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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 references46

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          Emphasizing the ecology in parasite community ecology.

          In natural systems, individuals are often co-infected by many species of parasites. However, the significance of interactions between species and the processes that shape within-host parasite communities remain unclear. Studies of parasite community ecology are often descriptive, focusing on patterns of parasite abundance across host populations rather than on the mechanisms that underlie interactions within a host. These within-host interactions are crucial for determining the fitness and transmissibility of co-infecting parasite species. Here, we highlight how techniques from community ecology can be used to restructure the approaches used to study parasite communities. We discuss insights offered by this mechanistic approach that will be crucial for predicting the impact on wildlife and human health of disease control measures, climate change or novel parasite species introductions.
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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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              Diagnosis of lyme borreliosis.

              A large amount of knowledge has been acquired since the original descriptions of Lyme borreliosis (LB) and of its causative agent, Borrelia burgdorferi sensu stricto. The complexity of the organism and the variations in the clinical manifestations of LB caused by the different B. burgdorferi sensu lato species were not then anticipated. Considerable improvement has been achieved in detection of B. burgdorferi sensu lato by culture, particularly of blood specimens during early stages of disease. Culturing plasma and increasing the volume of material cultured have accomplished this. Further improvements might be obtained if molecular methods are used for detection of growth in culture and if culture methods are automated. Unfortunately, culture is insensitive in extracutaneous manifestations of LB. PCR and culture have high sensitivity on skin samples of patients with EM whose diagnosis is based mostly on clinical recognition of the lesion. PCR on material obtained from extracutaneous sites is in general of low sensitivity, with the exception of synovial fluid. PCR on synovial fluid has shown a sensitivity of up to >90% (when using four different primer sets) in patients with untreated or partially treated Lyme arthritis, making it a helpful confirmatory test in these patients. Currently, the best use of PCR is for confirmation of the clinical diagnosis of suspected Lyme arthritis in patients who are IgG immunoblot positive. PCR should not be used as the sole laboratory modality to support a clinical diagnosis of extracutaneous LB. PCR positivity in seronegative patients suspected of having late manifestations of LB most likely represents a false-positive result. Because of difficulties in direct methods of detection, laboratory tests currently in use are mainly those detecting antibodies to B. burgdorferi sensu lato. Tests used to detect antibodies to B. burgdorferi sensu lato have evolved from the initial formats as more knowledge on the immunodominant antigens has been collected. The recommendation for two-tier testing was an attempt to standardize testing and improve specificity in the United States. First-tier assays using whole-cell sonicates of B. burgdorferi sensu lato need to be standardized in terms of antigen composition and detection threshold of specific immunoglobulin classes. The search for improved serologic tests has stimulated the development of recombinant protein antigens and the synthesis of specific peptides from immunodominant antigens. The use of these materials alone or in combination as the source of antigen in a single-tier immunoassay may someday replace the currently recommended two-tier testing strategy. Evaluation of these assays is currently being done, and there is evidence that certain of these antigens may be broadly cross-reactive with the B. burgdorferi sensu lato species causing LB in Europe.
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                Author and article information

                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
                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
                Article
                381
                10.1186/s12866-015-0381-0
                4359528
                25887119
                f4851114-1187-43df-bbc0-b076d0d6777e
                © 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.

                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Microbiology & Virology
                borrelia burdgorferi,ospc,priority effect,transmission,coinfection,strain competition,apparent competition

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