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Mélanie Ribeiro Lopes & Federica Calevro (UMR BF2I) will present their work on " The bacteriocyte: a biological innovation to sustain and control bacterial symbionts in insect nutritional symbioses”, on Thursday 17th of November 2022, at 1pm, Room 3203, Université Claude Bernard Lyon 1, 50 Av Tony Garnier, 69007 Lyon. 

In insects that are obligatorily dependent on intracellular bacterial symbionts, novel host cells, the bacteriocytes, have evolved to harbour beneficial microbial partners. These cells have been described in at least six insect orders (i.e. Coleoptera, Diptera, Dictyoptera, Hemiptera, Hymenoptera and Phthiraptera) in which they are thought to have evolved independently. This multiple origin of bacteriocytes results in a great diversity of shapes, organizations and locations in the insect body, despite a common role in the control and protection of symbionts. If bacteriocytes are at the heart of symbiotic interactions in insects, they remain a fascinating enigma in developmental and evolutionary cell biology, with many questions still unanswered. In particular, the molecular mechanisms underlying their development and governing their dynamics in response to host physiology remain largely unresolved.

Aphids are ideal model systems to study bacteriocytes. Aphid bacteriocytes have large size, are easy to individualize and to isolate by manual dissection. Moreover, the availability of numerous aphid and symbiotic partner genomes allows the combination of cellular and molecular approaches to study the dynamics of bacteriocytes throughout the insect's life in different evolutionary contexts. Using the pea aphid/Buchnera aphidicola symbiotic system, we recently demonstrated that bacteriocytes are highly dynamic cells, adjusting their growth and death, as well as their symbiont load, to the variation of the aphid demand throughout its development (Simonet et al., Sci. Rep. 2016, doi: 10.1038/srep19967) or in response to its diet (Colella et al., Front. Physiol. 2018, doi: 10.3389/fphys.2018.01498; Ribeiro Lopes et al., Front. Physiol. In press). These studies led to the discovery, in the pea aphid, of a novel form of non-apoptotic cell death, that shares features with ancestral processes such as paraptosis and is involved in the elimination of senescent bacteriocytes (Simonet et al., PNAS 2018, doi: 10.1073/pnas.1720237115). To address the molecular mechanisms governing bacteriocyte cell death, we annotated and studied the expression patterns of the apoptosis pathway genes in this insect. We found that, while the caspase repertoire is incomplete, with homologs for only four out of the eight proteins present in Drosophila melanogaster, apoptosis inhibitors underwent a large gene expansion, with 28 Inhibitor-of-Apoptosis (IAP) proteins (contrary to the 4 to 7 IAPs present in other insects). Tissue-specific qRT-PCR and RNAseq analyses have shown that five of those IAPs are expressed specifically in aphid bacteriocytes and that their expression is induced in bacteriocyte cell death. We have confirmed the anti-apoptotic role of these bacteriocyte-associated IAPs in heterologous expression experiments using a tractable in vivo model, the D. melanogaster developing eye, demonstrating that three of them (Ap-IAP1, 2 and 4) are super-IAPs, containing duplications of the classic IAP domains (Ribeiro Lopes et al., PNAS 2020, doi: 10.1073/pnas.2013847117). The induction of a restricted set of strong anti-apoptotic IAPs provides a possible mechanism whereby apoptosis is prevented in senescent bacteriocytes, enabling the emergence of a novel cell death process and the maintenance of symbionts throughout the entire aphid life cycle.

We are now taking advantage of the fact that aphids can host one or more secondary symbionts in addition to the obligatory symbiont B. aphidicola, to study how bacteriocyte dynamics and cell death are impacted by different symbiotic suites. While B. aphidicola is always restricted to so-called primary bacteriocytes, secondary symbionts have a variable tropism. For instance, the secondary symbiont Serratia symbiotica can be found in the hemolymph and/or secondary bacteriocytes depending on the aphid species (Renoz et al., Microbiol. Spectr. 2022, doi: 10.1128/spectrum.00457-22). This provides a unique opportunity to study how bacteriocyte compartmentalization has evolved and how the fate of bacteriocytes is affected by symbionts with distinct genomic potential and immunogenic capabilities.

 Host: Fabienne Archer (iWAYS-IVPC)