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The Burkholderia bcpAIOB Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems

Microbes have evolved many strategies to adapt to changes in environmental conditions and population structures, including cooperation and competition. One apparently competitive mechanism is contact dependent growth inhibition (CDI). Identified in Escherichia coli, CDI is mediated by Two–Partner Se...

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Autores principales: Anderson, Melissa S., Garcia, Erin C., Cotter, Peggy A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3415462/
https://www.ncbi.nlm.nih.gov/pubmed/22912595
http://dx.doi.org/10.1371/journal.pgen.1002877
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author Anderson, Melissa S.
Garcia, Erin C.
Cotter, Peggy A.
author_facet Anderson, Melissa S.
Garcia, Erin C.
Cotter, Peggy A.
author_sort Anderson, Melissa S.
collection PubMed
description Microbes have evolved many strategies to adapt to changes in environmental conditions and population structures, including cooperation and competition. One apparently competitive mechanism is contact dependent growth inhibition (CDI). Identified in Escherichia coli, CDI is mediated by Two–Partner Secretion (TPS) pathway proteins, CdiA and CdiB. Upon cell contact, the toxic C-terminus of the TpsA family member CdiA, called the CdiA-CT, inhibits the growth of CDI(−) bacteria. CDI(+) bacteria are protected from autoinhibition by an immunity protein, CdiI. Bioinformatic analyses indicate that CDI systems are widespread amongst α, β, and γ proteobacteria and that the CdiA-CTs and CdiI proteins are highly variable. CdiI proteins protect against CDI in an allele-specific manner. Here we identify predicted CDI system-encoding loci in species of Burkholderia, Ralstonia and Cupriavidus, named bcpAIOB, that are distinguished from previously-described CDI systems by gene order and the presence of a small ORF, bcpO, located 5′ to the gene encoding the TpsB family member. A requirement for bcpO in function of BcpA (the TpsA family member) was demonstrated, indicating that bcpAIOB define a novel class of TPS system. Using fluorescence microscopy and flow cytometry, we show that these genes are expressed in a probabilistic manner during culture of Burkholderia thailandensis in liquid medium. The bcpAIOB genes and extracellular DNA were required for autoaggregation and adherence to an abiotic surface, suggesting that CDI is required for biofilm formation, an activity not previously attributed to CDI. By contrast to what has been observed in E. coli, the B. thailandensis bcpAIOB genes only mediated interbacterial competition on a solid surface. Competition occurred in a defined spatiotemporal manner and was abrogated by allele-specific immunity. Our data indicate that the bcpAIOB genes encode distinct classes of CDI and TPS systems that appear to function in sociomicrobiological community development.
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spelling pubmed-34154622012-08-21 The Burkholderia bcpAIOB Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems Anderson, Melissa S. Garcia, Erin C. Cotter, Peggy A. PLoS Genet Research Article Microbes have evolved many strategies to adapt to changes in environmental conditions and population structures, including cooperation and competition. One apparently competitive mechanism is contact dependent growth inhibition (CDI). Identified in Escherichia coli, CDI is mediated by Two–Partner Secretion (TPS) pathway proteins, CdiA and CdiB. Upon cell contact, the toxic C-terminus of the TpsA family member CdiA, called the CdiA-CT, inhibits the growth of CDI(−) bacteria. CDI(+) bacteria are protected from autoinhibition by an immunity protein, CdiI. Bioinformatic analyses indicate that CDI systems are widespread amongst α, β, and γ proteobacteria and that the CdiA-CTs and CdiI proteins are highly variable. CdiI proteins protect against CDI in an allele-specific manner. Here we identify predicted CDI system-encoding loci in species of Burkholderia, Ralstonia and Cupriavidus, named bcpAIOB, that are distinguished from previously-described CDI systems by gene order and the presence of a small ORF, bcpO, located 5′ to the gene encoding the TpsB family member. A requirement for bcpO in function of BcpA (the TpsA family member) was demonstrated, indicating that bcpAIOB define a novel class of TPS system. Using fluorescence microscopy and flow cytometry, we show that these genes are expressed in a probabilistic manner during culture of Burkholderia thailandensis in liquid medium. The bcpAIOB genes and extracellular DNA were required for autoaggregation and adherence to an abiotic surface, suggesting that CDI is required for biofilm formation, an activity not previously attributed to CDI. By contrast to what has been observed in E. coli, the B. thailandensis bcpAIOB genes only mediated interbacterial competition on a solid surface. Competition occurred in a defined spatiotemporal manner and was abrogated by allele-specific immunity. Our data indicate that the bcpAIOB genes encode distinct classes of CDI and TPS systems that appear to function in sociomicrobiological community development. Public Library of Science 2012-08-09 /pmc/articles/PMC3415462/ /pubmed/22912595 http://dx.doi.org/10.1371/journal.pgen.1002877 Text en © 2012 Anderson 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, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Anderson, Melissa S.
Garcia, Erin C.
Cotter, Peggy A.
The Burkholderia bcpAIOB Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems
title The Burkholderia bcpAIOB Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems
title_full The Burkholderia bcpAIOB Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems
title_fullStr The Burkholderia bcpAIOB Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems
title_full_unstemmed The Burkholderia bcpAIOB Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems
title_short The Burkholderia bcpAIOB Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems
title_sort burkholderia bcpaiob genes define unique classes of two-partner secretion and contact dependent growth inhibition systems
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3415462/
https://www.ncbi.nlm.nih.gov/pubmed/22912595
http://dx.doi.org/10.1371/journal.pgen.1002877
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