Members of the genus Trichonympha are among the most well-known, recognizable and widely distributed parabasalian symbionts of lower termites and the wood-eating cockroach species of the genus Cryptocercus. 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 Trichonympha 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 Trichonympha collected from South American and Australian lower termites: Trichonympha hueyi sp. nov. from Rugitermes laticollis, Trichonympha deweyi sp. nov. from Glyptotermes brevicornis, Trichonympha louiei sp. nov. from Calcaritermes temnocephalus and Trichonympha webbyae sp. nov. from Rugitermes bicolor. We provide molecular barcodes to identify both the symbionts and their hosts, and infer the phylogeny of the genus Trichonympha based on small subunit rRNA gene sequences. The analysis confirms the considerable divergence of symbionts of members of the genus Cryptocercus, and shows that the two clades of the genus Trichonympha harboured by termites reflect only in part the phylogeny of their hosts.
YaminMA. 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). Sociobiology1979; 4:1–120
CepickaI, HamplV, KuldaJ. Critical taxonomic revision of parabasalids with description of one new genus and three new species. Protist2010; 161:400–433 [View Article][PubMed]
NodaS, MantiniC, MeloniD, InoueJ, KitadeO et al. Molecular phylogeny and evolution of Parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1α. PLoS One2012; 7:e29938 [View Article][PubMed]
BrugerolleG, LeeJJ. Phylum Parabasalia. In LeeJJ, LeedaleGF, BradburyP. (editors) An Illustrated Guide to the Protozoa Lawrence, KS: Allen Press Inc; 2000 pp. 1196–1250
JamesER, TaiV, ScheffrahnRH, KeelingPJ. Trichonympha burlesquei n. sp. from Reticulitermes virginicus and evidence against a cosmopolitan distribution of Trichonympha agilis in many termite hosts. Int J Syst Evol Microbiol2013; 63:3873–3876 [View Article][PubMed]
TaiV, JamesER, PerlmanSJ, KeelingPJ. 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 One2013; 8:e58728 [View Article][PubMed]
ScheffrahnRH, MullinsAJ, KrecekJ, ChaseJA, MangoldJR et al. Global elevational, latitudinal, and climatic limits for termites and the redescription of Rugitermes laticollis Snyder (Isoptera: Kalotermitidae) from the Andean Highlands. Sociobiology2015; 62:426–438[CrossRef]
JamesER, OkamotoN, BurkiF, ScheffrahnRH, KeelingPJ. Cthulhu Macrofasciculumque n. g., n. sp. and Cthylla Microfasciculumque n. g., n. sp., a newly identified lineage of parabasalian termite symbionts. PLoS One2013; 8:e58509 [View Article][PubMed]
BourguignonT, LoN, CameronSL, ŠobotníkJ, HayashiY et al. The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol Biol Evol2015; 32:406–421 [View Article][PubMed]
LegendreF, WhitingMF, BordereauC, CancelloEM, EvansTA 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 Evol2008; 48:615–627 [View Article][PubMed]
TragerW. The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. Biol Bull1934; 66:182–190 [View Article]
GouyM, GuindonS, GascuelO. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol2010; 27:221–224 [View Article][PubMed]
OhkumaM, IidaT, OhtokoK, YuzawaH, NodaS et al. Molecular phylogeny of parabasalids inferred from small subunit rRNA sequences, with emphasis on the Hypermastigea. Mol Phylogenet Evol2005; 35:646–655 [View Article][PubMed]
NguyenLT, SchmidtHA, von HaeselerA, MinhBQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol2015; 32:268–274 [View Article][PubMed]
Ikeda-OhtsuboW, BruneA. Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and 'Candidatus Endomicrobium trichonymphae'. Mol Ecol2009; 18:332–342 [View Article][PubMed]
KitadeO. Comparison of symbiotic flagellate faunae between termites and a wood-feeding cockroach of the genus Cryptocercus. Microbes Environ2004; 19:215–220[CrossRef]
OhkumaM, NodaS, HongohY, NalepaCA, InoueT. Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proc Biol Sci2009; 276:239–245 [View Article][PubMed]
KeelingPJ, PoulsenN, McfaddenGI. Phylogenetic diversity of parabasalian symbionts from termites, including the phylogenetic position of Pseudotrypanosoma and Trichonympha. J Eukaryot Microbiol1998; 45:643–650[PubMed][CrossRef]
International Commission on Zoological Nomenclature Declaration 45 – Addition of recommendations to Article 73 and of the term “specimen, preserved” to the Glossary. Bull Zool Nomencl2017; 73:96–97[CrossRef]