Natural variation in the contribution of microbial density to inducible immune dynamics

Natural variation in the contribution of microbial density to inducible immune dynamics
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DOI:
10.1111/mec.15293
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发表时间:
2019-11-21
期刊:
影响因子:
4.9
通讯作者:
Tate, Ann T.
Tate, Ann T.
中科院分区:
生物学1区
文献类型:
--
作者:
Jent, Derrick;Perry, Abby;Tate, Ann T.

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免疫反应的进化是为了平衡微生物杀死的好处与自身免疫和能量资源使用的成本。探索最佳免疫反应进化的模型通常包括一个术语,即结构性免疫,即微生物暴露前的免疫投资水平,以及诱导免疫,或微生物挑战后的免疫功能投资。然而,尽管免疫系统的进化理论上依赖于微生物对宿主的损害,但研究很少考虑可诱导免疫反应的功能形式与微生物密度的关系。在本研究中,我们分析了七个野生捕获的粉甲种群(Tribolium spp.)在苏云金芽孢杆菌(Bt)和发光杆菌(P.lum)的急性感染过程中,证明了体液IMD途径介导的可诱导免疫反应在微生物密度依赖和独立时间动力学上都表现出自然变化。对Bt密度表现出更高的AMP表达敏感性的甲虫种群也更有可能死于感染,而表现出更高的微生物密度非依赖性AMP表达的种群更有可能在发光菌感染下存活下来。通过RNAi介导的IMD基因敲除降低了途径信号效率,降低了微生物独立和依赖反应的幅度,降低了寄主对Bt生长的抗性,但对寄主存活没有净影响。这项研究为理解可诱导免疫反应投资灵活性的自然变异提供了一个框架,并将为关于非平衡宿主-微生物动态对免疫系统进化的贡献的理论提供信息。
Immune responses evolve to balance the benefits of microbial killing against the costs of autoimmunity and energetic resource use. Models that explore the evolution of optimal immune responses generally include a term for constitutive immunity, or the level of immunological investment prior to microbial exposure, and for inducible immunity, or investment in immune function after microbial challenge. However, studies rarely consider the functional form of inducible immune responses with respect to microbial density, despite the theoretical dependence of immune system evolution on microbe- versus immune-mediated damage to the host. In this study, we analyse antimicrobial peptide (AMP) gene expression from seven wild-caught flour beetle populations (Tribolium spp.) during acute infection with the virulent bacteria Bacillus thuringiensis (Bt) and Photorhabdus luminescens (P.lum) to demonstrate that inducible immune responses mediated by the humoral IMD pathway exhibit natural variation in both microbe density-dependent and independent temporal dynamics. Beetle populations that exhibited greater AMP expression sensitivity to Bt density were also more likely to die from infection, while populations that exhibited higher microbe density-independent AMP expression were more likely to survive P. luminescens infection. Reduction in pathway signalling efficiency through RNAi-mediated knockdown of the imd gene reduced the magnitude of both microbe-independent and dependent responses and reduced host resistance to Bt growth, but had no net effect on host survival. This study provides a framework for understanding natural variation in the flexibility of investment in inducible immune responses and should inform theory on the contribution of nonequilibrium host-microbe dynamics to immune system evolution.