Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PA14 and PAO1

ABSTRACT What are bacteria doing during “reversible attachment,” the period of transient surface attachment when they initially engage a surface, besides attaching themselves to the surface? Can an attaching cell help any other cell attach? If so, does it help all cells or employ a more selective st...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Calvin K. Lee, Jérémy Vachier, Jaime de Anda, Kun Zhao, Amy E. Baker, Rachel R. Bennett, Catherine R. Armbruster, Kimberley A. Lewis, Rebecca L. Tarnopol, Charles J. Lomba, Deborah A. Hogan, Matthew R. Parsek, George A. O’Toole, Ramin Golestanian, Gerard C. L. Wong
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Pseudomonas aeruginosa bacterial biofilms reversible attachment stochastic model surface sensing Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/338c3de6bea14687ad6f5567e98794ee
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:338c3de6bea14687ad6f5567e98794ee
record_format	dspace
spelling	oai:doaj.org-article:338c3de6bea14687ad6f5567e98794ee2021-11-15T15:56:58ZSocial Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PA14 and PAO110.1128/mBio.02644-192150-7511https://doaj.org/article/338c3de6bea14687ad6f5567e98794ee2020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02644-19https://doaj.org/toc/2150-7511ABSTRACT What are bacteria doing during “reversible attachment,” the period of transient surface attachment when they initially engage a surface, besides attaching themselves to the surface? Can an attaching cell help any other cell attach? If so, does it help all cells or employ a more selective strategy to help either nearby cells (spatial neighbors) or its progeny (temporal neighbors)? Using community tracking methods at the single-cell resolution, we suggest answers to these questions based on how reversible attachment progresses during surface sensing for Pseudomonas aeruginosa strains PAO1 and PA14. Although PAO1 and PA14 exhibit similar trends of surface cell population increase, they show unanticipated differences when cells are considered at the lineage level and interpreted using the quantitative framework of an exactly solvable stochastic model. Reversible attachment comprises two regimes of behavior, processive and nonprocessive, corresponding to whether cells of the lineage stay on the surface long enough to divide, or not, before detaching. Stark differences between PAO1 and PA14 in the processive regime of reversible attachment suggest the existence of two surface colonization strategies. PAO1 lineages commit quickly to a surface compared to PA14 lineages, with early c-di-GMP-mediated exopolysaccharide (EPS) production that can facilitate the attachment of neighbors. PA14 lineages modulate their motility via cyclic AMP (cAMP) and retain memory of the surface so that their progeny are primed for improved subsequent surface attachment. Based on the findings of previous studies, we propose that the differences between PAO1 and PA14 are potentially rooted in downstream differences between Wsp-based and Pil-Chp-based surface-sensing systems, respectively. IMPORTANCE The initial pivotal phase of bacterial biofilm formation known as reversible attachment, where cells undergo a period of transient surface attachment, is at once universal and poorly understood. What is more, although we know that reversible attachment culminates ultimately in irreversible attachment, it is not clear how reversible attachment progresses phenotypically, as bacterial surface-sensing circuits fundamentally alter cellular behavior. We analyze diverse observed bacterial behavior one family at a time (defined as a full lineage of cells related to one another by division) using a unifying stochastic model and show that our findings lead to insights on the time evolution of reversible attachment and the social cooperative dimension of surface attachment in PAO1 and PA14 strains.Calvin K. LeeJérémy VachierJaime de AndaKun ZhaoAmy E. BakerRachel R. BennettCatherine R. ArmbrusterKimberley A. LewisRebecca L. TarnopolCharles J. LombaDeborah A. HoganMatthew R. ParsekGeorge A. O’TooleRamin GolestanianGerard C. L. WongAmerican Society for MicrobiologyarticlePseudomonas aeruginosabacterial biofilmsreversible attachmentstochastic modelsurface sensingMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa bacterial biofilms reversible attachment stochastic model surface sensing Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa bacterial biofilms reversible attachment stochastic model surface sensing Microbiology QR1-502 Calvin K. Lee Jérémy Vachier Jaime de Anda Kun Zhao Amy E. Baker Rachel R. Bennett Catherine R. Armbruster Kimberley A. Lewis Rebecca L. Tarnopol Charles J. Lomba Deborah A. Hogan Matthew R. Parsek George A. O’Toole Ramin Golestanian Gerard C. L. Wong Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PA14 and PAO1
description	ABSTRACT What are bacteria doing during “reversible attachment,” the period of transient surface attachment when they initially engage a surface, besides attaching themselves to the surface? Can an attaching cell help any other cell attach? If so, does it help all cells or employ a more selective strategy to help either nearby cells (spatial neighbors) or its progeny (temporal neighbors)? Using community tracking methods at the single-cell resolution, we suggest answers to these questions based on how reversible attachment progresses during surface sensing for Pseudomonas aeruginosa strains PAO1 and PA14. Although PAO1 and PA14 exhibit similar trends of surface cell population increase, they show unanticipated differences when cells are considered at the lineage level and interpreted using the quantitative framework of an exactly solvable stochastic model. Reversible attachment comprises two regimes of behavior, processive and nonprocessive, corresponding to whether cells of the lineage stay on the surface long enough to divide, or not, before detaching. Stark differences between PAO1 and PA14 in the processive regime of reversible attachment suggest the existence of two surface colonization strategies. PAO1 lineages commit quickly to a surface compared to PA14 lineages, with early c-di-GMP-mediated exopolysaccharide (EPS) production that can facilitate the attachment of neighbors. PA14 lineages modulate their motility via cyclic AMP (cAMP) and retain memory of the surface so that their progeny are primed for improved subsequent surface attachment. Based on the findings of previous studies, we propose that the differences between PAO1 and PA14 are potentially rooted in downstream differences between Wsp-based and Pil-Chp-based surface-sensing systems, respectively. IMPORTANCE The initial pivotal phase of bacterial biofilm formation known as reversible attachment, where cells undergo a period of transient surface attachment, is at once universal and poorly understood. What is more, although we know that reversible attachment culminates ultimately in irreversible attachment, it is not clear how reversible attachment progresses phenotypically, as bacterial surface-sensing circuits fundamentally alter cellular behavior. We analyze diverse observed bacterial behavior one family at a time (defined as a full lineage of cells related to one another by division) using a unifying stochastic model and show that our findings lead to insights on the time evolution of reversible attachment and the social cooperative dimension of surface attachment in PAO1 and PA14 strains.
format	article
author	Calvin K. Lee Jérémy Vachier Jaime de Anda Kun Zhao Amy E. Baker Rachel R. Bennett Catherine R. Armbruster Kimberley A. Lewis Rebecca L. Tarnopol Charles J. Lomba Deborah A. Hogan Matthew R. Parsek George A. O’Toole Ramin Golestanian Gerard C. L. Wong
author_facet	Calvin K. Lee Jérémy Vachier Jaime de Anda Kun Zhao Amy E. Baker Rachel R. Bennett Catherine R. Armbruster Kimberley A. Lewis Rebecca L. Tarnopol Charles J. Lomba Deborah A. Hogan Matthew R. Parsek George A. O’Toole Ramin Golestanian Gerard C. L. Wong
author_sort	Calvin K. Lee
title	Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PA14 and PAO1
title_short	Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PA14 and PAO1
title_full	Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PA14 and PAO1
title_fullStr	Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PA14 and PAO1
title_full_unstemmed	Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PA14 and PAO1
title_sort	social cooperativity of bacteria during reversible surface attachment in young biofilms: a quantitative comparison of <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> pa14 and pao1
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/338c3de6bea14687ad6f5567e98794ee
work_keys_str_mv	AT calvinklee socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT jeremyvachier socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT jaimedeanda socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT kunzhao socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT amyebaker socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT rachelrbennett socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT catherinerarmbruster socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT kimberleyalewis socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT rebeccaltarnopol socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT charlesjlomba socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT deborahahogan socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT matthewrparsek socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT georgeaotoole socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT ramingolestanian socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1 AT gerardclwong socialcooperativityofbacteriaduringreversiblesurfaceattachmentinyoungbiofilmsaquantitativecomparisonofnamedcontentcontenttypegenusspeciespseudomonasaeruginosanamedcontentpa14andpao1
_version_	1718427079188414464

Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PA14 and PAO1

Ejemplares similares