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Characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in Bacillus subtilis
The soil bacterium Bacillus subtilis is often found in association with plants in the rhizosphere. Previously, plant polysaccharides have been shown to stimulate formation of root-associated multicellular communities, or biofilms, in this bacterium, yet the underlying mechanism is not fully understo...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5472308/ https://www.ncbi.nlm.nih.gov/pubmed/28617843 http://dx.doi.org/10.1371/journal.pone.0179761 |
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author | Habib, Cameron Yu, Yiyang Gozzi, Kevin Ching, Carly Shemesh, Moshe Chai, Yunrong |
author_facet | Habib, Cameron Yu, Yiyang Gozzi, Kevin Ching, Carly Shemesh, Moshe Chai, Yunrong |
author_sort | Habib, Cameron |
collection | PubMed |
description | The soil bacterium Bacillus subtilis is often found in association with plants in the rhizosphere. Previously, plant polysaccharides have been shown to stimulate formation of root-associated multicellular communities, or biofilms, in this bacterium, yet the underlying mechanism is not fully understood. A five-gene gan operon (ganSPQAB) in B. subtilis has recently been shown to be involved in utilization of the plant-derived polysaccharide galactan. Despite these findings, molecular details about the regulation of the operon and the role of the operon in biofilm formation remain elusive. In this study, we performed comprehensive genetic analyses on the regulation of the gan operon. We show that this operon is regulated both by a LacI-like transcription repressor (GanR), which directly binds to pairs of inverted DNA repeats in the promoter region of the operon, and by the catabolite control protein A (CcpA). Derepression can be triggered by the presence of the inducer β-1,4-galactobiose, a hydrolysis product of galactan, or in situ when B. subtilis cells are associated with plant roots. In addition to the transcriptional regulation, the encoded ß-galactosidase GanA (by ganA), which hydrolyzes ß-1,4-galactobiose into galactose, is inhibited at the enzymatic level by the catalytic product galactose. Thus, the galactan utilization pathway is under complex regulation involving both positive and negative feedback mechanisms in B. subtilis. We discuss about the biological significance of such complex regulation as well as a hypothesis of biofilm induction by galactan via multiple mechanisms. |
format | Online Article Text |
id | pubmed-5472308 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-54723082017-07-03 Characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in Bacillus subtilis Habib, Cameron Yu, Yiyang Gozzi, Kevin Ching, Carly Shemesh, Moshe Chai, Yunrong PLoS One Research Article The soil bacterium Bacillus subtilis is often found in association with plants in the rhizosphere. Previously, plant polysaccharides have been shown to stimulate formation of root-associated multicellular communities, or biofilms, in this bacterium, yet the underlying mechanism is not fully understood. A five-gene gan operon (ganSPQAB) in B. subtilis has recently been shown to be involved in utilization of the plant-derived polysaccharide galactan. Despite these findings, molecular details about the regulation of the operon and the role of the operon in biofilm formation remain elusive. In this study, we performed comprehensive genetic analyses on the regulation of the gan operon. We show that this operon is regulated both by a LacI-like transcription repressor (GanR), which directly binds to pairs of inverted DNA repeats in the promoter region of the operon, and by the catabolite control protein A (CcpA). Derepression can be triggered by the presence of the inducer β-1,4-galactobiose, a hydrolysis product of galactan, or in situ when B. subtilis cells are associated with plant roots. In addition to the transcriptional regulation, the encoded ß-galactosidase GanA (by ganA), which hydrolyzes ß-1,4-galactobiose into galactose, is inhibited at the enzymatic level by the catalytic product galactose. Thus, the galactan utilization pathway is under complex regulation involving both positive and negative feedback mechanisms in B. subtilis. We discuss about the biological significance of such complex regulation as well as a hypothesis of biofilm induction by galactan via multiple mechanisms. Public Library of Science 2017-06-15 /pmc/articles/PMC5472308/ /pubmed/28617843 http://dx.doi.org/10.1371/journal.pone.0179761 Text en © 2017 Habib et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Habib, Cameron Yu, Yiyang Gozzi, Kevin Ching, Carly Shemesh, Moshe Chai, Yunrong Characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in Bacillus subtilis |
title | Characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in Bacillus subtilis |
title_full | Characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in Bacillus subtilis |
title_fullStr | Characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in Bacillus subtilis |
title_full_unstemmed | Characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in Bacillus subtilis |
title_short | Characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in Bacillus subtilis |
title_sort | characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in bacillus subtilis |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5472308/ https://www.ncbi.nlm.nih.gov/pubmed/28617843 http://dx.doi.org/10.1371/journal.pone.0179761 |
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