TY - JOUR
T1 - Idiosyncratic Genome Degradation in a Bacterial Endosymbiont of Periodical Cicadas
AU - Campbell, Matthew A.
AU - Łukasik, Piotr
AU - Simon, Chris
AU - McCutcheon, John P.
N1 - Funding Information:
We thank all members of the McCutcheon lab for helpful discussion and comments and Scott Miller for suggesting the use of the Jaccard index. Funding for the sequencing and analysis was supported by National Science Foundation (NSF) grants IOS-1256680 and IOS-1553529 and National Aeronautics and Space Administration Astrobiology Institute award NNA15BB04A . Funding for cicada collecting was provided by NSF DEB-09-55849 .
Publisher Copyright:
© 2017 Elsevier Ltd
PY - 2017/11/20
Y1 - 2017/11/20
N2 - 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 stable in size, structure, and coding capacity [3–5], as exemplified by Sulcia muelleri, a nutritional endosymbiont of cicadas. Sulcia's partner endosymbiont, Hodgkinia cicadicola, similarly remains co-linear in some cicadas diverged by 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 circles that sometimes reside in distinct Hodgkinia cells [8]. Previous data suggested that all other Magicicada species harbor 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 and two sister species, we show that each Magicicada species harbors Hodgkinia populations of at least 20 genomic circles. We find little synteny among the 256 Hodgkinia circles analyzed except between the most closely related cicada species. Gene phylogenies show multiple Hodgkinia lineages 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 among 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 nonadaptive for the host. These patterns mirror the genomic instability seen in some mitochondria. The stability of nutritional endosymbiont genomes reflects their importance to their hosts. Campbell et al. show that this stability has dramatically eroded in an endosymbiont of the 13- and 17-year periodical cicadas and that the outcome of this instability is wildly different in different cicadas.
AB - 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 stable in size, structure, and coding capacity [3–5], as exemplified by Sulcia muelleri, a nutritional endosymbiont of cicadas. Sulcia's partner endosymbiont, Hodgkinia cicadicola, similarly remains co-linear in some cicadas diverged by 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 circles that sometimes reside in distinct Hodgkinia cells [8]. Previous data suggested that all other Magicicada species harbor 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 and two sister species, we show that each Magicicada species harbors Hodgkinia populations of at least 20 genomic circles. We find little synteny among the 256 Hodgkinia circles analyzed except between the most closely related cicada species. Gene phylogenies show multiple Hodgkinia lineages 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 among 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 nonadaptive for the host. These patterns mirror the genomic instability seen in some mitochondria. The stability of nutritional endosymbiont genomes reflects their importance to their hosts. Campbell et al. show that this stability has dramatically eroded in an endosymbiont of the 13- and 17-year periodical cicadas and that the outcome of this instability is wildly different in different cicadas.
KW - Hodgkinia cicadicola
KW - Magicicada
KW - endosymbiosis
KW - levels of selection
KW - mutation
KW - nonadaptive evolution
KW - organelle genomes
KW - periodical cicadas
UR - http://www.scopus.com/inward/record.url?scp=85033390947&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85033390947&partnerID=8YFLogxK
U2 - 10.1016/j.cub.2017.10.008
DO - 10.1016/j.cub.2017.10.008
M3 - Article
C2 - 29129532
AN - SCOPUS:85033390947
SN - 0960-9822
VL - 27
SP - 3568-3575.e3
JO - Current Biology
JF - Current Biology
IS - 22
ER -