Dataset Information

Pleiotropic impact of endosymbiont load and co-occurrence in the maize weevil Sitophilus zeamais.

ABSTRACT: Individual traits vary among and within populations, and the co-occurrence of different endosymbiont species within a host may take place under varying endosymbiont loads in each individual host. This makes the recognition of the potential impact of such endosymbiont associations in insect species difficult, particularly in insect pest species. The maize weevil, Sitophilus zeamais Motsch. (Coleoptera: Curculionidae), a key pest species of stored cereal grains, exhibits associations with two endosymbiotic bacteria: the obligatory endosymbiont SZPE ("Sitophilus zeamais Primary Endosymbiont") and the facultative endosymbiont Wolbachia. The impact of the lack of SZPE in maize weevil physiology is the impairment of nutrient acquisition and energy metabolism, while Wolbachia is an important factor in reproductive incompatibility. However, the role of endosymbiont load and co-occurrence in insect behavior, grain consumption, body mass and subsequent reproductive factors has not yet been explored. Here we report on the impacts of co-occurrence and varying endosymbiont loads achieved via thermal treatment and antibiotic provision via ingested water in the maize weevil. SZPE exhibited strong effects on respiration rate, grain consumption and weevil body mass, with observed effects on weevil behavior, particularly flight activity, and potential consequences for the management of this pest species. Wolbachia directly favored weevil fertility and exhibited only mild indirect effects, usually enhancing the SZPE effect. SZPE suppression delayed weevil emergence, which reduced the insect population growth rate, and the thermal inactivation of both symbionts prevented insect reproduction. Such findings are likely important for strain divergences reported in the maize weevil and their control, aspects still deserving future attention.

SUBMITTER: Carvalho GA

PROVIDER: S-EPMC4210188 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Pleiotropic impact of endosymbiont load and co-occurrence in the maize weevil Sitophilus zeamais.

Carvalho Gislaine A GA Vieira Juliana L JL Haro Marcelo M MM Corrêa Alberto S AS Ribon Andrea Oliveira B AO de Oliveira Luiz Orlando LO Guedes Raul Narciso C RN

PloS one 20141027 10

Individual traits vary among and within populations, and the co-occurrence of different endosymbiont species within a host may take place under varying endosymbiont loads in each individual host. This makes the recognition of the potential impact of such endosymbiont associations in insect species difficult, particularly in insect pest species. The maize weevil, Sitophilus zeamais Motsch. (Coleoptera: Curculionidae), a key pest species of stored cereal grains, exhibits associations with two endo ...[more]

PMID: 25347417

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Project description:BackgroundInsects thriving on nutritionally poor habitats have integrated mutualistic intracellular symbiotic bacteria (endosymbionts) in a bacteria-bearing tissue (the bacteriome) that isolates the endosymbionts and protects them against a host systemic immune response. Whilst the metabolic and physiological features of long-term insect associations have been investigated in detail over the past decades, cellular and immune regulations that determine the host response to endosymbionts and pathogens have attracted interest more recently.ResultsTo investigate bacteriome cellular specificities and weevil immune responses to bacteria, we have constructed and sequenced 7 cDNA libraries from Sitophilus oryzae whole larvae and bacteriomes. Bioinformatic analysis of 26,886 ESTs led to the generation of 8,941 weevil unigenes. Based on in silico analysis and on the examination of genes involved in the cellular pathways of potential interest to intracellular symbiosis (i.e. cell growth and apoptosis, autophagy, immunity), we have selected and analyzed 29 genes using qRT-PCR, taking into consideration bacteriome specificity and symbiosis impact on the host response to pathogens. We show that the bacteriome tissue accumulates transcripts from genes involved in cellular development and survival, such as the apoptotic inhibitors iap2 and iap3, and endosomal fusion and trafficking, such as Rab7, Hrs, and SNARE. As regards our investigation into immunity, we first strengthen the bacteriome immunomodulation previously reported in S. zeamais. We show that the sarcotoxin, the c-type lysozyme, and the wpgrp2 genes are downregulated in the S. oryzae bacteriome, when compared to aposymbiotic insects and insects challenged with E. coli. Secondly, transcript level comparison between symbiotic and aposymbiotic larvae provides evidence that the immune systemic response to pathogens is decreased in symbiotic insects, as shown by the relatively high expression of wpgrp2, wpgrp3, coleoptericin-B, diptericin, and sarcotoxin genes in aposymbiotic insects.ConclusionsLibrary sequencing significantly increased the number of unigenes, allowing for improved functional and genetic investigations in the cereal weevil S. oryzae. Transcriptomic analyses support selective and local immune gene expression in the bacteriome tissue and uncover cellular pathways that are of potential interest to bacteriocyte survival and homeostasis. Bacterial challenge experiments have revealed that the systemic immune response would be less induced in a symbiotic insect, thus highlighting new perspectives on host immunity in long-term invertebrate co-evolutionary associations.

Dataset Information

Pleiotropic impact of endosymbiont load and co-occurrence in the maize weevil Sitophilus zeamais.

Publications

Pleiotropic impact of endosymbiont load and co-occurrence in the maize weevil Sitophilus zeamais.

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