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.
Highlights
Interaction, the availability of full genome sequences for both partners allowed considerable advances to be made in the understanding of the molecular basis of symbiotic interactions[7,8,9]
To develop this novel approach, we took into account the specificity of aphid symbiosis, in which symbiotic bacteria are localized in specific insect cells, the bacteriocytes, which need to be isolated from other aphid tissues
We have developed a novel approach based on flow cytometry to quantify the dynamics of absolute cell numbers of B. aphidicola, the obligate endosymbiont of A. pisum, during the entire insect host life cycle
Summary
Interaction, the availability of full genome sequences for both partners allowed considerable advances to be made in the understanding of the molecular basis of symbiotic interactions[7,8,9]. Aphids exhibit the particularity of reproducing asexually by viviparous parthenogenesis for much of their life cycle, leading to the development of embryos within maternal ovarioles. Considerable progress has been made in describing the maternal transmission of symbiotic bacteria in aphids, the relative dynamics between endosymbionts and bacteriocytes after the embryo/oocyte infection, and over the entire insect life cycle, remain largely unexplored. A few studies have analyzed the endosymbiont number and the bacteriocyte cell dynamics using microscopy techniques[24,25,26] These histological data are fragmented, not providing an overview of the complete aphid life cycle. In spite of its wide use in environmental applications, the flow cytometry technique has never been used to quantify the absolute number of unculturable symbiotic bacteria in insect models
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