Idiosyncratic genome degradation in a bacterial endosymbiont of periodical cicadas

Abstract

When a free-living bacterium transitions to a host-beneficial endosymbiotic lifestyle, it almost invariably loses a large fraction of its genome [1,2]. The resulting small genomes often become unusually stable in size, structure, and coding capacity [3][4][5]. Candidatus Hodgkinia cicadicola (Hodgkinia), a bacterial endosymbiont of cicadas, sometimes exemplifies this genomic stability. The Hodgkinia genome has remained completely co-linear in some cicadas diverged by tens of millions of years [6,7]. But in the long-lived periodical cicada Magicicada tredecim, the Hodgkinia genome has split into dozens of tiny, gene-sparse genomic circles that sometimes reside in distinct Hodgkinia cells [8]. Previous data suggested that other Magicicada species harbor similarly complex Hodgkinia populations, but the timing, number of origins, and outcomes of the splitting process were unknown. Here, by sequencing Hodgkinia metagenomes from the remaining six Magicicada species and two sister species, we show that all Magicicada species harbor Hodgkinia populations of at least twenty genomic circles each. We find little synteny among the 256 Hodgkinia circles analyzed except between the most closely related species. Individual gene phylogenies show that Hodgkinia first split in the common ancestor of Magicicada and its closest known relatives, but that most splitting has occurred within Magicicada and has given rise to highly variable Hodgkinia gene dosages between cicada species. These data show that Hodgkinia genome degradation has proceeded down different paths in different Magicicada species, and support a model of genomic degradation that is stochastic in outcome and likely nonadaptive for the host. These patterns mirror the genomic instability seen in some mitochondria.

Comparative genomics of a quadripartite symbiosis in a planthopper host reveals the origins and rearranged nutritional responsibilities of anciently diverged bacterial lineages

“…Nevertheless, it is possible that the jigsaw of nutritional contributions was largely shaped by genetic drift as the random corruption and loss of some nutritional pathways in a particular symbiont forced complementation in another. Several recent studies have highlighted the underlying role of drift in driving lineage specific gene losses and in shaping the co-evolution of host-symbiont interactions (Boscaro et al, 2017;Campbell et al, 2017;Sabater-Muñoz et al, 2017). Thus, as the genomes of the early bacterial symbionts in Auchenorrhyncha began to unravel, stochastic gene losses and partner complementation may have caused the bacterial symbionts to spiral down their own pathways.…”

No genome is an island: toward a 21st century agenda for evolution

“…For many endosymbionts, a process similar to mitochondrial and plastid genome reduction occurs. The initially free‐living bacterium loses most of its genome and transitions to “a host‐beneficial endosymbiotic lifestyle.” The reduced endosymbiont genomes typically stabilize in size, structure, and coding capacity. In some cases, descendants of a single obligate endosymbiotic bacterium can diverge into complementary intracellular constituents by losing different parts of the initial endosymbiont genome …”

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.…”

“…The number of Hodgkinia lineages varies in different cicada species. For example, a species in the cicada genus Diceroprocta has one Hodgkinia lineage (21), various species in the genus Tettigades have between one and six Hodgkinia lineages (17,20), and the seven species in the long-lived periodical genus Magicicada contain more, possibly dozens, of Hodgkinia lineages (18,19).…”