Transitional genomes and nutritional role reversals identified for dual symbionts of adelgids (Aphidoidea: Adelgidae)

Abstract

Many plant-sap-feeding insects have maintained a single, obligate, nutritional symbiont over the long history of their lineage. This senior symbiont may be joined by one or more junior symbionts that compensate for gaps in function incurred through genome-degradative forces. Adelgids are sap-sucking insects that feed solely on conifer trees and follow complex life cycles in which the diet fluctuates in nutrient levels. Adelgids are unusual in that both senior and junior symbionts appear to have been replaced repeatedly over their evolutionary history. Genomes can provide clues to understanding symbiont replacements, but only the dual symbionts of hemlock adelgids have been examined thus far. Here, we sequence and compare genomes of four additional dual-symbiont pairs in adelgids. We show that these symbionts are nutritional partners originating from diverse bacterial lineages and exhibiting wide variation in general genome characteristics. Although dual symbionts cooperate to produce nutrients, the balance of contributions varies widely across pairs, and total genome contents reflect a range of ages and degrees of degradation. Most symbionts appear to be in transitional states of genome reduction. Our findings support a hypothesis of periodic symbiont turnover driven by fluctuating selection for nutritional provisioning related to gains and losses of complex life cycles in their hosts.

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

“…Biotin was the second most common nutrient predicted to be supplied by the secondary co-obligate endosymbionts: it was found in all cases except in the co-obligate association observed in Pa. juglandis . A similar vitamin-biosynthetic role for the new co-obligate endosymbionts can be found in some psyllids (Sloan and Moran, 2012) as well as some adelgids (Dial et al ., 2022; Szabó et al ., 2022). In contrast, in other adelgids, retention of the B vitamin biosynthetic genes can also be observed in the primary symbionts, and not in the newly evolved symbiotic partners.…”

“…(Drepanosiphinae) (Fukatsu, 2001; Fukatsu and Ishikawa, 1993), Sipha maydis (Chaitophorinae: Siphini), Anoecia corni (Anoeciinae), and Glyphina betulae (Thelaxinae) (Kot, 2012; Michalik, 2010; Michalik et al ., 2014). In most above-mentioned cases, the co-obligate symbionts are not only inhabiting their own bacteriocytes, but also show a spherical cell shape, which is characteristic of many obligate symbionts of aphids and other insects with drastically reduced genomes (Dial et al ., 2022; Lamelas et al ., 2008, 2011b; Manzano-Marín et al ., 2016, 2017, 2020; Michalik et al ., 2021; Szabó et al ., 2022; Toenshoff et al ., 2012, 2014).…”

“…While ancient symbiont replacement and complementation has been well documented in hemipteran taxa such as the Auchenorrhyncha ( e.g . cicadas, treehoppers, leafhoppers, and planthoppers; Koga and Moran, 2014; Łukasik et al ., 2018; Matsuura et al ., 2018; McCutcheon and Moran, 2007; Michalik et al ., 2021), Pseudococcinae (mealybugs; Husnik and McCutcheon, 2016; Szabó et al ., 2017), Adelgidae (adelgids; Dial et al ., 2022; Szabó et al ., 2022; Toenshoff et al ., 2012; Weglarz et al ., 2018), and Psylloidea (psyllids; Nakabachi et al ., 2013, 2020; Sloan and Moran, 2012), these associations have not been widely reported across aphids. The mutualism between aphids and Buchnera has generally been seen as stable and quite exclusive.…”

A highly divergent Wolbachia with a tiny genome in an insect-parasitic tylenchid nematode

“…Another possibility is that Wolbachia was perhaps acquired by Howardula nematodes relatively recently, from an as yet unknown lineage of hosts where it has been a symbiont for a long time. For example, some species of adelgids, insects that feed on conifer sap, have recently acquired obligate nutritional symbionts that are closely related to obligate bacterial symbionts of fungi [ 50 , 51 ]. It is interesting that the clade of fly parasitic Howardula nematodes and allies appears to contain mixtures of species that are free of symbionts, along with ones that have recently acquired putatively obligate symbionts.…”

Genomic Comparisons Reveal Selection Pressure and Functional Variation Between Nutritional Endosymbionts of Cave-Adapted and Epigean Hawaiian Planthoppers

“…However, essential genes are still often lost from these tiny genomes even among closely related host species likely resulting from strong genetic drift ( Chong et al 2019 ; Vasquez and Bennett 2022 ). Gene functions that are lost can be compensated for by several processes such as horizontal gene transfer of host-encoded homologs ( Hansen and Moran 2014 ; Sloan et al 2014 ), the acquisition of new co-endosymbionts ( McCutcheon et al 2009 ; Sheffer et al 2020 ; Dial et al 2021 ), or senior symbiont replacement by junior endosymbionts ( Clayton et al 2012 ; Toenshoff et al 2012 ; Koga and Moran 2014 ; Sudakaran et al 2017 ; Chong and Moran 2018 ; Mao and Bennett 2020 ).…”