Genome expansion via lineage splitting and genome reduction in the cicada endosymbiont Hodgkinia

Matthew A. Campbell, James T. Van Leuven, Russell C. Meister, Kaitlin M. Carey, Chris Simon, John P. McCutcheon

Research output: Contribution to journalArticlepeer-review

45 Scopus citations

Abstract

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.

Original languageEnglish (US)
Pages (from-to)10192-10199
Number of pages8
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number33
DOIs
StatePublished - Aug 18 2015
Externally publishedYes

Keywords

  • Bacteria
  • Genome evolution
  • Nonadaptive evolution
  • Organelles
  • Symbiosis

ASJC Scopus subject areas

  • General

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