Sequence data from isolated lichen-associated melanized fungi enhance delimitation of two new lineages within Chaetothyriomycetidae

Abstract

Lichen thalli provide a long-lived and stable habitat for colonization by a wide range of microorganisms. Increased interest in these lichen-associated microbial communities has revealed an impressive diversity of fungi, including several novel lineages which still await formal taxonomic recognition. Among these, members of the Eurotiomycetes and Dothideomycetes usually occur asymptomatically in the lichen thalli, even if they share ancestry with fungi that may be parasitic on their host. Mycelia of the isolates are characterized by melanized cell walls and the fungi display exclusively asexual propagation. Their taxonomic placement requires, therefore, the use of DNA sequence data. Here, we consider recently published sequence data from lichen-associated fungi and characterize and formally describe two new, individually monophyletic lineages at family, genus, and species levels. The Pleostigmataceae fam. nov. and Melanina gen. nov. both comprise rock-inhabiting fungi that associate with epilithic, crust-forming lichens in subalpine habitats. The phylogenetic placement and the monophyly of Pleostigmataceae lack statistical support, but the family was resolved as sister to the order Verrucariales. This family comprises the species Pleostigma alpinum sp. nov., P. frigidum sp. nov., P. jungermannicola, and P. lichenophilum sp. nov. The placement of the genus Melanina is supported as a lineage within the Chaetothyriales. To date, this genus comprises the single species M. gunde-cimermaniae sp. nov. and forms a sister group to a large lineage including Herpotrichiellaceae, Chaetothyriaceae, Cyphellophoraceae, and Trichomeriaceae. The new phylogenetic analysis of the subclass Chaetothyiomycetidae provides new insight into genus and family level delimitation and classification of this ecologically diverse group of fungi.

Life on top: cryptoendolithic ascomycetes and microalgae isolated from over 6000 m altitude

“…Notwithstanding the phylogenetic position of the here isolated strains, the lineage comprises two samples named Exophiala which may represent misidentified samples. Indeed Exophiala is a genus confirmed to belong to Herpotrichiellaceae (Quan et al 2020;Muggia et al 2021) and this has been strengthened by our results. The present dataset, indeed, includes 13 species of Exophiala (Supplementary Material Table S1) which, among others, represents the collapsed Herpotrichiellaceae clade in the phylogenetic analyses (Fig.…”

“…We report the phylogenetic analyses performed for each taxonomic group -Chaetothyriales, Dothideomycetes, Myrmecia and Trebouxia -based on the concatenated datasets of fungal nucITS-nucLSU and algal nucITS-rbcL, respectively. The Bayesian and the ML phylogenetic inferences were highly concordant, and clades were well supported and topologically congruent with previously published phylogenies (Moya et al 2018;Ametrano et al 2019b;Muggia et al 2020Muggia et al , 2021Quan et al 2020;Samolov et al 2020). The phylogenetic distance between the ML and BI topologies was 0.23 nRF for Chaetothyriales, 0.24 nRF for Dothideomycetes, 0.30 for Myrmecia and 0.17 for Trebouxia.…”

“…The MSAs included both the closest Genbank matches that were recovered for our strains and a broader taxon sampling comprising closely related genera and families selected from previous studies (Supplementary Material Tables S1-S4). In particular, the Chaetothyriales dataset was based on Quan et al (2020) and Muggia et al (2021), that of Dothideomycetes was based on Ametrano et al (2019a), that of Trebouxia s.str. on Muggia et al (2020) andDe Carolis et al, (2022), and that of Trebouxiophyceae s. lat.…”

Tackling fungal diversity in lichen symbioses: molecular and morphological data recognize new lineages in Chaetothyriales (Eurotiomycetes, Ascomycota)

“…The lichenicolous fungi which cryptically occur in lichens belong mainly to the classes Eurotiomycetes and Dothideomycetes and are represented by lamentous or yeast-like melanised taxa, which are closely related to the polyphyletic lineages of rockinhabiting fungi (RIF) and black yeasts (Gueidan et al 2008;Ruibal et al 2009; Gostinčar et al 2012; Quan et al 2020). These have frequently been reported from epilithic lichens (Harutyunyan et al 2008;Muggia et al 2016Muggia et al , 2017Muggia et al , 2021; Muggia and Grube 2018; Quan et al 2020). Only a few taxa, such as lichenicolous Phoma species in Phaeosphaeriaceae (Dothideomycetes), were reported both cryptically and symptomatically occurring in epilithic, epiphytic and soil inhabiting lichens (Lawrey et al 2012; Muggia et al 2016Muggia et al , 2017.…”

“…Indeed, three strains represent Pleostigma species, one Muellerella and another seven correspond to the recently described species Melanina gunde-cimermaniae. Muellerella is a well-known genus of symptomatic lichenicolous fungi which was successfully isolated from ascospores and conidia but occurs also cryptically in lichens(Muggia et al 2015(Muggia et al , 2019(Muggia et al , 2021. The strain L3774 which is in the clade 'Muellerella + Lichenodiplis' sensuMuggia et al (2015Muggia et al ( , 2019 was indeed isolated from a thallus of Tephromela atra (which is the original lichen host species of Muellerella atricola and Lichenodiplis lecanorae;Atienza et al 2009;Muggia et al 2015Muggia et al , 2019, but morphological inspections con rmed that this thallus is devoid of any perithecia or sporodochia, thus supporting the cryptic occurrence of the Muellerella fungus.The genera Pleostigma -together with the corresponding family Pleostigmataceae -and Melanina were recently described byMuggia et al (2021) to allocate black fungal strains that were isolated from alpine lichens (i.e.…”