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First arrived takes all: inhibitory priority effects dominate competition between co-infecting Borrelia burgdorferi strains

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      Abstract

      Background

      Within-host microbial communities and interactions among microbes are increasingly recognized as important factors influencing host health and pathogen transmission. The microbial community associated with a host is indeed influenced by a complex network of direct and indirect interactions between the host and the lineages of microbes it harbors, but the mechanisms are rarely established. We investigated the within-host interactions among strains of Borrelia burgdorferi, the causative agent of Lyme disease, using experimental infections in mice. We used a fully crossed-design with three distinct strains, each group of hosts receiving two sequential inoculations. We used data from these experimental infections to assess the effect of coinfection on bacterial dissemination and fitness (by measuring the transmission of bacteria to xenodiagnostic ticks) as well as the effect of coinfection on host immune response compared to single infection.

      Results

      The infection and transmission data strongly indicate a competitive interaction among B. burgdorferi strains within a host in which the order of appearance of the strain is the main determinant of the competitive outcome. This pattern is well described by the classic priority effect in the ecological literature. In all cases, the primary strain a mouse was infected with had an absolute fitness advantage primarily since it was transmitted an order of magnitude more than the secondary strain. The mechanism of exclusion of the secondary strain is an inhibition of the colonization of mouse tissues, even though 29% of mice showed some evidence of infection by secondary strain. Contrary to expectation, the strong and specific adaptive immune response evoked against the primary strain was not followed by production of immunoglobulins after the inoculation of the secondary strain, neither against strain-specific antigen nor against antigens common to all strains. Hence, the data do not support a major role of the immune response in the observed priority effect.

      Conclusion

      The strong inhibitory priority effect is a dominant mechanism underlying competition for transmission between coinfecting B. burgdorferi strains, most likely through resource exploitation. The observed priority effect could shape bacterial diversity in nature, with consequences in epidemiology and evolution of the disease.

      Electronic supplementary material

      The online version of this article (doi:10.1186/s12866-015-0381-0) contains supplementary material, which is available to authorized users.

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      Most cited references 48

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      Host-bacterial mutualism in the human intestine.

      The distal human intestine represents an anaerobic bioreactor programmed with an enormous population of bacteria, dominated by relatively few divisions that are highly diverse at the strain/subspecies level. This microbiota and its collective genomes (microbiome) provide us with genetic and metabolic attributes we have not been required to evolve on our own, including the ability to harvest otherwise inaccessible nutrients. New studies are revealing how the gut microbiota has coevolved with us and how it manipulates and complements our biology in ways that are mutually beneficial. We are also starting to understand how certain keystone members of the microbiota operate to maintain the stability and functional adaptability of this microbial organ.
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        Ecological and evolutionary forces shaping microbial diversity in the human intestine.

        The human gut is populated with as many as 100 trillion cells, whose collective genome, the microbiome, is a reflection of evolutionary selection pressures acting at the level of the host and at the level of the microbial cell. The ecological rules that govern the shape of microbial diversity in the gut apply to mutualists and pathogens alike.
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          The ecology of genetically diverse infections.

          Microparasite infections often consist of genetically distinct clonal lineages. Ecological interactions between these lineages within hosts can influence disease severity, epidemiology, and evolution. Many medical and veterinary interventions have an impact on genetic diversity within infections, but there is little understanding of the long-term consequences of such interventions for public and animal health. Indeed, much of the theory in this area is based on assumptions contradicted by the available data.
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            Author and article information

            Affiliations
            [ ]Department of Biology, Leidy Laboratories, University of Pennsylvania, Hamilton Walk, Philadelphia, PA 19104 USA
            [ ]Institute of Evolutionary Biology, Ashworth Laboratories, University of Edinburgh, King’s Building Campus, EH9 3JT Edinburgh, UK
            [ ]Department of Integrative Biology, Oregon State University, Corvallis, OR 97331 USA
            [ ]Department of Ecology and Evolutionary Biology, Walter Hall, Brown University, 80 Waterman Street, Providence, RI 02912 USA
            Contributors
            godefroy.devevey@ed.ac.uk
            trangdn.dang@gmail.com
            cjgraves3@gmail.com
            murs@sas.upenn.edu
            dbrisson@sas.upenn.edu
            Journal
            BMC Microbiol
            BMC Microbiol
            BMC Microbiology
            BioMed Central (London )
            1471-2180
            7 March 2015
            7 March 2015
            2015
            : 15
            4359528 381 10.1186/s12866-015-0381-0
            © Devevey et al.; licensee BioMed Central. 2015

            This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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            © The Author(s) 2015

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