Genome expansion via lineage splitting and genome reduction in the cicada endosymbiont Hodgkinia.
Comparative genomics from mitochondria, plastids, and mutualistic endosymbiotic bacteria has shown that the stable establishment of a bacterium in a host cell results in genome reduction. Although many highly reduced genomes from endosymbiotic bacteria are stable in gene content and genome structure, organelle genomes are sometimes characterized by dramatic structural diversity. Previous results from Candidatus Hodgkinia cicadicola, an endosymbiont of cicadas, revealed that some lineages of this bacterium had split into two new cytologically distinct yet genetically interdependent species. It was hypothesized that the long life cycle of cicadas in part enabled this unusual lineage-splitting event. Here we test this hypothesis by investigating the structure of the Ca. Hodgkinia genome in one of the longest-lived cicadas, Magicicada tredecim. We show that the Ca. Hodgkinia genome from M. tredecim has fragmented into multiple new chromosomes or genomes, with at least some remaining partitioned into discrete cells. We also show that this lineage-splitting process has resulted in a complex of Ca. Hodgkinia genomes that are 1.1-Mb pairs in length when considered together, an almost 10-fold increase in size from the hypothetical single-genome ancestor. These results parallel some examples of genome fragmentation and expansion in organelles, although the mechanisms that give rise to these extreme genome instabilities are likely different.
Division of Biological Sciences, University of Montana, Missoula, MT 59812;
Matthew A
MA
Campbell
Division of Biological Sciences, University of Montana, Missoula, MT 59812;
James T
JT
Van Leuven
Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269;
Russell C
RC
Meister
Division of Biological Sciences, University of Montana, Missoula, MT 59812;
Kaitlin M
KM
Carey
Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269;
Chris
C
Simon
Division of Biological Sciences, University of Montana, Missoula, MT 59812; Program in Integrated Microbial Biodiversity, Canadian Institute for Advanced Research, Toronto, ON, Canada M5G 1Z8 john.mccutcheon@umontana.edu.
John P
JP
McCutcheon
D020561:Alphaproteobacteria / Q000235:genetics*; D000818:Animals; D019143:Evolution, Molecular; D005260:Female; D016680:Genome, Bacterial; D054629:Genome, Mitochondrial; D023281:Genomics; D006430:Hemiptera / Q000382:microbiology*; D017404:In Situ Hybridization, Fluorescence; D008969:Molecular Sequence Data; D016366:Open Reading Frames; D015388:Organelles; D010802:Phylogeny; D018087:Plastids / Q000235:genetics; D012270:Ribosomes / Q000378:metabolism; D013045:Species Specificity; D013559:Symbiosis
bacteria; genome evolution; nonadaptive evolution; organelles; symbiosis