Molecular characterization and phylogeny of four new species of the genus (Parabasalia, Trichonymphea) from lower termite hindguts Free

Abstract

Members of the genus are among the most well-known, recognizable and widely distributed parabasalian symbionts of lower termites and the wood-eating cockroach species of the genus . Nevertheless, the species diversity of this genus is largely unknown. Molecular data have shown that the superficial morphological similarities traditionally used to identify species are inadequate, and have challenged the view that the same species of the genus can occur in many different host species. Ambiguities in the literature, uncertainty in identification of both symbiont and host, and incomplete samplings are limiting our understanding of the systematics, ecology and evolution of this taxon. Here we describe four closely related novel species of the genus collected from South American and Australian lower termites: sp. nov. from , sp. nov. from , sp. nov. from and sp. nov. from . We provide molecular barcodes to identify both the symbionts and their hosts, and infer the phylogeny of the genus based on small subunit rRNA gene sequences. The analysis confirms the considerable divergence of symbionts of members of the genus , and shows that the two clades of the genus harboured by termites reflect only in part the phylogeny of their hosts.

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2017-09-01
2024-03-28
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References

  1. Cleveland LR. Symbiosis between termites and their intestinal protozoa. Proc Natl Acad Sci USA 1923; 9:424–428[PubMed] [CrossRef]
    [Google Scholar]
  2. Kirby H. Flagellates of the genus Trichonympha in termites. Univ Calif Publ Zool 1932; 37:349–476
    [Google Scholar]
  3. Yamin MA. Flagellates of the order Trichomonadida Kirby, Oxymonadida Grassé, and Hypermastigida Grassi & Foà reported from the lower termites (Isoptera families Mastotermitidae, Kalotermitidae, Hodotermitidae, Termopsidae, Rhinotermitidae, and Serritermitidae) and from the wood-feeding roach Cryptocercus (Dictyoptera: Cryptocercidae). Sociobiology 1979; 4:1–120
    [Google Scholar]
  4. Cepicka I, Hampl V, Kulda J. Critical taxonomic revision of parabasalids with description of one new genus and three new species. Protist 2010; 161:400–433 [View Article][PubMed]
    [Google Scholar]
  5. Noda S, Mantini C, Meloni D, Inoue J, Kitade O et al. Molecular phylogeny and evolution of Parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1α. PLoS One 2012; 7:e29938 [View Article][PubMed]
    [Google Scholar]
  6. Brugerolle G, Lee JJ. Phylum Parabasalia. In Lee JJ, Leedale GF, Bradbury P. (editors) An Illustrated Guide to the Protozoa Lawrence, KS: Allen Press Inc; 2000 pp. 1196–1250
    [Google Scholar]
  7. Vickerman K. Mastigophora. In Parker SP. (editor) Synopsis and Classification of Living Organisms New York: McGraw-Hill; 1982 pp. 496–508
    [Google Scholar]
  8. Leidy J. On intestinal parasites of Termes flavipes. Proc Acad Sci Philadelphia 1877; 29:146–149
    [Google Scholar]
  9. James ER, Tai V, Scheffrahn RH, Keeling PJ. Trichonympha burlesquei n. sp. from Reticulitermes virginicus and evidence against a cosmopolitan distribution of Trichonympha agilis in many termite hosts. Int J Syst Evol Microbiol 2013; 63:3873–3876 [View Article][PubMed]
    [Google Scholar]
  10. Tai V, James ER, Perlman SJ, Keeling PJ. Single-cell DNA barcoding using sequences from the small subunit rRNA and internal transcribed spacer region identifies new species of Trichonympha and Trichomitopsis from the hindgut of the termite Zootermopsis angusticollis. PLoS One 2013; 8:e58728 [View Article][PubMed]
    [Google Scholar]
  11. Scheffrahn RH, Mullins AJ, Krecek J, Chase JA, Mangold JR et al. Global elevational, latitudinal, and climatic limits for termites and the redescription of Rugitermes laticollis Snyder (Isoptera: Kalotermitidae) from the Andean Highlands. Sociobiology 2015; 62:426–438 [CrossRef]
    [Google Scholar]
  12. James ER, Okamoto N, Burki F, Scheffrahn RH, Keeling PJ. Cthulhu Macrofasciculumque n. g., n. sp. and Cthylla Microfasciculumque n. g., n. sp., a newly identified lineage of parabasalian termite symbionts. PLoS One 2013; 8:e58509 [View Article][PubMed]
    [Google Scholar]
  13. Bourguignon T, Lo N, Cameron SL, Šobotník J, Hayashi Y et al. The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol Biol Evol 2015; 32:406–421 [View Article][PubMed]
    [Google Scholar]
  14. Legendre F, Whiting MF, Bordereau C, Cancello EM, Evans TA et al. The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers: implications for the evolution of the worker and pseudergate castes, and foraging behaviors. Mol Phylogenet Evol 2008; 48:615–627 [View Article][PubMed]
    [Google Scholar]
  15. Trager W. The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. Biol Bull 1934; 66:182–190 [View Article]
    [Google Scholar]
  16. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010; 27:221–224 [View Article][PubMed]
    [Google Scholar]
  17. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article][PubMed]
    [Google Scholar]
  18. Ohkuma M, Iida T, Ohtoko K, Yuzawa H, Noda S et al. Molecular phylogeny of parabasalids inferred from small subunit rRNA sequences, with emphasis on the Hypermastigea. Mol Phylogenet Evol 2005; 35:646–655 [View Article][PubMed]
    [Google Scholar]
  19. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article][PubMed]
    [Google Scholar]
  20. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article][PubMed]
    [Google Scholar]
  21. Carpenter KJ, Chow L, Keeling PJ. Morphology, phylogeny, and diversity of Trichonympha (Parabasalia: Hypermastigida) of the wood-feeding cockroach Cryptocercus punctulatus. J Eukaryot Microbiol 2009; 56:305–313 [View Article][PubMed]
    [Google Scholar]
  22. Ikeda-Ohtsubo W, Brune A. Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and 'Candidatus Endomicrobium trichonymphae'. Mol Ecol 2009; 18:332–342 [View Article][PubMed]
    [Google Scholar]
  23. Kitade O. Comparison of symbiotic flagellate faunae between termites and a wood-feeding cockroach of the genus Cryptocercus. Microbes Environ 2004; 19:215–220 [CrossRef]
    [Google Scholar]
  24. Ohkuma M, Noda S, Hongoh Y, Nalepa CA, Inoue T. Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proc Biol Sci 2009; 276:239–245 [View Article][PubMed]
    [Google Scholar]
  25. James ER, Burki F, Todd Harper J, Scheffrahn RH, Keeling PJ. Molecular characterization of parabasalian symbionts Coronympha clevelandii and Trichonympha subquasilla from the Hawaiian lowland tree termite Incisitermes immigrans. J Eukaryot Microbiol 2013; 60:313–316 [View Article][PubMed]
    [Google Scholar]
  26. Keeling PJ, Poulsen N, Mcfadden GI. Phylogenetic diversity of parabasalian symbionts from termites, including the phylogenetic position of Pseudotrypanosoma and Trichonympha. J Eukaryot Microbiol 1998; 45:643–650[PubMed] [CrossRef]
    [Google Scholar]
  27. International Commission on Zoological Nomenclature Declaration 45 – Addition of recommendations to Article 73 and of the term “specimen, preserved” to the Glossary. Bull Zool Nomencl 2017; 73:96–97 [CrossRef]
    [Google Scholar]
  28. Zhang ZQ. Species names based on photographs: debate closed. Zootaxa 2017; 4269:451–452[PubMed] [CrossRef]
    [Google Scholar]
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