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Transient heterogeneity in extracellular protease production by Bacillus subtilis

The most sophisticated survival strategy Bacillus subtilis employs is the differentiation of a subpopulation of cells into highly resistant endospores. To examine the expression patterns of non-sporulating cells within heterogeneous populations, we used buoyant density centrifugation to separate veg...

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Autores principales: Veening, Jan-Willem, Igoshin, Oleg A, Eijlander, Robyn T, Nijland, Reindert, Hamoen, Leendert W, Kuipers, Oscar P
Formato: Texto
Lenguaje:English
Publicado: Nature Publishing Group 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2387230/
https://www.ncbi.nlm.nih.gov/pubmed/18414485
http://dx.doi.org/10.1038/msb.2008.18
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author Veening, Jan-Willem
Igoshin, Oleg A
Eijlander, Robyn T
Nijland, Reindert
Hamoen, Leendert W
Kuipers, Oscar P
author_facet Veening, Jan-Willem
Igoshin, Oleg A
Eijlander, Robyn T
Nijland, Reindert
Hamoen, Leendert W
Kuipers, Oscar P
author_sort Veening, Jan-Willem
collection PubMed
description The most sophisticated survival strategy Bacillus subtilis employs is the differentiation of a subpopulation of cells into highly resistant endospores. To examine the expression patterns of non-sporulating cells within heterogeneous populations, we used buoyant density centrifugation to separate vegetative cells from endospore-containing cells and compared the transcriptome profiles of both subpopulations. This demonstrated the differential expression of various regulons. Subsequent single-cell analyses using promoter-gfp fusions confirmed our microarray results. Surprisingly, only part of the vegetative subpopulation highly and transiently expresses genes encoding the extracellular proteases Bpr (bacillopeptidase) and AprE (subtilisin), both of which are under the control of the DegU transcriptional regulator. As these proteases and their degradation products freely diffuse within the liquid growth medium, all cells within the clonal population are expected to benefit from their activities, suggesting that B. subtilis employs cooperative or even altruistic behavior. To unravel the mechanisms by which protease production heterogeneity within the non-sporulating subpopulation is established, we performed a series of genetic experiments combined with mathematical modeling. Simulations with our model yield valuable insights into how population heterogeneity may arise by the relatively long and variable response times within the DegU autoactivating pathway.
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spelling pubmed-23872302008-05-21 Transient heterogeneity in extracellular protease production by Bacillus subtilis Veening, Jan-Willem Igoshin, Oleg A Eijlander, Robyn T Nijland, Reindert Hamoen, Leendert W Kuipers, Oscar P Mol Syst Biol Article The most sophisticated survival strategy Bacillus subtilis employs is the differentiation of a subpopulation of cells into highly resistant endospores. To examine the expression patterns of non-sporulating cells within heterogeneous populations, we used buoyant density centrifugation to separate vegetative cells from endospore-containing cells and compared the transcriptome profiles of both subpopulations. This demonstrated the differential expression of various regulons. Subsequent single-cell analyses using promoter-gfp fusions confirmed our microarray results. Surprisingly, only part of the vegetative subpopulation highly and transiently expresses genes encoding the extracellular proteases Bpr (bacillopeptidase) and AprE (subtilisin), both of which are under the control of the DegU transcriptional regulator. As these proteases and their degradation products freely diffuse within the liquid growth medium, all cells within the clonal population are expected to benefit from their activities, suggesting that B. subtilis employs cooperative or even altruistic behavior. To unravel the mechanisms by which protease production heterogeneity within the non-sporulating subpopulation is established, we performed a series of genetic experiments combined with mathematical modeling. Simulations with our model yield valuable insights into how population heterogeneity may arise by the relatively long and variable response times within the DegU autoactivating pathway. Nature Publishing Group 2008-04-15 /pmc/articles/PMC2387230/ /pubmed/18414485 http://dx.doi.org/10.1038/msb.2008.18 Text en Copyright © 2008, EMBO and Nature Publishing Group http://creativecommons.org/licenses/by-nc-nd/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution Licence, which permits distribution and reproduction in any medium, provided the original author and source are credited. This licence does not permit commercial exploitation or the creation of derivative works without specific permission.
spellingShingle Article
Veening, Jan-Willem
Igoshin, Oleg A
Eijlander, Robyn T
Nijland, Reindert
Hamoen, Leendert W
Kuipers, Oscar P
Transient heterogeneity in extracellular protease production by Bacillus subtilis
title Transient heterogeneity in extracellular protease production by Bacillus subtilis
title_full Transient heterogeneity in extracellular protease production by Bacillus subtilis
title_fullStr Transient heterogeneity in extracellular protease production by Bacillus subtilis
title_full_unstemmed Transient heterogeneity in extracellular protease production by Bacillus subtilis
title_short Transient heterogeneity in extracellular protease production by Bacillus subtilis
title_sort transient heterogeneity in extracellular protease production by bacillus subtilis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2387230/
https://www.ncbi.nlm.nih.gov/pubmed/18414485
http://dx.doi.org/10.1038/msb.2008.18
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