The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena

Bacteria in general serve two main tasks: cell growth and division. Both processes include peptidoglycan extension to allow cell expansion and to form the poles of the daughter cells, respectively. The cyanobacterium Anabaena forms filaments of communicated cells in which the outer membrane and the...

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Autores: Velázquez Suárez, Cristina, Valladares, A., Luque, I., Herrero, A.
Tipo de documento: artigo
Estado:Versão publicada
Data de publicação:2022
País:España
Recursos:Universidad de Sevilla (US)
Repositório:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/177262
Acesso em linha:https://hdl.handle.net/11441/177262
https://doi.org/10.1128/mbio.01165-22
Access Level:Acceso aberto
Palavra-chave:Cell growth
Anabaena filaments
Intercellular septa
Lateral peptidoglycan growth
Septal peptidoglycan growth
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spelling The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium AnabaenaVelázquez Suárez, CristinaValladares, A.Luque, I.Herrero, A.Cell growthAnabaena filamentsIntercellular septaLateral peptidoglycan growthSeptal peptidoglycan growthBacteria in general serve two main tasks: cell growth and division. Both processes include peptidoglycan extension to allow cell expansion and to form the poles of the daughter cells, respectively. The cyanobacterium Anabaena forms filaments of communicated cells in which the outer membrane and the peptidoglycan sacculus, which is engrossed in the intercellular regions between contiguous cells, are continuous along the filament. During the growth of Anabaena, peptidoglycan incorporation was weak at the cell periphery. During cell division, midcell peptidoglycan incorporation matched the localization of the divisome, and incorporation persisted in the intercellular septa, even after the division was completed. MreB, MreC, and MreD were located throughout the cell periphery and, in contrast to other bacteria, also to the divisome all along midcell peptidoglycan growth. In Anabaena mutants bearing inactivated mreB, mreC, or mreD genes, which showed conspicuous alterations in the filament morphology, consecutive septal bands of peptidoglycan growth were frequently not parallel to each other and were irregularly spaced along the filament, reproducing the disposition of the Z-ring. Both lateral and septal growth was impaired in strains down-expressing Z-ring components, and MreB and MreD appeared to directly interact with some divisome components. We propose that, in Anabaena, association with the divisome is a way for localization of MreB, MreC, and MreD at the cell poles, where they regulate lateral, midcell, and septal peptidoglycan growth with the latter being involved in localization and maintenance of the intercellular septal-junction protein structures that mediate cell-cell communication along the filament. IMPORTANCE Peptidoglycan surrounds the bacterial cell, being essential for the determination of the bacterium-specific morphology and survival. Peptidoglycan growth has been thoroughly investigated in some model rod-shaped bacteria, and more recently some representatives with disparate morphologies became into focus, revealing that patterns of peptidoglycan growth are much more diverse than previously anticipated. Anabaena forms filaments of communicated cells exhibiting features of multicellular organisms, such as the production of morphogens and coupled circadian oscillations. Here, we showed that Anabaena presented a distinct pattern of peptidoglycan growth characterized by continuous incorporation of material at the polar intercellular regions, contributing to assembling and maintaining the protein complexes that expand the septal peptidoglycan mediating intercellular molecular exchange in the filament.American Society for MicrobiologyGenéticaMinisterio de Ciencia e Innovación (MICIN). EspañaJunta de AndalucíaEuropean Commission (EC). Fondo Europeo de Desarrollo Regional (FEDER)2022info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttps://hdl.handle.net/11441/177262https://doi.org/10.1128/mbio.01165-22reponame:idUS. Depósito de Investigación de la Universidad de Sevillainstname:Universidad de Sevilla (US)InglésMBIO, 13 (4).BFU2016-77097-PP20-00032https://doi.org/10.1128/mbio.01165-22info:eu-repo/semantics/openAccessoai:idus.us.es:11441/1772622026-06-17T12:51:07Z
dc.title.none.fl_str_mv The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena
title The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena
spellingShingle The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena
Velázquez Suárez, Cristina
Cell growth
Anabaena filaments
Intercellular septa
Lateral peptidoglycan growth
Septal peptidoglycan growth
title_short The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena
title_full The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena
title_fullStr The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena
title_full_unstemmed The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena
title_sort The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena
dc.creator.none.fl_str_mv Velázquez Suárez, Cristina
Valladares, A.
Luque, I.
Herrero, A.
author Velázquez Suárez, Cristina
author_facet Velázquez Suárez, Cristina
Valladares, A.
Luque, I.
Herrero, A.
author_role author
author2 Valladares, A.
Luque, I.
Herrero, A.
author2_role author
author
author
dc.contributor.none.fl_str_mv Genética
Ministerio de Ciencia e Innovación (MICIN). España
Junta de Andalucía
European Commission (EC). Fondo Europeo de Desarrollo Regional (FEDER)
dc.subject.none.fl_str_mv Cell growth
Anabaena filaments
Intercellular septa
Lateral peptidoglycan growth
Septal peptidoglycan growth
topic Cell growth
Anabaena filaments
Intercellular septa
Lateral peptidoglycan growth
Septal peptidoglycan growth
description Bacteria in general serve two main tasks: cell growth and division. Both processes include peptidoglycan extension to allow cell expansion and to form the poles of the daughter cells, respectively. The cyanobacterium Anabaena forms filaments of communicated cells in which the outer membrane and the peptidoglycan sacculus, which is engrossed in the intercellular regions between contiguous cells, are continuous along the filament. During the growth of Anabaena, peptidoglycan incorporation was weak at the cell periphery. During cell division, midcell peptidoglycan incorporation matched the localization of the divisome, and incorporation persisted in the intercellular septa, even after the division was completed. MreB, MreC, and MreD were located throughout the cell periphery and, in contrast to other bacteria, also to the divisome all along midcell peptidoglycan growth. In Anabaena mutants bearing inactivated mreB, mreC, or mreD genes, which showed conspicuous alterations in the filament morphology, consecutive septal bands of peptidoglycan growth were frequently not parallel to each other and were irregularly spaced along the filament, reproducing the disposition of the Z-ring. Both lateral and septal growth was impaired in strains down-expressing Z-ring components, and MreB and MreD appeared to directly interact with some divisome components. We propose that, in Anabaena, association with the divisome is a way for localization of MreB, MreC, and MreD at the cell poles, where they regulate lateral, midcell, and septal peptidoglycan growth with the latter being involved in localization and maintenance of the intercellular septal-junction protein structures that mediate cell-cell communication along the filament. IMPORTANCE Peptidoglycan surrounds the bacterial cell, being essential for the determination of the bacterium-specific morphology and survival. Peptidoglycan growth has been thoroughly investigated in some model rod-shaped bacteria, and more recently some representatives with disparate morphologies became into focus, revealing that patterns of peptidoglycan growth are much more diverse than previously anticipated. Anabaena forms filaments of communicated cells exhibiting features of multicellular organisms, such as the production of morphogens and coupled circadian oscillations. Here, we showed that Anabaena presented a distinct pattern of peptidoglycan growth characterized by continuous incorporation of material at the polar intercellular regions, contributing to assembling and maintaining the protein complexes that expand the septal peptidoglycan mediating intercellular molecular exchange in the filament.
publishDate 2022
dc.date.none.fl_str_mv 2022
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/11441/177262
https://doi.org/10.1128/mbio.01165-22
url https://hdl.handle.net/11441/177262
https://doi.org/10.1128/mbio.01165-22
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv MBIO, 13 (4).
BFU2016-77097-P
P20-00032
https://doi.org/10.1128/mbio.01165-22
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:idUS. Depósito de Investigación de la Universidad de Sevilla
instname:Universidad de Sevilla (US)
instname_str Universidad de Sevilla (US)
reponame_str idUS. Depósito de Investigación de la Universidad de Sevilla
collection idUS. Depósito de Investigación de la Universidad de Sevilla
repository.name.fl_str_mv
repository.mail.fl_str_mv
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