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      Diversity of bet‐hedging strategies in microbial communities—Recent cases and insights

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          Abstract

          Microbial communities are continuously exposed to unpredictable changes in their environment. To thrive in such dynamic habitats, microorganisms have developed the ability to readily switch phenotypes, resulting in a number of differently adapted subpopulations expressing various traits. In evolutionary biology, a particular case of phenotypic heterogeneity that evolved in an unpredictably changing environment has been defined as bet‐hedging. Bet‐hedging is a risk‐spreading strategy where isogenic populations stochastically (randomly) diversify their phenotypes, often resulting in maladapted individuals that suffer lower reproductive success. This fitness trade‐off in a specific environment may have a selective advantage upon the sudden environmental shift. Thus, a bet‐hedging strategy allows populations to persist in very dynamic habitats, but with a particular fitness cost. In recent years, numerous examples of phenotypic heterogeneity in different microorganisms have been observed, some suggesting bet‐hedging. Here, we highlight the latest reports concerning bet‐hedging phenomena in various microorganisms to show how versatile this strategy is within the microbial realms.

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          • Infectious Diseases > Molecular and Cellular Physiology

          Abstract

          Overview of recent studies on phenotypic heterogeneity and possible employment of bet‐hedging strategies in various microorganisms. In this work, we highlight some recent studies regarding bet‐hedging traits that fall into several categories of microbial lifestyle, including signaling (purple), dormancy (yellow), and resource use (blue). In some cases, the same population manifests different bet‐hedging strategies because of direct or indirect relationships between traits. With an asterisk, we marked examples of studies where a population was shown to employ several bet‐hedging strategies, for example, nutrient utilization is directly involved in spore or persisters formation.

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          Most cited references136

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          Bacterial persistence as a phenotypic switch.

          A fraction of a genetically homogeneous microbial population may survive exposure to stress such as antibiotic treatment. Unlike resistant mutants, cells regrown from such persistent bacteria remain sensitive to the antibiotic. We investigated the persistence of single cells of Escherichia coli with the use of microfluidic devices. Persistence was linked to preexisting heterogeneity in bacterial populations because phenotypic switching occurred between normally growing cells and persister cells having reduced growth rates. Quantitative measurements led to a simple mathematical description of the persistence switch. Inherent heterogeneity of bacterial populations may be important in adaptation to fluctuating environments and in the persistence of bacterial infections.
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            Stochasticity in gene expression: from theories to phenotypes.

            Genetically identical cells exposed to the same environmental conditions can show significant variation in molecular content and marked differences in phenotypic characteristics. This variability is linked to stochasticity in gene expression, which is generally viewed as having detrimental effects on cellular function with potential implications for disease. However, stochasticity in gene expression can also be advantageous. It can provide the flexibility needed by cells to adapt to fluctuating environments or respond to sudden stresses, and a mechanism by which population heterogeneity can be established during cellular differentiation and development.
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              Persister cells, dormancy and infectious disease.

              Kim Lewis (2007)
              Several well-recognized puzzles in microbiology have remained unsolved for decades. These include latent bacterial infections, unculturable microorganisms, persister cells and biofilm multidrug tolerance. Accumulating evidence suggests that these seemingly disparate phenomena result from the ability of bacteria to enter into a dormant (non-dividing) state. The molecular mechanisms that underlie the formation of dormant persister cells are now being unravelled and are the focus of this Review.
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                Author and article information

                Contributors
                o.p.kuipers@rug.nl
                Journal
                WIREs Mech Dis
                WIREs Mech Dis
                10.1002/(ISSN)2692-9368
                WSBM
                Wires Mechanisms of Disease
                John Wiley & Sons, Inc. (Hoboken, USA )
                2692-9368
                01 November 2021
                Mar-Apr 2022
                : 14
                : 2 ( doiID: 10.1002/wsbm.v14.2 )
                : e1544
                Affiliations
                [ 1 ] Department of Molecular Genetics Groningen Biomolecular Sciences and Biotechnology Institute Groningen The Netherlands
                [ 2 ]Present address: IFF Health & Biosciences Oegstgeest The Netherlands
                Author notes
                [*] [* ] Correspondence

                Oscar P. Kuipers, Department of Molecular Genetics, Groningen Biomolecular Sciences and Biotechnology Institute, Nijenborgh 7, Groningen 9747 AG, The Netherlands.

                Email: o.p.kuipers@ 123456rug.nl

                Author information
                https://orcid.org/0000-0003-2781-3610
                https://orcid.org/0000-0001-9186-4792
                https://orcid.org/0000-0001-5596-7735
                Article
                WSBM1544
                10.1002/wsbm.1544
                9286555
                35266649
                af8b563d-46f0-4f88-b6e9-2104dd6fc6f1
                © 2021 The Authors. WIREs Mechanisms of Disease published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 05 October 2021
                : 11 January 2021
                : 07 October 2021
                Page count
                Figures: 5, Tables: 0, Pages: 15, Words: 11602
                Funding
                Funded by: BE‐Basic R&D Program
                Funded by: Christian Hansen company, Denmark
                Funded by: the Netherlands Organization for Scientific Research (NWO)
                Award ID: 13858
                Categories
                Molecular and Cellular Physiology
                Focus Article
                Focus Article
                Custom metadata
                2.0
                March/April 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.7 mode:remove_FC converted:15.07.2022

                adaptation,bet‐hedging,evolutionary strategy,persisters,phenotypic heterogeneity

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