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

First arrived takes all: inhibitory priority effects dominate competition between co-infecting Borrelia burgdorferi strains.
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DOI:
10.1186/s12866-015-0381-0
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发表时间:
2015-03-07
期刊:
影响因子:
4.2
通讯作者:
Brisson D
Brisson D
中科院分区:
生物学3区
文献类型:
--
作者:
Devevey G;Dang T;Graves CJ;Murray S;Brisson D

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宿主内微生物群落和微生物间的相互作用越来越被认为是影响宿主健康和病原体传播的重要因素。与宿主相关的微生物群落确实受到宿主与其所含微生物谱系之间直接和间接相互作用的复杂网络的影响,但机制很少建立。我们研究了莱姆病的病原体伯氏疏螺旋体菌株之间的宿主内相互作用,使用小鼠实验感染。我们使用了三种不同菌株的完全交叉设计,每组宿主接受两次连续接种。我们使用这些实验感染的数据来评估合并感染对细菌传播和适应性的影响(通过测量细菌向异种诊断蜱的传播),以及与单一感染相比,合并感染对宿主免疫反应的影响。感染和传播数据强烈表明B之间存在竞争性相互作用。在宿主内的伯氏菌株,其中菌株出现的顺序是竞争结果的主要决定因素。生态学文献中经典的优先效应对这一模式有很好的描述。在所有情况下,小鼠感染的主要菌株都具有绝对的适应性优势,主要是因为它比次要菌株传播了一个数量级。排除继发菌株的机制是抑制小鼠组织的定殖,尽管29%的小鼠显示出继发菌株感染的一些证据。与预期相反,针对主要菌株诱发的强烈和特异性的适应性免疫应答之后,接种次要菌株后未产生免疫球蛋白,既不针对菌株特异性抗原,也不针对所有菌株共有的抗原。因此,数据不支持免疫应答在观察到的优先效应中的主要作用。强抑制优先效应是共同感染B之间竞争传播的主导机制。burgdorferi菌株,很可能是通过资源开采。观察到的优先效应可以塑造自然界中的细菌多样性,从而影响疾病的流行病学和演变。本文的在线版本(doi:10.1186/s12866-015-0381-0)包含补充材料,可供授权用户使用。
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. 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. 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. 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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