bioRxiv Science⌕ Search

Biology subjects

Renoz, F.

Publications and source records attributed to Renoz, F..

5 recordsLinked to original sources

The two-component microbial system of the black soldier fly larvae (BSFL) gut: a plastic microbiota in the midgut, but a stable one in the hindgut

Due to their highly polyphagous capacities, black soldier fly (Hermetia illucens) larvae (BSFL) are increasingly valued for their ability to convert organic waste into valuable biomass that can be used for a variety of purposes. These remarkable digestive capabilities are highly dependent on an extremely plastic gut microbiota. However, the distribution and functioning of bacterial communities in the various gut compartments - particularly in the hindgut - remain little understood. In this study, we used a metabarcoding approach based on 16S gene sequencing to investigate the effect of three carbohydrate-rich diets with distinct molecular compositions on the functional diversity of the BSFL gut microbiota. Our results showed that the midgut harbors a highly substrate-sensitive microbiota, with a high abundance of Actinomyces spp., regardless of the substrate. A bacterial diversity oriented toward fatty acid biosynthesis pathways is promoted by starch-rich environment, whereas a lignocellulosic substrate fosters a midgut microbiota dominated by Paenibacillus spp. In contrast, the hindgut exhibits a distinctly stable and homogeneous bacterial composition dominated by Dysgonomonas spp. Overall, our results provide clear evidence of a two-compartment microbial system, in which the midgut primarily serves as a substrate-adaptive primary degradation chamber, while the hindgut functions as a stable terminal compartment for the final processing of residual substrates and the recycling of nutrients. These findings contribute to our understanding of the functional diversity of the bacterial microbiota along the BSFL digestive tract, which is a key factor in explaining this insect's remarkable polyphagous behavior and optimizing its use for industrial purposes.

microbiology↗

ArtSymbioCyc, a metabolic network database collection dedicated to arthropod symbioses: a case study, the tripartite cooperation in Sipha maydis

Most arthropods live in close association with bacteria. The genomes of associated partners have co-evolved creating situations of interdependence that are complex to decipher despite the availability of their complete sequences. We developed ArtSymbioCyc, a metabolism-oriented database collection gathering genomic resources for arthropods and their associated bacteria. ArtSymbioCyc uses the powerful tools of the BioCyc community to produce high quality annotations and to analyze and compare metabolic networks on a genome-wide scale. We used ArtSymbioCyc to study the case of the tripartite symbiosis of the cereal aphid Sipha maydis focusing on amino acid and vitamin metabolisms, as these compounds are known to be important in this strictly phloemophagous insect. We showed how the metabolic pathways of the insect host and its two obligate bacterial associates are interdependent and specialized in the exploitation of Poaceae phloem, for example for the biosynthesis of sulfur-containing amino acids and most vitamins. This demonstrates that ArtSymbioCyc does not only reveal the individual metabolic capacities of each partner and their respective contributions to the holobiont they constitute, but also allows to predict the essential inputs that must come from host nutrition. IMPORTANCEEvolution has driven the emergence of complex arthropod-microbe symbiotic systems, whose metabolic integration is difficult to unravel. With its user-friendly interface, ArtSymbioCyc (https://artsymbiocyc.cycadsys.org) eases and speeds up the analysis of metabolic networks by enabling precise inference of compound exchanges between associated partners, and helps unveil the adaptive potential of arthropods in contexts such as conservation or agricultural control.

bioinformatics↗

The di-symbiotic systems in the aphids Sipha maydis and Peryphillus lyropictus provide a contrasting picture of recent co-obligate nutritional endosymbiosis in aphids

Dependence on multiple nutritional bacterial symbionts forming a metabolic unit has repeatedly evolved in many insect species that feed on nutritionally unbalanced diets such as plant sap. This is the case for aphids of the subfamilies Lachninae and Chaitophorinae, which have evolved di-symbiotic systems in which the ancient obligate nutritional symbiont Buchnera aphidicola is metabolically complemented by an additional nutritional symbiont acquired more recently. Deciphering how different symbionts integrate both metabolically and anatomically in such systems is crucial to understanding how complex nutritional symbiotic systems function and evolve. In this study, we sequenced and analyzed the genomes of the symbionts B. aphidicola and Serratia symbiotica associated with the Chaitophorinae aphids Sipha maydis and Periphyllus lyropictus. Our results show that, in these two species, B. aphidicola and S. symbiotica complement each other metabolically (and their hosts) for the biosynthesis of essential amino acids and vitamins but with distinct metabolic reactions supported by each symbiont depending on the host species. Furthermore, the S. symbiotica symbiont associated with S. maydis appears to be strictly compartmentalized into the specialized host cells housing symbionts in aphids, the bacteriocytes, whereas the S. symbiotica symbiont associated with P. lyropictus exhibits a highly invasive phenotype, presumably because it is capable of expressing a larger set of virulence factors, including a complete flagellum for bacterial motility. Such contrasting levels of metabolic and anatomical integration for two S. symbiotica symbionts that were recently acquired as nutritional co-obligate partners reflect distinct coevolutionary processes specific to each association.

microbiology↗

Ubiquity of the Symbiont Serratia symbiotica in the Aphid Natural Environment: Distribution, Diversity and Evolution at a Multitrophic Level

Bacterial symbioses are significant drivers of insect evolutionary ecology. However, despite recent findings that these associations can emerge from environmentally derived bacterial precursors, there is still little information on how these potential progenitors of insect symbionts circulates in the trophic systems. The aphid symbiont Serratia symbiotica represents a valuable model for deciphering evolutionary scenarios of bacterial acquisition by insects, as its diversity includes intracellular host-dependent strains as well as gut-associated strains that have retained some ability to live independently of their hosts and circulate in plant phloem sap. These strains represent a potential reservoir for the emergence of new and more intimate symbioses. Here, we conducted a field study to examine the distribution and diversity of S. symbiotica found in aphid populations, as well as in different compartments of their surrounding environment. A total of 250 aphid colonies, 203 associated insects, and 161 plant samples associated with aphid colonies were screened for S. symbiotica. Twenty percent of aphids were infected with S. symbiotica, and the symbiont includes a wide diversity of strains with varied tissue tropism corresponding to different lifestyle. We also showed that the prevalence of S. symbiotica is influenced by seasonal temperatures. For the first time, we found that S. symbiotica was present in non aphid species and in host plants, and that the prevalence of the bacterium in these samples was higher when associated aphid colonies were infected. Furthermore, phylogenetic analyses suggest the existence of horizontal transfers between the different trophic levels examined. These results provide a completely new picture of the ubiquity of an insect symbiont in nature. They suggest that ecological interactions promote the dissemination of strains that are still free-living and poorly specialized, and for which plants are a proabable reservoir for the acquisition of new bacterial partners in insects.

evolutionary biology↗

New Insights into the Nature of Symbiotic Associations in Aphids: Initial Steps Involved in Aphid Gut Infection by Serratia symbiotica Bacteria

Symbiotic microorganisms are widespread in nature and can play a major role in the ecology and evolution of animals. The aphid-Serratia symbiotica bacterium interaction provides a valuable model to study mechanisms behind these symbiotic associations. The recent discovery of cultivable S. symbiotica strains having the possibility of free-living lifestyle allowed us to simulate their environmental acquisition by aphids to examine the mechanisms involved in this infection pathway. Here, after oral ingestion, we analyzed the infection dynamic of cultivable S. symbiotica strains during the hosts lifetime using qPCR and fluorescence techniques and determined the immediate fitness consequences of these bacteria on their new host. We further examined the transmission behavior and phylogenetic position of cultivable strains. Usually, S. symbiotica are considered as maternally-transmitted bacteria living within aphid body cavity and bringing some benefits to their hosts despite their costs. Otherwise, our study revealed that cultivable S. symbiotica are predisposed to establish a symbiotic association with new aphid host, settling in its gut. We showed that cultivable S. symbiotica colonized the entire aphid digestive tract following infection, after which the bacterium multiplied exponentially during aphid development. Our results further revealed that gut colonization by the bacteria induce a fitness cost to their hosts. Nevertheless, it appeared that they also offer an immediate protection against parasitoids. Interestingly, cultivable S. symbiotica seem to be extracellularly transmitted, possibly through the honeydew. These findings provide new insights into the nature of symbiosis in aphids and the mechanisms underpinning these interactions.\n\nImportanceFor the first time, our study provides experimental data that highlight a new kind of symbiotic associations in aphids. By successfully isolating microbial symbiont from aphids and by cultivating it in vitro in our laboratory, we established artificial association by simulating new bacterial acquisitions involved in aphid gut infection. Our results showed the early stages involved in this route of infection. Until now, Serratia symbiotica is considered as a maternally-transmitted aphid endosymbiont. Nevertheless, here, we showed that our cultivable strains having an intermediate status between a strict free-living bacterium and a facultative endosymbiont, occupy and replicate in aphid gut and seem to be transmitted over generations through an environmental transmission mechanism. Moreover, they are both parasites and mutualists given the context, as many of the endosymbionts in aphids. Our findings give new perception of associations involved in aphids symbiosis.

evolutionary biology↗