, McpB and HemAT, sense these alcohols. In the case of McpB, the signaling domain directly binds ethanol. We were further able to identify a single amino acid residue, Ala431, on the cytoplasmic signaling domain of McpB that, when mutated to serine, reduces taxis to alcohols. Molecular dynamics simulations suggest that the conversion of Ala431 to serine increases coiled-coil packing within the signaling domain, thereby reducing the ability of ethanol to bind between the helices of the signaling domain. In the case of HemAT, the myoglobin-like sensing domain binds ethanol, likely between the helices encapsulating the heme group. Aside from being sensed by an unconventional mechanism, ethanol also differs from many other chemoattractants because it is not metabolized by B. subtilis and is toxic. We propose that B. subtilis uses ethanol and other short-chain alcohols to locate prey, namely, alcohol-producing microorganisms. IMPORTANCE Ethanol is a chemoattractant for Bacillus subtilis even though it is not metabolized and inhibits growth. B. subtilis likely uses ethanol to find ethanol-fermenting microorganisms to utilize as prey. Two chemoreceptors sense ethanol: HemAT and McpB. HemAT’s myoglobin-like sensing domain directly binds ethanol, but the heme group is not involved. McpB is a transmembrane receptor consisting of an extracellular sensing domain and a cytoplasmic signaling domain. While most attractants bind the extracellular sensing domain, we found that ethanol directly binds between intermonomer helices of the cytoplasmic signaling domain of McpB, using a mechanism akin to those identified in many mammalian ethanol-binding proteins. Our results indicate that the sensory repertoire of chemoreceptors extends beyond the sensing domain and can directly involve the signaling domain.
format	article
author	Payman Tohidifar Girija A. Bodhankar Sichong Pei C. Keith Cassidy Hanna E. Walukiewicz George W. Ordal Phillip J. Stansfeld Christopher V. Rao
author_facet	Payman Tohidifar Girija A. Bodhankar Sichong Pei C. Keith Cassidy Hanna E. Walukiewicz George W. Ordal Phillip J. Stansfeld Christopher V. Rao
author_sort	Payman Tohidifar
title	The Unconventional Cytoplasmic Sensing Mechanism for Ethanol Chemotaxis in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_short	The Unconventional Cytoplasmic Sensing Mechanism for Ethanol Chemotaxis in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_full	The Unconventional Cytoplasmic Sensing Mechanism for Ethanol Chemotaxis in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_fullStr	The Unconventional Cytoplasmic Sensing Mechanism for Ethanol Chemotaxis in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_full_unstemmed	The Unconventional Cytoplasmic Sensing Mechanism for Ethanol Chemotaxis in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_sort	unconventional cytoplasmic sensing mechanism for ethanol chemotaxis in <named-content content-type="genus-species">bacillus subtilis</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/063646b204624a6a963f9fa7b1e17a7b
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The Unconventional Cytoplasmic Sensing Mechanism for Ethanol Chemotaxis in <named-content content-type="genus-species">Bacillus subtilis</named-content>

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