Dataset Information

Insect Gut Symbiont Susceptibility to Host Antimicrobial Peptides Caused by Alteration of the Bacterial Cell Envelope.

ABSTRACT: The molecular characterization of symbionts is pivotal for understanding the cross-talk between symbionts and hosts. In addition to valuable knowledge obtained from symbiont genomic studies, the biochemical characterization of symbionts is important to fully understand symbiotic interactions. The bean bug (Riptortus pedestris) has been recognized as a useful experimental insect gut symbiosis model system because of its cultivatable Burkholderia symbionts. This system is greatly advantageous because it allows the acquisition of a large quantity of homogeneous symbionts from the host midgut. Using these naïve gut symbionts, it is possible to directly compare in vivo symbiotic cells with in vitro cultured cells using biochemical approaches. With the goal of understanding molecular changes that occur in Burkholderia cells as they adapt to the Riptortus gut environment, we first elucidated that symbiotic Burkholderia cells are highly susceptible to purified Riptortus antimicrobial peptides. In search of the mechanisms of the increased immunosusceptibility of symbionts, we found striking differences in cell envelope structures between cultured and symbiotic Burkholderia cells. The bacterial lipopolysaccharide O antigen was absent from symbiotic cells examined by gel electrophoretic and mass spectrometric analyses, and their membranes were more sensitive to detergent lysis. These changes in the cell envelope were responsible for the increased susceptibility of the Burkholderia symbionts to host innate immunity. Our results suggest that the symbiotic interactions between the Riptortus host and Burkholderia gut symbionts induce bacterial cell envelope changes to achieve successful gut symbiosis.

SUBMITTER: Kim JK

PROVIDER: S-EPMC4543662 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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Insect Gut Symbiont Susceptibility to Host Antimicrobial Peptides Caused by Alteration of the Bacterial Cell Envelope.

Kim Jiyeun Kate JK Son Dae Woo DW Kim Chan-Hee CH Cho Jae Hyun JH Marchetti Roberta R Silipo Alba A Sturiale Luisa L Park Ha Young HY Huh Ye Rang YR Nakayama Hiroshi H Fukatsu Takema T Molinaro Antonio A Lee Bok Luel BL

The Journal of biological chemistry 20150626 34

The molecular characterization of symbionts is pivotal for understanding the cross-talk between symbionts and hosts. In addition to valuable knowledge obtained from symbiont genomic studies, the biochemical characterization of symbionts is important to fully understand symbiotic interactions. The bean bug (Riptortus pedestris) has been recognized as a useful experimental insect gut symbiosis model system because of its cultivatable Burkholderia symbionts. This system is greatly advantageous beca ...[more]

PMID: 26116716

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Project description: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, Dysdercus fasciatus, 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.IMPORTANCE 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.

Project description:Insects share an intimate relationship with their gut microflora and this symbiotic association has developed into an essential evolutionary outcome intended for their survival through extreme environmental conditions. While it has been clearly established that insects, with very few exceptions, associate with several microbes during their life cycle, information regarding several aspects of these associations is yet to be fully unraveled. Acquisition of bacteria by insects marks the onset of microbial symbiosis, which is followed by the adaptation of these bacterial species to the gut environment for prolonged sustenance and successful transmission across generations. Although several insect-microbiome associations have been reported and each with their distinctive features, diversifications and specializations, it is still unclear as to what led to these diversifications. Recent studies have indicated the involvement of various evolutionary processes operating within an insect body that govern the transition of a free-living microbe to an obligate or facultative symbiont and eventually leading to the establishment and diversification of these symbiotic relationships. Data from various studies, summarized in this review, indicate that the symbiotic partners, i.e., the bacteria and the insect undergo several genetic, biochemical and physiological changes that have profound influence on their life cycle and biology. An interesting outcome of the insect-microbe interaction is the compliance of the microbial partner to its eventual genome reduction. Endosymbionts possess a smaller genome as compared to their free-living forms, and thus raising the question what is leading to reductive evolution in the microbial partner. This review attempts to highlight the fate of microbes within an insect body and its implications for both the bacteria and its insect host. While discussion on each specific association would be too voluminous and outside the scope of this review, we present an overview of some recent studies that contribute to a better understanding of the evolutionary trajectory and dynamics of the insect-microbe association and speculate that, in the future, a better understanding of the nature of this interaction could pave the path to a sustainable and environmentally safe way for controlling economically important pests of crop plants.

Dataset Information

Insect Gut Symbiont Susceptibility to Host Antimicrobial Peptides Caused by Alteration of the Bacterial Cell Envelope.

Publications

Insect Gut Symbiont Susceptibility to Host Antimicrobial Peptides Caused by Alteration of the Bacterial Cell Envelope.

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