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Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism

Biofilms are dense microbial communities. Although widely distributed and medically important, how biofilm cells interact with one another is poorly understood. Recently, we described a novel process whereby myxobacterial biofilm cells exchange their outer membrane (OM) lipoproteins. For the first t...

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Autores principales: Pathak, Darshankumar T., Wei, Xueming, Bucuvalas, Alex, Haft, Daniel H., Gerloff, Dietlind L., Wall, Daniel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3325183/
https://www.ncbi.nlm.nih.gov/pubmed/22511878
http://dx.doi.org/10.1371/journal.pgen.1002626
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author Pathak, Darshankumar T.
Wei, Xueming
Bucuvalas, Alex
Haft, Daniel H.
Gerloff, Dietlind L.
Wall, Daniel
author_facet Pathak, Darshankumar T.
Wei, Xueming
Bucuvalas, Alex
Haft, Daniel H.
Gerloff, Dietlind L.
Wall, Daniel
author_sort Pathak, Darshankumar T.
collection PubMed
description Biofilms are dense microbial communities. Although widely distributed and medically important, how biofilm cells interact with one another is poorly understood. Recently, we described a novel process whereby myxobacterial biofilm cells exchange their outer membrane (OM) lipoproteins. For the first time we report here the identification of two host proteins, TraAB, required for transfer. These proteins are predicted to localize in the cell envelope; and TraA encodes a distant PA14 lectin-like domain, a cysteine-rich tandem repeat region, and a putative C-terminal protein sorting tag named MYXO-CTERM, while TraB encodes an OmpA-like domain. Importantly, TraAB are required in donors and recipients, suggesting bidirectional transfer. By use of a lipophilic fluorescent dye, we also discovered that OM lipids are exchanged. Similar to lipoproteins, dye transfer requires TraAB function, gliding motility and a structured biofilm. Importantly, OM exchange was found to regulate swarming and development behaviors, suggesting a new role in cell–cell communication. A working model proposes TraA is a cell surface receptor that mediates cell–cell adhesion for OM fusion, in which lipoproteins/lipids are transferred by lateral diffusion. We further hypothesize that cell contact–dependent exchange helps myxobacteria to coordinate their social behaviors.
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spelling pubmed-33251832012-04-17 Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism Pathak, Darshankumar T. Wei, Xueming Bucuvalas, Alex Haft, Daniel H. Gerloff, Dietlind L. Wall, Daniel PLoS Genet Research Article Biofilms are dense microbial communities. Although widely distributed and medically important, how biofilm cells interact with one another is poorly understood. Recently, we described a novel process whereby myxobacterial biofilm cells exchange their outer membrane (OM) lipoproteins. For the first time we report here the identification of two host proteins, TraAB, required for transfer. These proteins are predicted to localize in the cell envelope; and TraA encodes a distant PA14 lectin-like domain, a cysteine-rich tandem repeat region, and a putative C-terminal protein sorting tag named MYXO-CTERM, while TraB encodes an OmpA-like domain. Importantly, TraAB are required in donors and recipients, suggesting bidirectional transfer. By use of a lipophilic fluorescent dye, we also discovered that OM lipids are exchanged. Similar to lipoproteins, dye transfer requires TraAB function, gliding motility and a structured biofilm. Importantly, OM exchange was found to regulate swarming and development behaviors, suggesting a new role in cell–cell communication. A working model proposes TraA is a cell surface receptor that mediates cell–cell adhesion for OM fusion, in which lipoproteins/lipids are transferred by lateral diffusion. We further hypothesize that cell contact–dependent exchange helps myxobacteria to coordinate their social behaviors. Public Library of Science 2012-04-12 /pmc/articles/PMC3325183/ /pubmed/22511878 http://dx.doi.org/10.1371/journal.pgen.1002626 Text en Pathak 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
Pathak, Darshankumar T.
Wei, Xueming
Bucuvalas, Alex
Haft, Daniel H.
Gerloff, Dietlind L.
Wall, Daniel
Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism
title Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism
title_full Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism
title_fullStr Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism
title_full_unstemmed Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism
title_short Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism
title_sort cell contact–dependent outer membrane exchange in myxobacteria: genetic determinants and mechanism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3325183/
https://www.ncbi.nlm.nih.gov/pubmed/22511878
http://dx.doi.org/10.1371/journal.pgen.1002626
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