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A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis

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dc.citation.titlemBio
dc.citation.volume6
dc.contributor.orcidhttp://orcid.org/0000-0001-6430-7122
dc.contributor.orcidhttp://orcid.org/0000-0001-6784-2534
dc.creatorGrau, Roberto Ricardo
dc.creatorDe Oña, Paula
dc.creatorKunert, Maritta
dc.creatorLeñini, Cecilia
dc.creatorGallegos Monterrosa, Ramses
dc.creatorMhatre, Eisha
dc.creatorVileta, Darío
dc.creatorDonato, Verónica
dc.creatorHölscher, Theresa
dc.creatorBoland, Sebastian
dc.creatorKuipers, Oscar P.
dc.creatorKovács, Ákos T.
dc.date.accessioned2024-05-31T13:59:04Z
dc.date.available2024-05-31T13:59:04Z
dc.date.issued2015-07-07
dc.description.abstractMulticellular biofilm formation and surface motility are bacterial behaviors considered mutually exclusive. However, the basic decision to move over or stay attached to a surface is poorly understood. Here, we discover that in Bacillus subtilis, the key root biofilm-controlling transcription factor Spo0A~Pi (phosphorylated Spo0A) governs the flagellum-independent mechanism of social sliding motility. A Spo0A-deficient strain was totally unable to slide and colonize plant roots, evidencing the important role that sliding might play in natural settings. Microarray experiments plus subsequent genetic characterization showed that the machineries of sliding and biofilm formation share the same main components (i.e., surfactin, the hydrophobin BslA, exopolysaccharide, and de novo-formed fatty acids). Sliding proficiency was transduced by the Spo0A-phosphorelay histidine kinases KinB and KinC. We discovered that potassium, a previously known inhibitor of KinC-dependent biofilm formation, is the specific sliding-activating signal through a thus-far-unnoticed cytosolic domain of KinB, which resembles the selectivity filter sequence of potassium channels. The differential expression of the Spo0A~Pireporter abrB gene and the different levels of the constitutively active form of Spo0A, Sad67, in spo0A cells grown in optimized media that simultaneously stimulate motile and sessile behaviors uncover the spatiotemporal response of KinB and KinC to potassium and the gradual increase in Spo0A~Pi that orchestrates the sequential activation of sliding, followed by sessile biofilm formation and finally sporulation in the same population. Overall, these results provide insights into how multicellular behaviors formerly believed to be antagonistic are coordinately activated in benefit of the bacterium and its interaction with the host. IMPORTANCE Alternation between motile and sessile behaviors is central to bacterial adaptation, survival, and colonization. However, how is the collective decision to move over or stay attached to a surface controlled? Here, we use the model plantbeneficial bacterium Bacillus subtilis to answer this question. Remarkably, we discover that sessile biofilm formation and social sliding motility share the same structural components and the Spo0A regulatory network via sensor kinases, KinB and KinC. Potassium, an inhibitor of KinC-dependent biofilm formation, triggers sliding via a potassium-perceiving cytosolic domain of KinB that resembles the selectivity filter of potassium channels. The spatiotemporal response of these kinases to variable potassium levels and the gradual increase in Spo0A~Pi levels that orchestrates the activation of sliding before biofilm formation shed light on how multicellular behaviors formerly believed to be antagonistic work together to benefit the population fitness.
dc.description.filFil: Grau, Roberto Ricardo. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Departamento de Microbiología. Consejo Nacional de Investigaciones Científicas y Técnicas (COICET); Argentina.
dc.description.filFil: De Oña, Paula. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Departamento de Microbiología. Consejo Nacional de Investigaciones Científicas y Técnicas (COICET); Argentina.
dc.description.filFil: Kunert, Maritta. Max Planck Institute for Chemical Ecology. Department of Bioorganic Chemistry; Germany.
dc.description.filFil: Leñini, Cecilia. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Departamento de Microbiología. Consejo Nacional de Investigaciones Científicas y Técnicas (COICET); Argentina.
dc.description.filFil: Gallegos Monterrosa, Ramses. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Departamento de Microbiología. Consejo Nacional de Investigaciones Científicas y Técnicas (COICET); Argentina.
dc.description.filFil: Mhatre, Eisha. Friedrich Schiller University of Jena. , Institute of Microbiology. Terrestrial Biofilms Group; Germany.
dc.description.filFil: Vileta, Darío. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Departamento de Microbiología. Consejo Nacional de Investigaciones Científicas y Técnicas (COICET); Argentina.
dc.description.filFil: Donato, Verónica. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Departamento de Microbiología. Consejo Nacional de Investigaciones Científicas y Técnicas (COICET); Argentina.
dc.description.filFil: Hölscher, Theresa. Friedrich Schiller University of Jena. , Institute of Microbiology. Terrestrial Biofilms Group; Germany.
dc.description.filFil: Boland, Sebastian. Max Planck Institute for Chemical Ecology. Department of Bioorganic Chemistry; Germany.
dc.description.filFil: Kuipers, Oscar P. University of Groningen. Groningen Biomolecular Sciences and Biotechnology Institute. Molecular Genetics; The Netherlands.
dc.description.filFil: Kovács, Ákos T. Friedrich Schiller University of Jena. , Institute of Microbiology. Terrestrial Biofilms Group; Germany.
dc.description.sponsorshipConsejo Nacional de Investigaciones Científicas y Técnicas (CONICET)
dc.description.sponsorshipAgencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (ANPCyT)
dc.description.sponsorshipPew Latin-American Program in Biological Sciences
dc.description.sponsorshipFulbright Committee
dc.description.sponsorshipFundación Antorchas
dc.description.sponsorshipDeutsche Forschungsgemeinschaft (DFG)
dc.description.sponsorshipJena School for Microbial Communication
dc.format.extent1-16
dc.identifier.issn2150-7511
dc.identifier.urihttps://hdl.handle.net/2133/27117
dc.language.isoen
dc.publisherAmerican Society for Microbiology
dc.relation.publisherversionhttps://journals.asm.org/doi/epdf/10.1128/mbio.00581-15
dc.relation.publisherversionhttps://doi.org/10.1128/mbio.00581-15
dc.rightsopenAccess
dc.rights.holderGrau, Roberto Ricardo
dc.rights.holderDe Oña, Paula
dc.rights.holderKunert, Maritta
dc.rights.holderLeñini, Cecilia
dc.rights.holderGallegos Monterrosa, Ramses
dc.rights.holderMhatre, Eisha
dc.rights.holderVileta, Darío
dc.rights.holderDonato, Verónica
dc.rights.holderHölscher, Theresa
dc.rights.holderBoland, Sebastian
dc.rights.holderKuipers, Oscar P.
dc.rights.holderKovács, Ákos T.
dc.rights.holderUniversidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas
dc.rights.textAttribution-NonCommercial-ShareAlike 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by-nc-sa/4.0/
dc.subjectBacillus subtilis
dc.subjectGene expression profiling
dc.subjectHistidine kinase
dc.subjectLocomotion
dc.subjectMolecular sequence data
dc.subjectPotassium
dc.subjectProtein kinases
dc.titleA duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis
dc.typearticulo
dc.type.versionpublishedVersion

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