A new connection between wood saprobism and beetle endosymbiosis: the rarely reported saprobic discomycete Tromeropsis is congeneric with the symbiotic yeast Symbiotaphrina (Symbiotaphrinales, Xylonomycetes) and two asexual morphs misplaced in Hyphozyma

Abstract

The only hitherto known species of the monotypic genus Tromeropsis, the rarely reported T. microtheca, is redescribed from recent collections on mostly little decayed, grayed, xeric, sun-exposed wood of decorticated trunks and branches of different gymnosperms, exceptionally angiosperms, from different humid regions of central Europe and a dry area in Macaronesia. Two further, very similar species are here newly described from decayed xeric wood of different angiosperm trees and shrubs from dry to arid regions of North America, Australia, and Macaronesia. Characteristics of the genus are: black sessile apothecia, dark olivaceous exudate, fissitunicate multi-spored asci, minute, cylindrical to ellipsoid, hyaline ascospores, a yeast-like asexual morph, and, in some species, a synanamorph with allantoid conidia formed on integrated conidiogenous cells reminiscent of the genus Lecythophora but with holoblastic conidiogenesis. A lectotype is designated for the type species of the likewise sexually typified, monotypic, illegitimate genus Microspora, M. dura, which was re-examined from the original material and found to be a later synonym of T. microtheca. Nuclear rDNA data were obtained from two collections of T. microtheca and four collections of the two new species. DNA sequences of T. microtheca match those from asexual morph isolates or environmental samples in public databases. Different misapplied names attributed to sequences from asexual morph isolates gained from coniferous wood from northern Europe, North America, and eastern Asia were re-identified as T. microtheca. A very close relationship between Tromeropsis and the type species of the asexually typified genus Symbiotaphrina, S. buchneri, was observed. Independent molecular phylogenetic analyses of three rDNA regions (partial SSU, ITS, partial LSU) each place Tromeropsis and the type species of Symbiotaphrina in a single supported clade without showing clear limits between the two genera. Based on multigene analysis, Symbiotaphrina was recently placed together with the small order Xylonales in the new class Xylonomycetes. We here validate the order Symbiotaphrinales previously published as nom. nud. and describe the family Symbiotaphrinaceae. Since the name Symbiotaphrina was validated one year before Tromeropsis was published, and is more widely used, it is adopted here and T. microtheca combined into Symbiotaphrina. rDNA data further suggest that two members of the asexually typified genus Hyphozyma, H. lignicola and H. sanguinea, belong to Symbiotaphrina, whereas the type species of Hyphozyma, H. variabilis, clusters in the Thelebolales (Leotiomycetes), where it is a later synonym of Cleistothelebolus nipigonensis, the type species of Cleistothelebolus. The new combinations S. lignicola and S. sanguinea are proposed, to which the newly described species S. desertorum and S. larreae are added. Based on their close relationship and a similar yeast-like asexual morph in pure culture, we hypothesize that the life cycles of all these wood-inhabiting taxa include a symbiotic phase in the gut of arthropods and, conversely, we suppose that the life cycles of S. buchneri and S. kochii include unknown sexual morphs growing on plant substrate.