The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis

Autores
Kitahara, Yuki; Ordewurtel, Enno; Sean, Wilson; Yingje, Sun; Altabe, Silvia Graciela; de Mendoza, Diego; Gardner, Ethan; Van Teefelen, Sven
Año de publicación
2022
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
All cells must increase their volumes in response to biomass growth to maintain intracellular mass density within physiologically permissive bounds. Here, we investigate the regulation of volume growth in the Gram-positive bacterium Bacillus subtilis. To increase volume, bacteria enzymatically expand their cell envelopes and insert new envelope material. First, we demonstrate that cell-volume growth is determined indirectly, by expanding their envelopes in proportion to mass growth, similarly to the Gram-negative Escherichia coli, despite their fundamentally different envelope structures. Next, we studied, which pathways might be responsible for robust surface-to-mass coupling: We found that both peptidoglycan synthesis and membrane synthesis are required for proper surface-to-mass coupling. However, surprisingly, neither pathway is solely rate-limiting, contrary to wide-spread belief, since envelope growth continues at a reduced rate upon complete inhibition of either process. To arrest cell-envelope growth completely, the simultaneous inhibition of both envelope-synthesis processes is required. Thus, we suggest that multiple envelope-synthesis pathways collectively confer an important aspect of volume regulation, the coordination between surface growth, and biomass growth.
Fil: Kitahara, Yuki. University of Montreal; Canadá. Universite de Paris; Francia. Instituto Pasteur; Francia
Fil: Ordewurtel, Enno. Instituto Pasteur; Francia
Fil: Sean, Wilson. Harvard University; Estados Unidos
Fil: Yingje, Sun. Harvard University; Estados Unidos
Fil: Altabe, Silvia Graciela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: de Mendoza, Diego. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Gardner, Ethan. Harvard University; Estados Unidos
Fil: Van Teefelen, Sven. University of Montreal; Canadá. Institut Pasteur de Paris.; Francia
Materia
CELL ENVELOPE
GROWTH
BACILLUS SUBTILIS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/213944
Acceder
id CONICETDig_ff6d43b587ffffb9fc3a2dfb40f5a599
oai_identifier_str oai:ri.conicet.gov.ar:11336/213944
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilisKitahara, YukiOrdewurtel, EnnoSean, WilsonYingje, SunAltabe, Silvia Gracielade Mendoza, DiegoGardner, EthanVan Teefelen, SvenCELL ENVELOPEGROWTHBACILLUS SUBTILIShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1All cells must increase their volumes in response to biomass growth to maintain intracellular mass density within physiologically permissive bounds. Here, we investigate the regulation of volume growth in the Gram-positive bacterium Bacillus subtilis. To increase volume, bacteria enzymatically expand their cell envelopes and insert new envelope material. First, we demonstrate that cell-volume growth is determined indirectly, by expanding their envelopes in proportion to mass growth, similarly to the Gram-negative Escherichia coli, despite their fundamentally different envelope structures. Next, we studied, which pathways might be responsible for robust surface-to-mass coupling: We found that both peptidoglycan synthesis and membrane synthesis are required for proper surface-to-mass coupling. However, surprisingly, neither pathway is solely rate-limiting, contrary to wide-spread belief, since envelope growth continues at a reduced rate upon complete inhibition of either process. To arrest cell-envelope growth completely, the simultaneous inhibition of both envelope-synthesis processes is required. Thus, we suggest that multiple envelope-synthesis pathways collectively confer an important aspect of volume regulation, the coordination between surface growth, and biomass growth.Fil: Kitahara, Yuki. University of Montreal; Canadá. Universite de Paris; Francia. Instituto Pasteur; FranciaFil: Ordewurtel, Enno. Instituto Pasteur; FranciaFil: Sean, Wilson. Harvard University; Estados UnidosFil: Yingje, Sun. Harvard University; Estados UnidosFil: Altabe, Silvia Graciela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: de Mendoza, Diego. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; ArgentinaFil: Gardner, Ethan. Harvard University; Estados UnidosFil: Van Teefelen, Sven. University of Montreal; Canadá. Institut Pasteur de Paris.; FranciaOxford University Press2022-07info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/213944Kitahara, Yuki; Ordewurtel, Enno; Sean, Wilson; Yingje, Sun; Altabe, Silvia Graciela; et al.; The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis; Oxford University Press; Proceedings of the National Academy of Sciences nexus; 26; 7-2022; 1-162752-6542CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/pnasnexus/article/1/4/pgac134/6650235info:eu-repo/semantics/altIdentifier/doi/ 10.1093/pnasnexus/pgac134info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:33:49Zoai:ri.conicet.gov.ar:11336/213944instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:33:50.027CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis
title The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis
spellingShingle The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis
Kitahara, Yuki
CELL ENVELOPE
GROWTH
BACILLUS SUBTILIS
title_short The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis
title_full The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis
title_fullStr The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis
title_full_unstemmed The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis
title_sort The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis
dc.creator.none.fl_str_mv Kitahara, Yuki
Ordewurtel, Enno
Sean, Wilson
Yingje, Sun
Altabe, Silvia Graciela
de Mendoza, Diego
Gardner, Ethan
Van Teefelen, Sven
author Kitahara, Yuki
author_facet Kitahara, Yuki
Ordewurtel, Enno
Sean, Wilson
Yingje, Sun
Altabe, Silvia Graciela
de Mendoza, Diego
Gardner, Ethan
Van Teefelen, Sven
author_role author
author2 Ordewurtel, Enno
Sean, Wilson
Yingje, Sun
Altabe, Silvia Graciela
de Mendoza, Diego
Gardner, Ethan
Van Teefelen, Sven
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv CELL ENVELOPE
GROWTH
BACILLUS SUBTILIS
topic CELL ENVELOPE
GROWTH
BACILLUS SUBTILIS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv All cells must increase their volumes in response to biomass growth to maintain intracellular mass density within physiologically permissive bounds. Here, we investigate the regulation of volume growth in the Gram-positive bacterium Bacillus subtilis. To increase volume, bacteria enzymatically expand their cell envelopes and insert new envelope material. First, we demonstrate that cell-volume growth is determined indirectly, by expanding their envelopes in proportion to mass growth, similarly to the Gram-negative Escherichia coli, despite their fundamentally different envelope structures. Next, we studied, which pathways might be responsible for robust surface-to-mass coupling: We found that both peptidoglycan synthesis and membrane synthesis are required for proper surface-to-mass coupling. However, surprisingly, neither pathway is solely rate-limiting, contrary to wide-spread belief, since envelope growth continues at a reduced rate upon complete inhibition of either process. To arrest cell-envelope growth completely, the simultaneous inhibition of both envelope-synthesis processes is required. Thus, we suggest that multiple envelope-synthesis pathways collectively confer an important aspect of volume regulation, the coordination between surface growth, and biomass growth.
Fil: Kitahara, Yuki. University of Montreal; Canadá. Universite de Paris; Francia. Instituto Pasteur; Francia
Fil: Ordewurtel, Enno. Instituto Pasteur; Francia
Fil: Sean, Wilson. Harvard University; Estados Unidos
Fil: Yingje, Sun. Harvard University; Estados Unidos
Fil: Altabe, Silvia Graciela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: de Mendoza, Diego. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina
Fil: Gardner, Ethan. Harvard University; Estados Unidos
Fil: Van Teefelen, Sven. University of Montreal; Canadá. Institut Pasteur de Paris.; Francia
description All cells must increase their volumes in response to biomass growth to maintain intracellular mass density within physiologically permissive bounds. Here, we investigate the regulation of volume growth in the Gram-positive bacterium Bacillus subtilis. To increase volume, bacteria enzymatically expand their cell envelopes and insert new envelope material. First, we demonstrate that cell-volume growth is determined indirectly, by expanding their envelopes in proportion to mass growth, similarly to the Gram-negative Escherichia coli, despite their fundamentally different envelope structures. Next, we studied, which pathways might be responsible for robust surface-to-mass coupling: We found that both peptidoglycan synthesis and membrane synthesis are required for proper surface-to-mass coupling. However, surprisingly, neither pathway is solely rate-limiting, contrary to wide-spread belief, since envelope growth continues at a reduced rate upon complete inhibition of either process. To arrest cell-envelope growth completely, the simultaneous inhibition of both envelope-synthesis processes is required. Thus, we suggest that multiple envelope-synthesis pathways collectively confer an important aspect of volume regulation, the coordination between surface growth, and biomass growth.
publishDate 2022
dc.date.none.fl_str_mv 2022-07
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/213944
Kitahara, Yuki; Ordewurtel, Enno; Sean, Wilson; Yingje, Sun; Altabe, Silvia Graciela; et al.; The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis; Oxford University Press; Proceedings of the National Academy of Sciences nexus; 26; 7-2022; 1-16
2752-6542
CONICET Digital
CONICET
url http://hdl.handle.net/11336/213944
identifier_str_mv Kitahara, Yuki; Ordewurtel, Enno; Sean, Wilson; Yingje, Sun; Altabe, Silvia Graciela; et al.; The role of cell-envelope synthesis for envelope growth and cytoplasmic density in Bacillus subtilis; Oxford University Press; Proceedings of the National Academy of Sciences nexus; 26; 7-2022; 1-16
2752-6542
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/pnasnexus/article/1/4/pgac134/6650235
info:eu-repo/semantics/altIdentifier/doi/ 10.1093/pnasnexus/pgac134
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
_version_ 1844613042398035968
score 13.070432

Publicaciones similares