Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity

Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity
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DOI:
10.1128/msphere.00740-19
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发表时间:
2020-03-01
期刊:
影响因子:
4.8
通讯作者:
Valls, Marc
Valls, Marc
中科院分区:
生物学2区
文献类型:
--
作者:
Corral, Jordi;Sebastia, Pau;Valls, Marc

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青枯雷尔氏菌是一种细菌性植物病原菌,在世界范围内造成重大的经济损失。除了极鞭毛负责游泳运动,这种病原体产生IV型皮利(TFP),支配抽搐运动,鞭毛独立的运动固体表面。趋化性在植物定殖中的意义,通过蛋白质CheW和CheA控制鞭毛旋转,先前已在R.青枯菌属在这项工作中,我们已经确定了在这种细菌的铜绿假单胞菌的同源物皮利和chpA基因,建议发挥作用,类似于那些发挥的cheW和cheA基因,分别在TFP相关的运动。我们证明了R.缺失了皮利I或chpA编码区的青枯菌菌株显示正常的游动和趋化性,但改变了生物膜形成,降低了抽搐运动性、转化效率和根附着。此外,这些突变体显示野生型生长在植物和受损的番茄植物的毒力土壤浸泡接种后,但不直接施加到木质部。pilA和fliC编码的主要菌毛蛋白和鞭毛蛋白亚基,分别与缺失突变体的比较表明,抽搐和游泳所需的植物定殖和全毒力。这项工作首次证明了由pil-chp基因编码的菌毛介导的途径在R.青枯菌,证明皮利和chpA基因是真正的运动调节因子,控制抽搐运动及其三种相关表型:毒力、自然转化和生物膜形成。重要信息抽搐和游泳是由皮利和鞭毛控制的两种细菌运动。目前的工作确定了第一次在革兰氏阴性植物病原菌青枯雷尔氏菌菌毛介导的趋化性途径类似于管理鞭毛介导的趋化性。我们表明,在这一途径中的调控基因控制所有的表型相关的皮利,包括抽搐运动,自然转化,和生物膜的形成,也直接牵连在毒力,主要是在第一步的植物感染。结果表明,皮利对细菌与细菌的相互作用有着比鞭毛更大的影响。青枯菌与番茄植物的关系,并揭示了游泳和抽搐运动表型之间的新类型的串扰:缺乏皮利的细菌中增强的游泳和鞭毛在根附着中的作用。
Ralstonia solanacearum is a bacterial plant pathogen causing important economic losses worldwide. In addition to the polar flagella responsible for swimming motility, this pathogen produces type IV pili (TFP) that govern twitching motility, a flagellum-independent movement on solid surfaces. The implication of chemotaxis in plant colonization, through the control flagellar rotation by the proteins CheW and CheA, has been previously reported in R. solanacearum. In this work, we have identified in this bacterium homologues of the Pseudomonas aeruginosa pilI and chpA genes, suggested to play roles in TFP-associated motility analogous to those played by the cheW and cheA genes, respectively. We demonstrate that R. solanacearum strains with a deletion of the pilI or the chpA coding region show normal swimming and chemotaxis but altered biofilm formation and reduced twitching motility, transformation efficiency, and root attachment. Furthermore, these mutants displayed wild-type growth in planta and impaired virulence on tomato plants after soil-drench inoculations but not when directly applied to the xylem. Comparison with deletion mutants for pilA and fliC-encoding the major pilin and flagellin subunits, respectively-showed that both twitching and swimming are required for plant colonization and full virulence. This work proves for the first time the functionality of a pilus-mediated pathway encoded by pil-chp genes in R. solanacearum, demonstrating that pilI and chpA genes are bona fide motility regulators controlling twitching motility and its three related phenotypes: virulence, natural transformation, and biofilm formation.IMPORTANCE Twitching and swimming are two bacterial movements governed by pili and flagella. The present work identifies for the first time in the Gram-negative plant pathogen Ralstonia solanacearum a pilus-mediated chemotaxis pathway analogous to that governing flagellum-mediated chemotaxis. We show that regulatory genes in this pathway control all of the phenotypes related to pili, including twitching motility, natural transformation, and biofilm formation, and are also directly implicated in virulence, mainly during the first steps of the plant infection. Our results show that pili have a higher impact than flagella on the interaction of R. solanacearum with tomato plants and reveal new types of cross-talk between the swimming and twitching motility phenotypes: enhanced swimming in bacteria lacking pili and a role for the flagellum in root attachment.