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      Multiple functions of flagellar motility and chemotaxis in bacterial physiology

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          ABSTRACT

          Most swimming bacteria are capable of following gradients of nutrients, signaling molecules and other environmental factors that affect bacterial physiology. This tactic behavior became one of the most-studied model systems for signal transduction and quantitative biology, and underlying molecular mechanisms are well characterized in Escherichia coli and several other model bacteria. In this review, we focus primarily on less understood aspect of bacterial chemotaxis, namely its physiological relevance for individual bacterial cells and for bacterial populations. As evident from multiple recent studies, even for the same bacterial species flagellar motility and chemotaxis might serve multiple roles, depending on the physiological and environmental conditions. Among these, finding sources of nutrients and more generally locating niches that are optimal for growth appear to be one of the major functions of bacterial chemotaxis, which could explain many chemoeffector preferences as well as flagellar gene regulation. Chemotaxis might also generally enhance efficiency of environmental colonization by motile bacteria, which involves intricate interplay between individual and collective behaviors and trade-offs between growth and motility. Finally, motility and chemotaxis play multiple roles in collective behaviors of bacteria including swarming, biofilm formation and autoaggregation, as well as in their interactions with animal and plant hosts.

          Abstract

          This review summarizes the recent advances in understanding the impact of flagellar motility and chemotaxis on various behaviors of bacteria, from nutrient acquisition and population range expansion to interactions among bacteria and with their animal and plant hosts.

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          Most cited references354

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          Gut microbiota in human metabolic health and disease

          Observational findings achieved during the past two decades suggest that the intestinal microbiota may contribute to the metabolic health of the human host and, when aberrant, to the pathogenesis of various common metabolic disorders including obesity, type 2 diabetes, non-alcoholic liver disease, cardio-metabolic diseases and malnutrition. However, to gain a mechanistic understanding of how the gut microbiota affects host metabolism, research is moving from descriptive microbiota census analyses to cause-and-effect studies. Joint analyses of high-throughput human multi-omics data, including metagenomics and metabolomics data, together with measures of host physiology and mechanistic experiments in humans, animals and cells hold potential as initial steps in the identification of potential molecular mechanisms behind reported associations. In this Review, we discuss the current knowledge on how gut microbiota and derived microbial compounds may link to metabolism of the healthy host or to the pathogenesis of common metabolic diseases. We highlight examples of microbiota-targeted interventions aiming to optimize metabolic health, and we provide perspectives for future basic and translational investigations within the nascent and promising research field.
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            Quorum sensing: cell-to-cell communication in bacteria.

            Bacteria communicate with one another using chemical signal molecules. As in higher organisms, the information supplied by these molecules is critical for synchronizing the activities of large groups of cells. In bacteria, chemical communication involves producing, releasing, detecting, and responding to small hormone-like molecules termed autoinducers . This process, termed quorum sensing, allows bacteria to monitor the environment for other bacteria and to alter behavior on a population-wide scale in response to changes in the number and/or species present in a community. Most quorum-sensing-controlled processes are unproductive when undertaken by an individual bacterium acting alone but become beneficial when carried out simultaneously by a large number of cells. Thus, quorum sensing confuses the distinction between prokaryotes and eukaryotes because it enables bacteria to act as multicellular organisms. This review focuses on the architectures of bacterial chemical communication networks; how chemical information is integrated, processed, and transduced to control gene expression; how intra- and interspecies cell-cell communication is accomplished; and the intriguing possibility of prokaryote-eukaryote cross-communication.
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              Two-component signal transduction.

              Most prokaryotic signal-transduction systems and a few eukaryotic pathways use phosphotransfer schemes involving two conserved components, a histidine protein kinase and a response regulator protein. The histidine protein kinase, which is regulated by environmental stimuli, autophosphorylates at a histidine residue, creating a high-energy phosphoryl group that is subsequently transferred to an aspartate residue in the response regulator protein. Phosphorylation induces a conformational change in the regulatory domain that results in activation of an associated domain that effects the response. The basic scheme is highly adaptable, and numerous variations have provided optimization within specific signaling systems. The domains of two-component proteins are modular and can be integrated into proteins and pathways in a variety of ways, but the core structures and activities are maintained. Thus detailed analyses of a relatively small number of representative proteins provide a foundation for understanding this large family of signaling proteins.
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                Author and article information

                Contributors
                Journal
                FEMS Microbiol Rev
                FEMS Microbiol Rev
                femsre
                FEMS Microbiology Reviews
                Oxford University Press
                0168-6445
                1574-6976
                November 2021
                06 July 2021
                06 July 2021
                : 45
                : 6
                : fuab038
                Affiliations
                Max Planck Institute for Terrestrial Microbiology & Center for Synthetic Microbiology (SYNMIKRO) , Karl-von-Frisch Strasse 16, Marburg D-35043, Germany
                Max Planck Institute for Terrestrial Microbiology & Center for Synthetic Microbiology (SYNMIKRO) , Karl-von-Frisch Strasse 16, Marburg D-35043, Germany
                College of Resources and Environmental Science, National Academy of Agriculture Green Development, China Agricultural University , Yuanmingyuan Xilu No. 2, Beijing 100193, China
                Institute of Microbiology , D-BIOL, ETH Zürich, Vladimir-Prelog-Weg 4, Zürich 8093, Switzerland
                Max Planck Institute for Terrestrial Microbiology & Center for Synthetic Microbiology (SYNMIKRO) , Karl-von-Frisch Strasse 16, Marburg D-35043, Germany
                Author notes
                Corresponding author: Max Planck Institute for Terrestrial Microbiology & Center for Synthetic Microbiology (SYNMIKRO), D-35043 Marburg, Germany. Tel: +49 6421 28 21400; E-mail: victor.sourjik@ 123456synmikro.mpi-marburg.mpg.de

                Remy Colin and Bin Ni are authors equally contributed to this work.

                Author information
                https://orcid.org/0000-0001-9051-8003
                https://orcid.org/0000-0003-1053-9192
                Article
                fuab038
                10.1093/femsre/fuab038
                8632791
                34227665
                94f02709-561a-4244-9a75-16854ac1dfe5
                © The Author(s) 2021. Published by Oxford University Press on behalf of FEMS.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 05 May 2021
                : 02 July 2021
                Page count
                Pages: 19
                Funding
                Funded by: Deutsche Forschungsgemeinschaft, DOI 10.13039/501100001659;
                Award ID: CO1813/2-1
                Award ID: 4572/1-1
                Categories
                Review Article
                AcademicSubjects/SCI01150

                Microbiology & Virology
                chemotaxis,motility,escherichia coli,environmental adaptation,physiology
                Microbiology & Virology
                chemotaxis, motility, escherichia coli, environmental adaptation, physiology

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