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

Abstract

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.

Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages

“…The description of the dual symbiotic system of Si. maydis has been very recently independently reported by Renoz et al (2022b), which resulted from parallel sequencing efforts and showing similar findings to ours for this system. Erwinia was also found in all samples from a specific clade of Cinara (Lachninae: Eulachnini), validating its co-obligate status (Manzano-Marín et al, 2020).…”

“…symbiotica endosymbiont in Si. maydis (Renoz et al ., 2022b) and another one showing the evolution of a co-obligate symbiotic system in Ceratovacuna japonica (Hormaphidinae: Cerataphidini; Yorimoto et al ., 2022). A few major aphid lineages are still missing from this reconstruction, most markedly members of two well-diversified subfamily Greenideinae and Hormaphidinae where more dual symbiotic systems might be revealed.…”

“…Such co-obligate symbioses have indeed arose in at least two aphid groups: the Lachninae (Manzano-Marín et al ., 2017) and the Periphyllus genus (Chaitophorinae: Chaitophorini; Monnin et al ., 2020; Renoz et al ., 2022a). Very recently, an additional two reports of co-obligate symbioses have been published in two species from two different tribes: Sipha maydis (Chaitophorinae: Siphini; Renoz et al ., 2022b), which has been idenpendently analysed in the current work, and Ceratovacuna japonica (Hormaphidinae: Cerataphidini; Yorimoto et al ., 2022). These secondary co-obligate symbionts now complement evolved auxotrophies of their corresponding Buchnera partners, most commonly those for biotin and riboflavin and less often those for tryptophan and histidine.…”

Subcellular niche segregation of co-obligate symbionts in whiteflies

“…In multiple endosymbiotic systems comprising two or more symbionts, each of the symbionts is generally localized in a different host cell or tissue. This type of localization is observed in various insect species, such as aphids, spittlebugs, leafhoppers, scale insects, adelgids, psyllids, and cicadas (1,(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13) (Supporting data only for review in Supplemental Information). The compartmentalization of multiple symbionts into different host cells is considered as an important step in evolution, to reduce direct conflict between the multiple symbionts and control them within the same host (12,14).…”

“…In some co-obligate symbiotic systems in insects, each symbiont can complete the biosynthetic pathway of some essential nutrients, such as essential amino acids or vitamins, on its own or with host genes (13,(54)(55)(56)(57)(58). In other co-symbiotic systems, metabolic interdependence for some essential nutrients is present, wherein one of the symbionts possesses genes necessary for the first part of the biosynthetic pathway, and the other symbiont has genes necessary for the latter part of the pathway (10,12,13,(59)(60). In such a system, metabolic intermediates must diffuse or be translocated from one symbiont to another to produce essential nutrients in adjacent host cells.…”