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

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Title First arrived takes all: inhibitory priority effects dominate competition between co-infecting Borrelia burgdorferi strains
Names Devevey, Godefroy (creator)
Dang, Trang (creator)
Graves, Christopher J. (creator)
Murray, Sarah (creator)
Brisson, Dustin (creator)
Date Issued 2015-03-07 (iso8601)
Note This is the publisher’s final pdf. The published article is copyrighted by the author(s) and published by BioMed Central Ltd. The published article can be found at: http://www.biomedcentral.com/bmcmicrobiol/.
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.
Genre Article
Access Condition http://creativecommons.org/licenses/by/3.0/us/
Topic Borrelia burdgorferi
Identifier Devevey, G., Dang, T., Graves, C. J., Murray, S., & Brisson, D. (2015). First arrived takes all: inhibitory priority effects dominate competition between co-infecting Borrelia burgdorferi strains. BMC Microbiology, 15, 61. doi:10.1186/s12866-015-0381-0

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