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Mycological Progress

, Volume 17, Issue 1–2, pp 215–254 | Cite as

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

  • H. O. Baral
  • E. Weber
  • G. Marson
  • L. Quijada
Original Article

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.

Keywords

Cleistothelebolus Desiccation tolerance Endosymbiont Fissitunicate Polyspory Xylona 

Notes

Acknowledgements

We are very thankful to Martin Bemmann for providing relevant literature and Regina Siemianowski and Lothar Krieglsteiner for sending their data of Bavarian collections of S. microtheca and two specimens for study. Keith A. Seifert is gratefully thanked for giving us detailed location data about his Canadian isolate, Eeva Terhonen and Anders Dahlberg for data of their isolates from Finland, Eeva also for supplying the whole set of sequences referrable to S. microtheca, and Natalija Burnevica & Rimvys Vasaitis and Vaidotas Lygis for chromatograms of their Finnish and Lithuanian strains, respectively. Sylvie Hermant from the National Natural History Museum in Luxembourg is greatly thanked for gaining sequences of Symbiotaphrina (Tromeropsis) spp. G.J.M. Verkleij (Westerdijk Fungal Biodiversity Institute) is acknowledged for providing LSU sequences of our S. microtheca cultures deposited in CBS, and Peik Haugen for help in the identification of intron positions. Roland Kirschner is thanked for critical comments and valuable contributions.

Abbreviations

*, Living state; †, Dead state; IKI, Lugol’s solution (highly concentrated): ~ 1% I2, 2% KI, in H2O; KOH, Potassium hydroxide, 5–10%; CRSDS, Congo Red with sodium dodecyl sulfate; CRB, Brilliant Cresyl Blue, ~ 1% in H2O; LBs, Lipid bodies (oil drops); ø, Unpreserved; a.i., Asexual morph obtained from ascospore isolate; a.o., Asexual morph only; d.v., Documentation seen; n.v., No material or documentation seen. Values in { } indicate the number of collections that were examined. Private herbaria: H.B., H.O. Baral; G.M., G. Marson; R.S., Regina Siemianowski (in Herbarium Nationalpark Bayerischer Wald); official herbaria listed in the Index Herbariorum: H (Helsinki), M (Munich), PRM (Prague), TFC Mic. (Herbarium of the University of La Laguna, section mycology)

Addendum

A sequence of S. microtheca from one of the collections on Fagus (H.B. 10124) was obtained too late to be included in the manuscript. In the ITS region, it fully agrees with the collection on Abies (H.B. 10054, KY657581) and thus confirms our previous finding, based on a sequence of the collection on Adenocarpus (TFC Mic. 24159, MF594685), that S. microtheca can also occur on angiosperm hosts.

Supplementary material

11557_2017_1340_MOESM1_ESM.fas (11 kb)
Online Resource 1 Alignment of partial SSU corresponding to ML phylogeny of Fig. 1. (FAS 10 kb)
11557_2017_1340_MOESM2_ESM.fas (11 kb)
Online Resource 2 Alignment of partial LSU corresponding to ML phylogeny of Fig. 2 (FAS 10 kb)
11557_2017_1340_MOESM3_ESM.fas (16 kb)
Online Resource 3 Alignment of ITS1-5.8S-ITS2 corresponding to ML phylogeny of Fig. 3. (FAS 16 kb)
11557_2017_1340_MOESM4_ESM.fas (7 kb)
Online Resource 4 Alignment of S1506 intron corresponding to ML phylogeny of Fig. 4. (FAS 6 kb)
11557_2017_1340_MOESM5_ESM.fas (33 kb)
Online Resource 5 Alignment of partial SSU + ITS1-5.8S-ITS2 + partial LSU corresponding to ML phylogeny of Fig. 5. (FAS 32 kb)

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Copyright information

© German Mycological Society and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.TübingenGermany
  2. 2.National Natural History MuseumLuxembourg CityLuxembourg
  3. 3.Departamento de Botánica, Ecología y Fisiología Vegetal, Facultad de Ciencias, Sección de BiologíaUniversidad de La LagunaLa Laguna, TenerifeSpain

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