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Anacanthotermes symbionts clarify the evolutionary history of termite-symbiotic Parabasalia

Kali SwichtenbergSchool of Life Sciences, Arizona State UniversityDaniel E. Jasso-SellesSchool of Life Sciences, Arizona State UniversityLeAnn NguyenSchool of Life Sciences, Arizona State UniversitySerena G. AguilarSchool of Life Sciences, Arizona State UniversityKelsi B McAnallySchool of Life Sciences, Arizona State UniversityStephen J. TaerumConnecticut Agricultural Experiment StationUlugbek TogaevAcademy of Science of Uzbekistan, Institute of Bioorganic ChemistryIkram Iskandarovich AbdullaevAcademy of Sciences of Uzbekistan, Khorezm Academy of MamunDavid Sillam-DussèsLaboratory of Experimental and Comparative Ethology, University Sorbonne Paris NordJan ŠobotníkBiology Center, Czech Academy of Sciences, Institute of EntomologyGillian H. GileSchool of Life Sciences, Arizona State University
ABI

Аннотация

The obligate symbiosis between wood-feeding termites and their intestinal microbial eukaryotes (protists) is a classic example of co-diversification. Closely related termites tend to harbor closely related protists, and certain protist lineages are restricted in their distribution to a particular host lineage, but there are exceptions to these trends. Horizontal symbiont transfer has been suggested to account for some of the discrepancies, but its extent is not clear, largely because the symbionts of many termite lineages have not yet been characterized by molecular methods. Anacanthotermes is one such understudied termite lineage. Anacanthotermes belong to the harvester termite family, Hodotermitidae, in the deep-branching termite clade Teletisoptera. Some of their symbiont genera, such as Rostronympha , Spiromastigotes , Kirbynia , and Polymastigoides , are unique to Anacanthotermes hosts. Other reported symbionts, such as Holomastigotes and Holomastigotoides , are known to inhabit distantly related termite lineages, which is surprising, and suggests either incorrect classification or horizontal symbiont transfer. In this study, we have used microscopy, single cell PCR, and long-read amplicon sequencing to characterize the morphology and phylogenetic position of Anacanthotermes symbionts and infer their coevolutionary history with their hosts. The symbionts belong to the Parabasalia classes Trichonymphea, Cristamonadea, Spirotrichonymphea, and Trichomonadea. Our results suggest that the Parabasalia class Spirotrichonymphea originated and diversified within the termite lineage Teletisoptera, rather than in the ancestor of termites as previously assumed, and therefore all occurrences of Spirotrichonymphea outside Teletisoptera are due to symbiont transfers.

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