TY - JOUR
T1 - Recurrent symbiont recruitment from fungal parasites in cicadas
AU - Matsuura, Yu
AU - Moriyama, Minoru
AU - Łukasik, Piotr
AU - Vanderpool, Dan
AU - Tanahashi, Masahiko
AU - Meng, Xian Ying
AU - McCutcheon, John P.
AU - Fukatsu, Takema
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank Junko Makino, Koki Murano, Kohei Oguchi, Keisuke Shimada, Masami Hayashi, Masaaki Kimura, Nahomi Kaiwa, Takahiro Hosokawa, Takashi Kanbe, and Yoshiko Ishii for cicada samples; Masami Hayashi and Mamoru Yasuda for cicada and fungal photographs; Chiaki Matsuura for cicada illustrations; and Yoshitomo Kikuchi for logistic support. This study was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI Grants JP26840116 (to Y.M.) and JP25221107 and JP17H06388 (to T.F.); by a general research grant of the Institute of Fermentation, Osaka; by National Science Foundation Grants IOS-1256680, IOS-1553529, DGE-1313190, IAA-1443108, and EPS-1101342; and by NASA Astrobiology Institute Award NNA15BB04A. Y.M., M.M., and M.T. were supported by a JSPS Fellowship for Young Scientists.
Funding Information:
We thank Junko Makino, Koki Murano, Kohei Oguchi, Keisuke Shimada, Masami Hayashi, Masaaki Kimura, Nahomi Kaiwa, Takahiro Hosokawa, Takashi Kanbe, and Yoshiko Ishii for cicada samples; Masami Hayashi and Mamoru Yasuda for cicada and fungal photographs; Chiaki Matsuura for cicada illustrations; and Yoshitomo Kikuchi for logistic support. This study was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI Grants JP26840116 (to Y.M.) and JP25221107 and JP17H06388 (to T.F.); by a general research grant of the Institute of Fermentation, Osaka; by National Science Foundation Grants IOS-1256680, IOS-1553529, DGE-1313190, IAA-1443108, and EPS-1101342; and by NASA Astro-biology Institute Award NNA15BB04A. Y.M., M.M., and M.T. were supported by a JSPS Fellowship for Young Scientists.
Publisher Copyright:
© 2018 National Academy of Sciences. All Rights Reserved.
PY - 2018/6/26
Y1 - 2018/6/26
N2 - Diverse insects are associated with ancient bacterial symbionts, whose genomes have often suffered drastic reduction and degeneration. In extreme cases, such symbiont genomes seem almost unable to sustain the basic cellular functioning, which comprises an open question in the evolution of symbiosis. Here, we report an insect group wherein an ancient symbiont lineage suffering massive genome erosion has experienced recurrent extinction and replacement by host-associated pathogenic microbes. Cicadas are associated with the ancient bacterial co-obligate symbionts Sulcia and Hodgkinia, whose streamlined genomes are specialized for synthesizing essential amino acids, thereby enabling the host to live on plant sap. However, our inspection of 24 Japanese cicada species revealed that while all species possessed Sulcia, only nine species retained Hodgkinia, and their genomes exhibited substantial structural instability. The remaining 15 species lacked Hodgkinia and instead harbored yeastlike fungal symbionts. Detailed phylogenetic analyses uncovered repeated Hodgkinia-fungus and fungus-fungus replacements in cicadas. The fungal symbionts were phylogenetically intermingled with cicada-parasitizing Ophiocordyceps fungi, identifying entomopathogenic origins of the fungal symbionts. Most fungal symbionts of cicadas were uncultivable, but the fungal symbiont of Meimuna opalifera was cultivable, possibly because it is at an early stage of fungal symbiont replacement. Genome sequencing of the fungal symbiont revealed its metabolic versatility, presumably capable of synthesizing almost all amino acids, vitamins, and other metabolites, which is more than sufficient to compensate for the Hodgkinia loss. These findings highlight a straightforward ecological and evolutionary connection between parasitism and symbiosis, which may provide an evolutionary trajectory to renovate deteriorated ancient symbiosis via pathogen domestication.
AB - Diverse insects are associated with ancient bacterial symbionts, whose genomes have often suffered drastic reduction and degeneration. In extreme cases, such symbiont genomes seem almost unable to sustain the basic cellular functioning, which comprises an open question in the evolution of symbiosis. Here, we report an insect group wherein an ancient symbiont lineage suffering massive genome erosion has experienced recurrent extinction and replacement by host-associated pathogenic microbes. Cicadas are associated with the ancient bacterial co-obligate symbionts Sulcia and Hodgkinia, whose streamlined genomes are specialized for synthesizing essential amino acids, thereby enabling the host to live on plant sap. However, our inspection of 24 Japanese cicada species revealed that while all species possessed Sulcia, only nine species retained Hodgkinia, and their genomes exhibited substantial structural instability. The remaining 15 species lacked Hodgkinia and instead harbored yeastlike fungal symbionts. Detailed phylogenetic analyses uncovered repeated Hodgkinia-fungus and fungus-fungus replacements in cicadas. The fungal symbionts were phylogenetically intermingled with cicada-parasitizing Ophiocordyceps fungi, identifying entomopathogenic origins of the fungal symbionts. Most fungal symbionts of cicadas were uncultivable, but the fungal symbiont of Meimuna opalifera was cultivable, possibly because it is at an early stage of fungal symbiont replacement. Genome sequencing of the fungal symbiont revealed its metabolic versatility, presumably capable of synthesizing almost all amino acids, vitamins, and other metabolites, which is more than sufficient to compensate for the Hodgkinia loss. These findings highlight a straightforward ecological and evolutionary connection between parasitism and symbiosis, which may provide an evolutionary trajectory to renovate deteriorated ancient symbiosis via pathogen domestication.
KW - Cicadas
KW - Ophiocordyceps
KW - Parasitic fungi
KW - Symbiont replacement
KW - Symbiotic fungi
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U2 - 10.1073/pnas.1803245115
DO - 10.1073/pnas.1803245115
M3 - Article
C2 - 29891654
AN - SCOPUS:85049028921
SN - 0027-8424
VL - 115
SP - E5970-E5979
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 - 26
ER -