Abstract
The acquisition and vertical transmission of bacterial symbionts plays an important role in insect evolution and ecology. However, the molecular mechanisms underlying the stable maintenance and control of mutualistic bacteria remain poorly understood. The cotton stainer Dysdercus fasciatus harbours the actinobacterial symbionts Coriobacterium glomerans and Gordonibacter sp. in its midgut. The symbionts supplement limiting B vitamins and thereby significantly contribute to the host’s fitness. In this study, we experimentally disrupted the symbionts’ vertical transmission route and performed comparative transcriptomic analyses of genes expressed in the gut of aposymbiotic (symbiont-free) and control individuals to study the host immune response in presence and absence of the mutualists. Annotation of assembled cDNA reads identified a considerable number of genes involved in the innate immune system, including different protein isoforms of several immune effector proteins (specifically i-type lysozyme, defensin, hemiptericin, and pyrrhocoricin), suggesting the possibility for a highly differentiated response towards the complex resident microbial community. Gene expression analyses revealed a constitutive expression of transcripts involved in signal transduction of the main insect immune pathways, but differential expression of certain antimicrobial peptide genes. Specifically, qPCRs confirmed the significant down-regulation of c-type lysozyme and up-regulation of hemiptericin in aposymbiotic individuals. The high expression of c-type lysozyme in symbiont-containing bugs may serve to lyse symbiont cells and thereby harvest B-vitamins that are necessary for subsistence on the deficient diet of Malvales seeds. Our findings suggest a sophisticated host response to perturbation of the symbiotic gut microbiota, indicating that the innate immune system not only plays an important role in combating pathogens, but also serves as a communication interface between host and symbionts.
Highlights
One of the reasons for the ecological success of insects is the acquisition and vertical transmission of bacterial symbionts [1]
Our findings suggest a sophisticated host response to perturbation of the symbiotic gut microbiota, indicating that the innate immune system plays an important role in combating pathogens, and serves as a communication interface between host and symbionts
We investigated the immune response of D. fasciatus with respect to symbiont perturbation by a comparative transcriptomic analysis of midgut samples from aposymbiotic and symbiotic individuals
Summary
One of the reasons for the ecological success of insects is the acquisition and vertical transmission of bacterial symbionts [1]. Intestinal associations with microorganisms have been shown to be beneficial for the host by the provision of nutrients important for growth [5]. Controlling and maintaining these populations of gut microbes is a challenging task for the host: While certain microorganisms are beneficial, others are detrimental and can lead to fitness disadvantages. This fine-tuned regulation is realized by the innate immune system, which serves as a communication interface between host and symbiont to guide and modulate cooperative interactions [7]
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