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Direct flow cytometry measurements reveal a fine-tuning of symbiotic cell dynamics according to the host developmental needs in aphid symbiosis

Abstract : Endosymbiotic associations constitute a driving force in the ecological and evolutionary diversification of metazoan organisms. Little is known about whether and how symbiotic cells are coordinated according to host physiology. Here, we use the nutritional symbiosis between the insect pest, Acyrthosiphon pisum, and its obligate symbiont, Buchnera aphidicola, as a model system. We have developed a novel approach for unculturable bacteria, based on flow cytometry, and used this method to estimate the absolute numbers of symbionts at key stages of aphid life. The endosymbiont population increases exponentially throughout nymphal development, showing a growing rate which has never been characterized by indirect molecular techniques. Using histology and imaging techniques, we have shown that the endosymbiont-bearing cells (bacteriocytes) increase significantly in number and size during the nymphal development, and clustering in the insect abdomen. Once adulthood is reached and the laying period has begun, the dynamics of symbiont and host cells is reversed: the number of endosymbionts decreases progressively and the bacteriocyte structure degenerates during insect aging. In summary, these results show a coordination of the cellular dynamics between bacteriocytes and primary symbionts and reveal a fine-tuning of aphid symbiotic cells to the nutritional demand imposed by the host physiology throughout development. Intracellular symbioses (endosymbioses) between prokaryotic and metazoan organisms play a central role in multicellular life, significantly impacting the evolution and shaping the ecology of countless species 1. In insects, which account for a great proportion of planet biodiversity, the exploitation of the metabolic capabilities of intra-cellular symbiotic bacteria (endosymbionts) enables the hosts to thrive on nutritionally unbalanced diets such as plant sap, grains, wood or vertebrate blood 2–4. The sustainability of these endosymbiotic relationships largely relies on the compartmentalization of bacterial endosymbionts into specialized host cells (or organs), called bac-teriocytes (or bacteriomes), whose functions are adapted to the tolerance and regulation of symbiotic populations 5,6. A detailed description of the interplay between bacteriocytes and endosymbionts across the host life cycle, and in response to an ever-changing environment, is expected to provide a better understanding of how microorganisms interact with eukaryotic cells, and, in turn, to contribute to the development of novel strategies for controlling pest and disease-vector insects. The relationship between aphids (Hemiptera: Aphididae) and the gamma-3-proteobacterium Buchnera aphidicola, represents the best-studied model among endosymbiotic associations. In the A. pisum/B. aphidicola
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Pierre Simonet, Gabrielle Duport, Karen Gaget, Michèle Weiss-Gayet, Stefano Colella, et al.. Direct flow cytometry measurements reveal a fine-tuning of symbiotic cell dynamics according to the host developmental needs in aphid symbiosis. Scientific Reports, 2016, 6, pp.19967. ⟨10.1038/srep19967⟩. ⟨hal-01352561⟩



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