The Bacillus subtilis chemoreceptor McpC senses multiple ligands using two discrete mechanisms

George D. Glekas, Brendan J. Mulhern, Abigail Kroc, Keegan A. Duelfer, Victor Lei, Christopher V. Rao, George W. Ordal

Research output: Contribution to journalArticle

Abstract

Bacillus subtilis can perform chemotaxis toward all 20 L-amino acids normally found in proteins. Loss of a single chemoreceptor, McpC, was previously found to reduce chemotaxis to 19 of these amino acids. In this study, we investigated the amino acid-sensing mechanism of McpC. We show that McpC alone can support chemotaxis to 17 of these amino acids to varying degrees. Eleven amino acids were found to directly bind the amino-terminal sensing domain of McpC in vitro. Sequence analysis indicates that the McpC sensing domain exhibits a dual Per-Arnt-Sim (PAS) domain structure. Using this structure as a guide, we were able to isolate mutants that suggest that four amino acids (arginine, glutamine, lysine, and methionine) are sensed by an indirect mechanism. We identified four candidate binding lipoproteins associated with amino acid transporters that may function in indirect sensing: ArtP, GlnH, MetQ, and YckB. ArtP was found to bind arginine and lysine; GlnH, glutamine; MetQ, methionine; and YckB, tryptophan. In addition, we found that ArtP, MetQ, and YckB bind the sensing domain of McpC, suggesting that the three participate in the indirect sensing of arginine, lysine, methionine, and possibly tryptophan as well. Taken together, these results further our understanding of amino acid chemotaxis in B. subtilis and gain insight into how a single chemoreceptor is able to sense many amino acids.

Original languageEnglish (US)
Pages (from-to)39412-39418
Number of pages7
JournalJournal of Biological Chemistry
Volume287
Issue number47
DOIs
StatePublished - Nov 16 2012

Fingerprint

Bacilli
Bacillus subtilis
Ligands
Amino Acids
Chemotaxis
Methionine
Lysine
Arginine
Glutamine
Tryptophan
Amino Acid Transport Systems
Lipoproteins
Sequence Analysis

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

The Bacillus subtilis chemoreceptor McpC senses multiple ligands using two discrete mechanisms. / Glekas, George D.; Mulhern, Brendan J.; Kroc, Abigail; Duelfer, Keegan A.; Lei, Victor; Rao, Christopher V.; Ordal, George W.

In: Journal of Biological Chemistry, Vol. 287, No. 47, 16.11.2012, p. 39412-39418.

Research output: Contribution to journalArticle

Glekas, George D. ; Mulhern, Brendan J. ; Kroc, Abigail ; Duelfer, Keegan A. ; Lei, Victor ; Rao, Christopher V. ; Ordal, George W. / The Bacillus subtilis chemoreceptor McpC senses multiple ligands using two discrete mechanisms. In: Journal of Biological Chemistry. 2012 ; Vol. 287, No. 47. pp. 39412-39418.
@article{5070dee70fe4469db2c66284948e0ed3,
title = "The Bacillus subtilis chemoreceptor McpC senses multiple ligands using two discrete mechanisms",
abstract = "Bacillus subtilis can perform chemotaxis toward all 20 L-amino acids normally found in proteins. Loss of a single chemoreceptor, McpC, was previously found to reduce chemotaxis to 19 of these amino acids. In this study, we investigated the amino acid-sensing mechanism of McpC. We show that McpC alone can support chemotaxis to 17 of these amino acids to varying degrees. Eleven amino acids were found to directly bind the amino-terminal sensing domain of McpC in vitro. Sequence analysis indicates that the McpC sensing domain exhibits a dual Per-Arnt-Sim (PAS) domain structure. Using this structure as a guide, we were able to isolate mutants that suggest that four amino acids (arginine, glutamine, lysine, and methionine) are sensed by an indirect mechanism. We identified four candidate binding lipoproteins associated with amino acid transporters that may function in indirect sensing: ArtP, GlnH, MetQ, and YckB. ArtP was found to bind arginine and lysine; GlnH, glutamine; MetQ, methionine; and YckB, tryptophan. In addition, we found that ArtP, MetQ, and YckB bind the sensing domain of McpC, suggesting that the three participate in the indirect sensing of arginine, lysine, methionine, and possibly tryptophan as well. Taken together, these results further our understanding of amino acid chemotaxis in B. subtilis and gain insight into how a single chemoreceptor is able to sense many amino acids.",
author = "Glekas, {George D.} and Mulhern, {Brendan J.} and Abigail Kroc and Duelfer, {Keegan A.} and Victor Lei and Rao, {Christopher V.} and Ordal, {George W.}",
year = "2012",
month = "11",
day = "16",
doi = "10.1074/jbc.M112.413518",
language = "English (US)",
volume = "287",
pages = "39412--39418",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "47",

}

TY - JOUR

T1 - The Bacillus subtilis chemoreceptor McpC senses multiple ligands using two discrete mechanisms

AU - Glekas, George D.

AU - Mulhern, Brendan J.

AU - Kroc, Abigail

AU - Duelfer, Keegan A.

AU - Lei, Victor

AU - Rao, Christopher V.

AU - Ordal, George W.

PY - 2012/11/16

Y1 - 2012/11/16

N2 - Bacillus subtilis can perform chemotaxis toward all 20 L-amino acids normally found in proteins. Loss of a single chemoreceptor, McpC, was previously found to reduce chemotaxis to 19 of these amino acids. In this study, we investigated the amino acid-sensing mechanism of McpC. We show that McpC alone can support chemotaxis to 17 of these amino acids to varying degrees. Eleven amino acids were found to directly bind the amino-terminal sensing domain of McpC in vitro. Sequence analysis indicates that the McpC sensing domain exhibits a dual Per-Arnt-Sim (PAS) domain structure. Using this structure as a guide, we were able to isolate mutants that suggest that four amino acids (arginine, glutamine, lysine, and methionine) are sensed by an indirect mechanism. We identified four candidate binding lipoproteins associated with amino acid transporters that may function in indirect sensing: ArtP, GlnH, MetQ, and YckB. ArtP was found to bind arginine and lysine; GlnH, glutamine; MetQ, methionine; and YckB, tryptophan. In addition, we found that ArtP, MetQ, and YckB bind the sensing domain of McpC, suggesting that the three participate in the indirect sensing of arginine, lysine, methionine, and possibly tryptophan as well. Taken together, these results further our understanding of amino acid chemotaxis in B. subtilis and gain insight into how a single chemoreceptor is able to sense many amino acids.

AB - Bacillus subtilis can perform chemotaxis toward all 20 L-amino acids normally found in proteins. Loss of a single chemoreceptor, McpC, was previously found to reduce chemotaxis to 19 of these amino acids. In this study, we investigated the amino acid-sensing mechanism of McpC. We show that McpC alone can support chemotaxis to 17 of these amino acids to varying degrees. Eleven amino acids were found to directly bind the amino-terminal sensing domain of McpC in vitro. Sequence analysis indicates that the McpC sensing domain exhibits a dual Per-Arnt-Sim (PAS) domain structure. Using this structure as a guide, we were able to isolate mutants that suggest that four amino acids (arginine, glutamine, lysine, and methionine) are sensed by an indirect mechanism. We identified four candidate binding lipoproteins associated with amino acid transporters that may function in indirect sensing: ArtP, GlnH, MetQ, and YckB. ArtP was found to bind arginine and lysine; GlnH, glutamine; MetQ, methionine; and YckB, tryptophan. In addition, we found that ArtP, MetQ, and YckB bind the sensing domain of McpC, suggesting that the three participate in the indirect sensing of arginine, lysine, methionine, and possibly tryptophan as well. Taken together, these results further our understanding of amino acid chemotaxis in B. subtilis and gain insight into how a single chemoreceptor is able to sense many amino acids.

UR - http://www.scopus.com/inward/record.url?scp=84869232446&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84869232446&partnerID=8YFLogxK

U2 - 10.1074/jbc.M112.413518

DO - 10.1074/jbc.M112.413518

M3 - Article

C2 - 23038252

AN - SCOPUS:84869232446

VL - 287

SP - 39412

EP - 39418

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 47

ER -