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Idiosyncratic genome degradation in a bacterial endosymbiont of periodical cicadas

Matthew A. Campbell, Piotr Łukasik, Chris Simon, View ORCID ProfileJohn P. McCutcheon
doi: https://doi.org/10.1101/199760
Matthew A. Campbell
aDivision of Biological Sciences, University of Montana, Missoula, MT, USA
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Piotr Łukasik
aDivision of Biological Sciences, University of Montana, Missoula, MT, USA
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Chris Simon
bDepartment of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA
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John P. McCutcheon
aDivision of Biological Sciences, University of Montana, Missoula, MT, USA
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  • ORCID record for John P. McCutcheon
  • For correspondence: john.mccutcheon@umontana.edu
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Summary

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 [3-5]. 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.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted October 07, 2017.
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Idiosyncratic genome degradation in a bacterial endosymbiont of periodical cicadas
Matthew A. Campbell, Piotr Łukasik, Chris Simon, John P. McCutcheon
bioRxiv 199760; doi: https://doi.org/10.1101/199760
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Idiosyncratic genome degradation in a bacterial endosymbiont of periodical cicadas
Matthew A. Campbell, Piotr Łukasik, Chris Simon, John P. McCutcheon
bioRxiv 199760; doi: https://doi.org/10.1101/199760

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