Insect-host control of obligate, intracellular symbiont density

Abstract

Many insects rely on intracellular bacterial symbionts to supplement their specialized diets with micronutrients. Using data from diverse and well-studied insect systems, we propose three lines of evidence suggesting that hosts have tight control over the density of their obligate, intracellular bacterial partners. First, empirical studies have demonstrated that the within-host symbiont density varies depending on the nutritional and developmental requirements of the host. Second, symbiont genomes are highly reduced and have limited capacity for self-replication or transcriptional regulation. Third, several mechanisms exist for hosts to tolerate, regulate and remove symbionts including physical compartmentalization and autophagy. We then consider whether such regulation is adaptive, by discussing the relationship between symbiont density and host fitness. We discuss current limitations of empirical studies for exploring fitness effects in host–symbiont relationships, and emphasize the potential for using mathematical models to formalize evolutionary hypotheses and to generate testable predictions for future work.

For the road: calibrated maternal investment in light of extracellular symbiont transmission

“…As demonstrated in aphids, differences in symbiont density early in insect development are correlated with fitness consequences that extend beyond the survivorship of immature stages, including growth rate and lifetime reproductive output [ 43 ]. Quantifying a broader set of fitness parameters in C. alternans relative to variation in Stammera titres will complement these efforts [ 43 , 44 ], yielding important insights into symbiont density dependence in obligate partnerships.…”

The Di-Symbiotic Systems in the Aphids Sipha maydis and Periphyllus lyropictus Provide a Contrasting Picture of Recent Co-Obligate Nutritional Endosymbiosis in Aphids

“…Compartmentalization within bacteriocytes is a typical feature of obligate nutritional symbionts [ 67 , 68 ] and a key adaptation that underpins the partnership between insects and these bacteria. Indeed, these specialized host cells mediate metabolic exchanges between the host and symbiotic bacteria and allow the host to control populations of its symbionts according to its nutritional needs [ 2 , 4 , 69 ]. The S. symbiotica co-obligate symbiont associated with P. lyropictus exhibits invasive traits and escape strict compartmentalization into bacteriocytes despite its integration into a cooperative lifestyle with its host and the ancestral symbiont B. aphidicola [ 30 ].…”

“…Bacteriocytes are the interface for metabolic exchanges between the host and the symbionts. They allow the host to control symbiont populations according to its nutritional needs and ensure stable vertical transmission of symbionts from mother to offspring [ 2 , 3 ]. This compartmentalization into bacteriocytes is considered as the outcome of a long coevolutionary history between the insect hosts and their obligate bacterial partners [ 4 ].…”

Compartmentalized into Bacteriocytes but Highly Invasive: the Puzzling Case of the Co-Obligate Symbiont Serratia symbiotica in the Aphid Periphyllus lyropictus

“…Compartmentalization of symbiotic bacteria into specialized host cells or organs is a key step in establishing interdependent nutritional cooperation in insect-microbial symbioses, in which confinement in bacteriocytes ensures the control of symbiont populations by the host and the coordination of metabolic exchanges according to its development ( 29 , 30 ). At the same time, adopting such an intimate lifestyle with the host promotes strong selection for avirulence, resulting in the loss of genes associated with infectivity and thus a decrease in the ability of these bacteria to colonize a wider range of niches ( 20 , 31 ).…”