TY - JOUR
T1 - Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
AU - Łukasik, Piotr
AU - Nazario, Katherine
AU - Van Leuven, James T.
AU - Campbell, Matthew A.
AU - Meyer, Mariah
AU - Michalik, Anna
AU - Pessacq, Pablo
AU - Simon, Chris
AU - Veloso, Claudio
AU - McCutcheon, John P.
N1 - Funding Information:
for helpful discussions. We thank Mario Enrique Elgueta Donoso (El Museo Nacional de Historia Natural), Ana M. Marino de Remes Lenicov (El Museo de La Plata), and Allen Sanborn (Barry University) for access to cicada collections; and Ben Price and Mick Web (National History Museum, London) and Jerome Sueur and Thiery Burgoin (Museum National d’Histoire Naturelle, Paris) for photographs of additional Tettigades types and nontypes. This work was supported by National Science Foundation Grants IOS-1256680 and IOS-1553529, National Aeronautics and Space Administration Astrobiology Institute Award NNA15BB04A, and National Geographic Society Grant 9760-15. C.S. and K.N. acknowledge funding from the Ernst Mayr Travel Grant, the Museum of Comparative Zoology (Harvard University), and the University of Connecticut.
Funding Information:
We thank Filip Husn?k and Dan Vanderpool for valuable methodological advice; David Quammen for field work assistance; Ada Jankowska for technical assistance; and all members of the J.P.M. laboratory for helpful discussions. We thank Mario Enrique Elgueta Donoso (El Museo Nacional de Historia Natural), Ana M. Marino de Remes Lenicov (El Museo de La Plata), and Allen Sanborn (Barry University) for access to cicada collections; and Ben Price and Mick Web (National History Museum, London) and Jerome Sueur and Thiery Burgoin (Museum National d'Histoire Naturelle, Paris) for photographs of additional Tettigades types and nontypes. This work was supported by National Science Foundation Grants IOS-1256680 and IOS-1553529, National Aeronautics and Space Administration Astrobiology Institute Award NNA15BB04A, and National Geographic Society Grant 9760-15. C.S. and K.N. acknowledge funding from the Ernst Mayr Travel Grant, the Museum of Comparative Zoology (Harvard University), and the University of Connecticut.
PY - 2017/1/9
Y1 - 2017/1/9
N2 - Bacterial endosymbionts that provide nutrients to hosts often have genomes that are extremely stable in structure and gene content. In contrast, the genome of the endosymbiont Hodgkinia cicadicola has fractured into multiple distinct lineages in some species of the cicada genus Tettigades. To better understand the frequency, timing, and outcomes of Hodgkinia lineage splitting throughout this cicada genus, we sampled cicadas over three field seasons in Chile and performed genomics and microscopy on representative samples. We found that a single ancestral Hodgkinia lineage has split at least six independent times in Tettigades over the last 4 million years, resulting in complexes of between two and six distinct Hodgkinia lineages per host. Individual genomes in these symbiotic complexes differ dramatically in relative abundance, genome size, organization, and gene content. Each Hodgkinia lineage retains a small set of core genes involved in genetic information processing, but the high level of gene loss experienced by all genomes suggests that extensive sharing of gene products among symbiont cells must occur. In total, Hodgkinia complexes that consist of multiple lineages encode nearly complete sets of genes present on the ancestral single lineage and presumably perform the same functions as symbionts that have not undergone splitting. However, differences in the timing of the splits, along with dissimilar gene loss patterns on the resulting genomes, have led to very different outcomes of lineage splitting in extant cicadas.
AB - Bacterial endosymbionts that provide nutrients to hosts often have genomes that are extremely stable in structure and gene content. In contrast, the genome of the endosymbiont Hodgkinia cicadicola has fractured into multiple distinct lineages in some species of the cicada genus Tettigades. To better understand the frequency, timing, and outcomes of Hodgkinia lineage splitting throughout this cicada genus, we sampled cicadas over three field seasons in Chile and performed genomics and microscopy on representative samples. We found that a single ancestral Hodgkinia lineage has split at least six independent times in Tettigades over the last 4 million years, resulting in complexes of between two and six distinct Hodgkinia lineages per host. Individual genomes in these symbiotic complexes differ dramatically in relative abundance, genome size, organization, and gene content. Each Hodgkinia lineage retains a small set of core genes involved in genetic information processing, but the high level of gene loss experienced by all genomes suggests that extensive sharing of gene products among symbiont cells must occur. In total, Hodgkinia complexes that consist of multiple lineages encode nearly complete sets of genes present on the ancestral single lineage and presumably perform the same functions as symbionts that have not undergone splitting. However, differences in the timing of the splits, along with dissimilar gene loss patterns on the resulting genomes, have led to very different outcomes of lineage splitting in extant cicadas.
KW - Mitochondria
KW - Nutritional endosymbiont
KW - Organelle
KW - cicadas
KW - genome evolution
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U2 - 10.1073/pnas.1712321115
DO - 10.1073/pnas.1712321115
M3 - Article
C2 - 29279407
AN - SCOPUS:85040229893
SN - 0027-8424
VL - 115
SP - E226-E235
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 2
ER -