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Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of Pseudomonas aeruginosa PA14 and PAO1.
mBio ( IF 6.4 ) Pub Date : 2020-02-25 , DOI: 10.1128/mbio.02644-19 Calvin K Lee 1, 2, 3 , Jérémy Vachier 4 , Jaime de Anda 1, 2, 3 , Kun Zhao 5, 6, 7 , Amy E Baker 8 , Rachel R Bennett 9 , Catherine R Armbruster 10, 11 , Kimberley A Lewis 8 , Rebecca L Tarnopol 12 , Charles J Lomba 1, 2, 3 , Deborah A Hogan 8 , Matthew R Parsek 10 , George A O'Toole 8 , Ramin Golestanian 13, 14 , Gerard C L Wong 2, 3, 15
mBio ( IF 6.4 ) Pub Date : 2020-02-25 , DOI: 10.1128/mbio.02644-19 Calvin K Lee 1, 2, 3 , Jérémy Vachier 4 , Jaime de Anda 1, 2, 3 , Kun Zhao 5, 6, 7 , Amy E Baker 8 , Rachel R Bennett 9 , Catherine R Armbruster 10, 11 , Kimberley A Lewis 8 , Rebecca L Tarnopol 12 , Charles J Lomba 1, 2, 3 , Deborah A Hogan 8 , Matthew R Parsek 10 , George A O'Toole 8 , Ramin Golestanian 13, 14 , Gerard C L Wong 2, 3, 15
Affiliation
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.
中文翻译:
在年轻生物膜的可逆表面附着过程中细菌的社会合作能力:铜绿假单胞菌PA14和PAO1的定量比较。
除了将细菌自身附着在表面上之外,细菌在“可逆附着”期间(即最初与表面接合时的瞬态表面附着期间)在做什么?附着细胞可以帮助其他细胞附着吗?如果是这样,它是否有助于所有细胞,还是采用更具选择性的策略来帮助附近的细胞(空间邻居)或其后代(时间邻居)?使用单细胞分辨率下的社区跟踪方法,我们基于铜绿假单胞菌PAO1和PA14的表面感测过程中可逆附着的进展情况,为这些问题提出了答案。尽管PAO1和PA14表现出相似的表面细胞数量增长趋势,当在谱系水平考虑细胞并使用完全可解决的随机模型的定量框架进行解释时,它们显示出出乎意料的差异。可逆的附着包括行为的两种状态,即进行性和非进行性,对应于谱系的细胞在分离前是否在表面上停留足够长的时间以分裂或不分裂。在可逆附着过程中,PAO1和PA14之间的明显差异表明存在两种表面定殖策略。与PA14谱系相比,PAO1谱系可快速定型到表面,具有早期c-di-GMP介导的胞外多糖(EPS)产生,可促进邻居的附着。PA14谱系通过循环AMP(cAMP)调节其运动能力,并保留表面记忆,因此可以对它们的后代进行底漆处理,以改善随后的表面附着。根据以前的研究发现,我们认为PAO1和PA14之间的差异可能分别源于基于Wsp的表面传感系统和基于Pil-Chp的表面传感系统之间的下游差异。作为一种可逆的附着,细胞经历了一段短暂的表面附着,这是一个普遍的认识,人们对此知之甚少。而且,尽管我们知道可逆附着最终以不可逆附着达到顶峰,但尚不清楚可逆附着如何在表型上发展,因为细菌表面传感电路从根本上改变了细胞行为。
更新日期:2020-02-25
中文翻译:
在年轻生物膜的可逆表面附着过程中细菌的社会合作能力:铜绿假单胞菌PA14和PAO1的定量比较。
除了将细菌自身附着在表面上之外,细菌在“可逆附着”期间(即最初与表面接合时的瞬态表面附着期间)在做什么?附着细胞可以帮助其他细胞附着吗?如果是这样,它是否有助于所有细胞,还是采用更具选择性的策略来帮助附近的细胞(空间邻居)或其后代(时间邻居)?使用单细胞分辨率下的社区跟踪方法,我们基于铜绿假单胞菌PAO1和PA14的表面感测过程中可逆附着的进展情况,为这些问题提出了答案。尽管PAO1和PA14表现出相似的表面细胞数量增长趋势,当在谱系水平考虑细胞并使用完全可解决的随机模型的定量框架进行解释时,它们显示出出乎意料的差异。可逆的附着包括行为的两种状态,即进行性和非进行性,对应于谱系的细胞在分离前是否在表面上停留足够长的时间以分裂或不分裂。在可逆附着过程中,PAO1和PA14之间的明显差异表明存在两种表面定殖策略。与PA14谱系相比,PAO1谱系可快速定型到表面,具有早期c-di-GMP介导的胞外多糖(EPS)产生,可促进邻居的附着。PA14谱系通过循环AMP(cAMP)调节其运动能力,并保留表面记忆,因此可以对它们的后代进行底漆处理,以改善随后的表面附着。根据以前的研究发现,我们认为PAO1和PA14之间的差异可能分别源于基于Wsp的表面传感系统和基于Pil-Chp的表面传感系统之间的下游差异。作为一种可逆的附着,细胞经历了一段短暂的表面附着,这是一个普遍的认识,人们对此知之甚少。而且,尽管我们知道可逆附着最终以不可逆附着达到顶峰,但尚不清楚可逆附着如何在表型上发展,因为细菌表面传感电路从根本上改变了细胞行为。