Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas

Abstract

Bacterial endosymbionts that provide nutrients to hosts often have genomes that are extremely stable in structure and gene content. In contrast, the genome of the endosymbiont has fractured into multiple distinct lineages in some species of the cicada genus To better understand the frequency, timing, and outcomes of lineage splitting throughout this cicada genus, we sampled cicadas over three field seasons in Chile and performed genomics and microscopy on representative samples. We found that a single ancestral lineage has split at least six independent times in over the last 4 million years, resulting in complexes of between two and six distinct lineages per host. Individual genomes in these symbiotic complexes differ dramatically in relative abundance, genome size, organization, and gene content. Each lineage retains a small set of core genes involved in genetic information processing, but the high level of gene loss experienced by all genomes suggests that extensive sharing of gene products among symbiont cells must occur. In total, complexes that consist of multiple lineages encode nearly complete sets of genes present on the ancestral single lineage and presumably perform the same functions as symbionts that have not undergone splitting. However, differences in the timing of the splits, along with dissimilar gene loss patterns on the resulting genomes, have led to very different outcomes of lineage splitting in extant cicadas.

Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

“…Indeed, ancestral Coxiella ‐LE may have evolved overly reduced (degraded) genomes and become maladapted, opening the road to replacement by a new symbiont. This degeneration–replacement model has been proposed for other arthropods such as cicadas (Campbell et al, ; Łukasik et al, ; Matsuura et al, ), but replacements are expected to be transient making them difficult to observe (McCutcheon et al, ). In Amblyomma , the observations of three species with co‐infections by ancestral Coxiella ‐LE and recently acquired Francisella ‐LE may correspond to this transient state before extinction of Coxiella ‐LE.…”

“…This degeneration-replacement model has been proposed for other arthropods such as cicadas (Campbell et al, 2015;Łukasik et al, 2018;Matsuura et al, 2018) That ecological specialization to strict haematophagy is driven by nutritional symbiotic interactions is beyond doubt for ticks.…”

Cicada endosymbionts contain tRNAs that are processed despite having genomes that lack tRNA processing activities

“…Although RNase Y is typically thought to initiate mRNA decay, it is also implicated in multiple RNA processing tasks (59). No such putative enzyme can be found in the D. semicinta Hodgkinia genome, although a gene for the endoribonuclease YbeY is present in Hodgkinia genomes from other cicada species (14). After 3' tRNA trailers are trimmed, a terminal CCA is added by a CCA-adding enzyme (30).…”

“…Sulcia muelleri" (Bacteroidetes; hereafter Hodgkinia and Sulcia) have two of the smallest bacterial genomes published. Sulcia and Hodgkinia are obligate nutritional endosymbionts of many cicadas (13,14). In the cicada Diceroprocta semicincta, the Hodgkinia genome is 143 kilobases (kb) and the Sulcia genome is 277 kb.…”

Changes in endosymbiont complexity drive host-level compensatory adaptations in cicadas

“…In many of the cicada species characterized to date (but see (13)), these nutritional services are provided by two transovarially transmitted bacterial endosymbionts, Candidatus Sulcia muelleri (hereafter referred to as Sulcia) and Candidatus Hodgkinia cicadicola (hereafter Hodgkinia) (14)(15)(16). We have previously shown that in two cicada genera, Tettigades and Magicicada, Hodgkinia has undergone an unusual form of lineage splitting (17)(18)(19)(20). In some of these cicada species, a single Hodgkinia lineage has split into two or more derived lineages, each containing only a subset of the genes present in the single ancestral lineage.…”