Search bioRxiv⌕ Search

Biology subjects

Zaidman-Remy, A.

Publications and source records attributed to Zaidman-Remy, A..

5 recordsLinked to original sources

Cereal Weevil's Antimicrobial Peptides: At the Crosstalk between Development, Endosymbiosis and Immune Response

Interactions between animals and microbes are ubiquitous in nature and strongly impact animal physiology. These interactions are shaped by the host immune system, which responds to infections and contributes to tailor the associations with beneficial microorganisms. In many insects, beneficial symbiotic associations not only include gut commensals, but also intracellular bacteria, or endosymbionts. Endosymbionts are housed within specialised host cells, the bacteriocytes, and are transmitted vertically across host generations. Host-endosymbiont co-evolution shapes the endosymbiont genome and host immune system, which not only fights against microbial intruders, but also ensures the preservation of endosymbionts and the control of their load and location. The cereal weevil Sitophilus spp. is a remarkable model to study the evolutionary adaptation of the immune system to endosymbiosis since its binary association with a unique, relatively recently acquired nutritional endosymbiont, Sodalis pierantonius. This Gram-negative bacterium has not experienced the genome size shrinkage observed in long-term endosymbioses and has retained immunogenicity. We focus here on the 16 antimicrobial peptides (AMPs) identified in the Sitophilus oryzae genome and their expression patterns in different tissues, along host development or upon immune challenges, to address their potential functions in the defensive response and endosymbiosis homeostasis along the insect life cycle.

immunology↗

Coordination of host and endosymbiont gene expression governs endosymbiont growth and elimination in the cereal weevil Sitophilus spp.

BackgroundInsects living in nutritionally poor environments often establish long-term relationships with intracellular bacteria that supplement their diets and improve their adaptive and invasive powers. Even though these symbiotic associations have been extensively studied on physiological, ecological and evolutionary levels, few studies have focused on the molecular dialogue between host and endosymbionts to identify genes and pathways involved in endosymbiosis control and dynamics throughout host development. ResultsWe simultaneously analyzed host and endosymbiont gene expression during the life cycle of the cereal weevil Sitophilus oryzae, from larval stages to adults, with a particular emphasis on emerging adults where the endosymbiont Sodalis pierantonius experiences a contrasted growth-climax-elimination dynamics. We unraveled a constant arms race in which different biological functions are intertwined and coregulated across both partners. These include immunity, metabolism, metal control, apoptosis, and bacterial stress response. ConclusionsThe study of these tightly regulated functions, which are at the center of symbiotic regulations, provides evidence on how hosts and bacteria finely tune their gene expression and respond to different physiological challenges constrained by insect development in a nutritionally limited ecological niche. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=143 HEIGHT=200 SRC="FIGDIR/small/535335v2_ufig1.gif" ALT="Figure 1"> View larger version (42K): org.highwire.dtl.DTLVardef@800121org.highwire.dtl.DTLVardef@1ca2c25org.highwire.dtl.DTLVardef@183d56org.highwire.dtl.DTLVardef@163074f_HPS_FORMAT_FIGEXP M_FIG C_FIG

bioinformatics↗

Transcriptional survey of ovarian bacteriomes in the cereal weevil, Sitophilus oryzae, shows down-regulation of immune effectors at the onset of sexual maturity

Insects often establish long-term relationships with intracellular symbiotic bacteria, i.e. endosymbionts, that provide them with essential nutrients such as amino acids and vitamins. Endosymbionts are typically confined within specialized host cells called bacteriocytes that may form an organ, the bacteriome. Compartmentalization within host cells is paramount for protecting the endosymbionts and also avoiding chronic activation of the host immune system. In the cereal weevil Sitophilus oryzae, bacteriomes are present as a single organ at the larval foregut-midgut junction, and in adults, at the apex of midgut mesenteric caeca and at the apex of the four ovarioles. While the adult midgut endosymbionts experience a drastic proliferation during early adulthood followed by complete elimination through apoptosis and autophagy, ovarian endosymbionts are maintained throughout the weevil lifetime by unknown mechanisms. Bacteria present in ovarian bacteriomes are thought to be involved in the maternal transmission of endosymbionts through infection of the female germline, but the exact mode of transmission is not fully understood. Here, we show that endosymbionts are able to colonize the germarium in one-week-old females, pinpointing a potential infection route of oocytes. To identify potential immune regulators of ovarian endosymbionts, we have analyzed the transcriptomes of the ovarian bacteriomes through young adult development, from one-day-old adults to sexually mature ones. In contrast with midgut bacteriomes, immune effectors are downregulated in ovarian bacteriomes at the onset of sexual maturation. We hypothesize that relaxation of endosymbiont control by antimicrobial peptides might allow bacterial migration and potential oocyte infection, ensuring endosymbiont transmission.

immunology↗

Transcriptomic-based selection of reference genes for quantitative real-time PCR in an insect endosymbiotic model

Reference genes are a fundamental tool for analyses of gene expression by real-time quantitative PCR (qRT-PCR), in that they ensure the correct comparison between conditions, stages, or treatments. Because of this, selection of appropriate genes to use as references is crucial for proper application of the technique. Nevertheless, efforts to find appropriate, stably expressed transcripts are still lacking, in particular in the field of insect science. Here, we took advantage of a massive transcriptomic high-throughput analysis of various developmental stages of the gut and associated-bacteriomes of the cereal weevil Sitophilus oryzae and identified a subset of stably expressed genes with the potential to be used as housekeeping genes from the larva to the adult stage. We employed several normalization techniques to select the most suitable genes among our subset. Our final selection includes three genes - TAO, YTH3 and PP12A - which can also be used to compare transcript abundance at various developmental stages in symbiotic insects, and in insects devoid of endosymbionts (aposymbiotic). Since they are well conserved, these genes have the potential to be useful for many other insect species. This work confirms the interest in using large-scale, unbiased methods for reference gene selection.

molecular biology↗

Antimicrobial peptide secretion protects endosymbionts from bacteriome autoimmunity in insects

BackgroundMany insects house symbiotic intracellular bacteria (endosymbionts) that provide them with essential nutrients, thus promoting usage of nutrient-poor habitats. Endosymbiont seclusion within host specialized cells, called bacteriocytes, often organized in a dedicated organ, the bacteriome, is crucial in protecting them from host immune defenses while avoiding chronic host immune activation. Previous evidence obtained in the cereal weevil Sitophilus oryzae has shown that bacteriome immunity is activated against invading pathogens, suggesting endosymbionts might be targeted and impacted by immune effectors during an immune challenge. To pinpoint any molecular determinants associated with such challenges, we conducted a dual transcriptomic analysis of S. oryzaes bacteriome subjected to immunogenic peptidoglycan fragments. ResultsWe show that upon immune challenge the bacteriome actively participates in the innate immune response via an induction of antimicrobial peptides (AMPs). Surprisingly, endosymbionts do not undergo any transcriptomic changes, indicating that this potential threat goes unnoticed. Immunohistochemistry showed that TCT-induced AMPs are located outside the bacteriome, excluding direct contact with the endosymbionts. ConclusionsThis work demonstrates that endosymbiont protection during an immune challenge is mainly achieved by efficient confinement within bacteriomes, which provides physical separation between host systemic response and endosymbionts.

immunology↗