Department for Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Mainz, Germany.
Department for Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Mainz, Germany
Appl Environ Microbiol. 2019 Jun 17;85(13). doi: 10.1128/AEM.00738-19. Print 2019 Jul 1.
Symbioses with microorganisms are ubiquitous in nature and confer important ecological traits to animal hosts but also require control mechanisms to ensure homeostasis of the symbiotic interactions. In addition to protecting hosts against pathogens, animal immune systems recognize, respond to, and regulate mutualists. The gut bacterial symbionts of the cotton stainer bug, , elicit an immune response characterized by the upregulation of c-type lysozyme and the antimicrobial peptide pyrrhocoricin in bugs with their native gut microbiota compared to that in dysbiotic insects. In this study, we investigated the impact of the elicited antimicrobial immune response on the established cotton stainer gut bacterial symbiont populations. To this end, we used RNA interference (RNAi) to knock down immunity-related genes hypothesized to regulate the symbionts, and we subsequently measured the effect of this silencing on host fitness and on the abundance of the major gut bacterial symbionts. Despite successful downregulation of target genes by both ingestion and injection of double-stranded RNA (dsRNA), the silencing of immunity-related genes had no effect on either host fitness or the qualitative and quantitative composition of established gut bacterial symbionts, indicating that the host immune responses are not actively involved in the regulation of the nutritional and defensive gut bacterial mutualists. These results suggest that close associations of bacterial symbionts with their hosts can result in the evolution of mechanisms ensuring that symbionts remain insensitive to host immunological responses, which may be important for the evolutionary stability of animal-microbe symbiotic associations. Animal immune systems are central for the protection of hosts against enemies by preventing or eliminating successful infections. However, in the presence of beneficial bacterial mutualists, the immune system must strike a balance of not killing the beneficial symbionts while at the same time preventing enemy attacks. Here, using the cotton stainer bug, we reveal that its long-term associated bacterial symbionts are insensitive to the host's immune effectors, suggesting adaptation to the host's defenses, thereby strengthening the stability of the symbiotic relationship. The ability of the symbionts to elicit host immune responses but remain insensitive themselves may be a mechanism by which the symbionts prime hosts to fight future pathogenic infections.
共生体与微生物在自然界中无处不在，赋予动物宿主重要的生态特征，但也需要控制机制来确保共生相互作用的体内平衡。除了保护宿主免受病原体侵害外，动物免疫系统还能识别、响应和调节共生体。与肠道菌群失调的昆虫相比，棉盲蝽的肠道共生细菌会引发免疫反应，导致 C 型溶菌酶和抗菌肽 Pyrrhocoricin 的上调。在这项研究中，我们研究了引发的抗菌免疫反应对已建立的棉盲蝽肠道细菌共生体种群的影响。为此，我们使用 RNA 干扰 (RNAi) 敲低了被假设调节共生体的免疫相关基因，然后测量了这种沉默对宿主适应性和主要肠道细菌共生体丰度的影响。尽管通过摄入和注射双链 RNA (dsRNA) 成功下调了靶基因，但免疫相关基因的沉默对宿主适应性或已建立的肠道细菌共生体的定性和定量组成均没有影响，这表明宿主免疫反应并未主动参与营养和防御性肠道细菌共生体的调节。这些结果表明，细菌共生体与宿主的紧密关联可能导致进化出确保共生体对宿主免疫反应不敏感的机制，这对于动物-微生物共生体关联的进化稳定性可能很重要。动物免疫系统是宿主抵御敌人的保护者，通过防止或消除成功的感染来实现。然而，在有益的细菌共生体存在的情况下，免疫系统必须在不杀死有益共生体的同时保持平衡，同时防止敌人的攻击。在这里，我们使用棉盲蝽揭示了其长期相关的细菌共生体对宿主免疫效应物不敏感，这表明它们对宿主防御有适应性，从而加强了共生关系的稳定性。共生体引发宿主免疫反应但自身保持不敏感的能力可能是共生体使宿主为未来的致病性感染做好准备的一种机制。
