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Article

The Evolution of Life Modes in Stictidaceae, with Three Novel Taxa

by
Vinodhini Thiyagaraja
1,2,3,
Robert Lücking
4,
Damien Ertz
5,6,
Samantha C. Karunarathna
3,7,
Dhanushka N. Wanasinghe
3,7,
Saisamorn Lumyong
8,9 and
Kevin D. Hyde
2,3,8,10,*
1
Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand
2
Centre of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand
3
CAS Key Laboratory for Plant Biodiversity and Biogeography of East Asia (KLPB), Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, China
4
Botanischer Garten und Botanisches Museum, Freie Universität Berlin, Königin-Luise-Str. 6-8, 14195 Berlin, Germany
5
Research Department, Meise Botanic Garden, Nieuwelaan 38, BE-1860 Meise, Belgium
6
Fédération Wallonie-Bruxelles, Service Général de l’Enseignement Supérieur et de la Recherche Scientifique, Rue A. Lavallée 1, BE-1080 Bruxelles, Belgium
7
World Agro forestry Centre East and Central Asia, Kunming 650201, China
8
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
9
Center of Excellence in Bioresources for Agriculture, Industry and Medicine, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
10
Innovative Institute of Plant Health, Zhongkai University of Agriculture and Engineering, Haizhu District, Guangzhou 510225, China
*
Author to whom correspondence should be addressed.
J. Fungi 2021, 7(2), 105; https://doi.org/10.3390/jof7020105
Submission received: 27 December 2020 / Revised: 26 January 2021 / Accepted: 28 January 2021 / Published: 2 February 2021
(This article belongs to the Special Issue Fungal Biodiversity and Ecology)
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Versions Notes

Abstract

:
Ostropales sensu lato is a large group comprising both lichenized and non-lichenized fungi, with several lineages expressing optional lichenization where individuals of the same fungal species exhibit either saprotrophic or lichenized lifestyles depending on the substrate (bark or wood). Greatly variable phenotypic characteristics and large-scale phylogenies have led to frequent changes in the taxonomic circumscription of this order. Ostropales sensu lato is currently split into Graphidales, Gyalectales, Odontotrematales, Ostropales sensu stricto, and Thelenellales. Ostropales sensu stricto is now confined to the family Stictidaceae, which includes a large number of species that are poorly known, since they usually have small fruiting bodies that are rarely collected, and thus, their taxonomy remains partly unresolved. Here, we introduce a new genus Ostropomyces to accommodate a novel lineage related to Ostropa, which is composed of two new species, as well as a new species of Sphaeropezia, S. shangrilaensis. Maximum likelihood and Bayesian inference analyses of mitochondrial small subunit spacers (mtSSU), large subunit nuclear rDNA (LSU), and internal transcribed spacers (ITS) sequence data, together with phenotypic data documented by detailed morphological and anatomical analyses, support the taxonomic affinity of the new taxa in Stictidaceae. Ancestral character state analysis did not resolve the ancestral nutritional status of Stictidaceae with confidence using Bayes traits, but a saprotrophic ancestor was indicated as most likely in a Bayesian binary Markov Chain Monte Carlo sampling (MCMC) approach. Frequent switching in nutritional modes between lineages suggests that lifestyle transition played an important role in the evolution of this family.

1. Introduction

Lichenization is a successful lifestyle, forming a stable symbiotic association between fungi with cyanobacteria and/or algae. About 13% of the known fungal species form lichens, and these dominate around 7% of the earth’s terrestrial surface [1,2,3]. The origin of lichenization remains controversial. Molecular studies show that lichenization and de-lichenization events occurred independently in different lineages of Ascomycota and Basidiomycota [1,3,4,5,6,7,8,9,10,11,12].
Lecanoromycetes is the largest lichenized lineage in Ascomycota, comprising more than 15,000 species [1,13,14,15]. It currently contains four subclasses: Acarosporomycetidae, Lecanoromycetidae, Ostropomycetidae, and Umbilicariomycetidae [1,16]. Within subclass Ostropomycetidae, Ostropales sensu lato exhibits a remarkable transition toward larger, non-lichenized, saprotrophic or biotrophic lineages, including a loss of lichenization within Stictidaceae, making this group the most striking example comprising secondarily delichenized lineages in Lecanoromycetes [1,3,13,17,18].
Ostropales was introduced by Nannfeldt in 1932 to encompass a single family Ostropaceae, which is a younger synonym of Stictidaceae [19]. Various molecular studies have been conducted to resolve the phylogenetic relationships within Ostropales [18,19,20,21,22,23,24,25,26,27,28]. The delimitation of Ostropales has changed over time due to a high level of morphological plasticity [18,19], and the taxonomy of various groups remains unresolved [29]. Ostropales was recently very broadly defined [1] and reduced to a single family, Stictidaceae, whereas related families are now recognized in the separate orders Graphidales, Gyalectales, Odontotrematales, and Thelenellales [13,30]. Stictidaceae includes mostly small, drought-tolerant fungi [31], which have been poorly studied, and their generic delimitation is yet to be resolved [19,31,32]. There are many opportunities for discovering new species, even in well-studied areas [19].
Species of Stictidaceae are mainly saprotrophic and partly lichenized or lichenicolous, and they inhabit mostly bark and rock substrata [32]. Some species show optional lichenization; i.e., the same fungus may be either lichenized when growing on bark or saprotrophic when developing on wood [32]. Many species of Stictidaceae are characterized by ascomata with crystalline excipular incrustations and by long, filiform ascospores [24]. Sherwood [33] provided a detailed monograph of this family with special emphasis on taxa recorded from the USA.
Here, we provide updated multi-gene phylogenetic analyses for Ostropales and related orders focusing on Stictidaceae, thereby describing a newly discovered genus and three new species. Detailed morphological descriptions are provided for the new taxa. In addition, ancestral character state analysis was performed to assess the origin and transition of the various lifestyles occurring in the family.

2. Materials and Methods

2.1. Phenotypic Analysis

The bark and stem plant materials of newly described taxa were collected from China and Thailand and brought to the laboratory in paper bags. Materials were examined using a Motic SMZ 168 Series microscope. Hand sections of the ascomata were mounted with water, 5% KOH and KI (5% KOH and Lugol’s solution), and examined. Sections of ascomata and other micro-morphological characteristics were photographed using a Nikon ECLIPSE 80i compound microscope fitted with a Canon 550D digital camera. All microscopic measurements refer to dimensions in water and were made with Tarosoft Image Frame Work (0.9.0.7), and images used for figures were processed with Adobe Photoshop CS6 Extended 10.0 software (Adobe Systems, San Jose, CA, USA). The specimens were deposited in the Mae Fah Luang University (MFLU) Herbarium, Chiang Rai, Thailand. Index Fungorum and Faces of Fungi were registered following Index Fungorum [34] and Jayasiri et al. [35].

2.2. DNA Extraction, PCR Amplification, and Gene Sequencing

Genomic DNA was extracted directly from the ascomatal tissue and thalli of fungi as outlined by Wanasinghe et al. [36]. An E.Z.N.A.® Forensic DAT (D3591–01, Omega Bio–Tek) DNA extraction kit was used to extract DNA by following the manufacturer’s instructions. DNA samples that were intended for use as a template for PCR were stored at 4 °C for use in regular work, and duplicates were stored at −20 °C for long-term storage. The mitochondrial small subunit spacers (12S, mtSSU), large subunit nuclear rDNA (28S, LSU) and internal transcribed spacers (ITS) were amplified with primer pairs mtSSU1 and mtSSU3R [37], LR0R and LR5 [38], and ITS5 and ITS4 [39]. The PCR amplification for each gene was performed using a final volume of 25 µL, which was comprised of 2.0 µL of DNA template, 1 µL of each forward and reverse primers, 12.5 µL of Taq PCR Super Mix (mixture of Easy Taq TM DNA Polymerase, dNTPs, obtained buffer (Beijing Trans Gen Biotech Co., Chaoyang District, Beijing, China)) and 8.5 µL of sterilized water.
The PCR amplifications were performed following Zoller et al. [37], Vilgalys and Hester [38], and White et al. [39] for the genes mtSSU, LSU, and ITS respectively. Finally, PCR products were examined on 1% agarose electrophoresis gels and stained with ethidium bromide. Purification and DNA sequencing were performed at Shanghai Sangon Biological Engineering Technology & Services Co. (Shanghai, China). The nucleotide sequence data acquired were deposited in GenBank. Alignments and phylogenetic trees were submitted to TreeBASE under submission number 27653.

2.3. Phylogenetic Analyses and Species Recognition

The Basic Local Alignment Search Tool (BLAST) search engine of the National Center for Biotechnology Information (NCBI) was used for the preliminary identification of DNA sequences of the new taxa [40]. Sequences of available closely related taxa for Ostropales were retrieved from GenBank (Table 1), including all representatives available of Stictidaceae. Phylogenetic analyses were constructed based on mtSSU, LSU, and ITS sequence data. Outgroup taxa were selected following Lücking [30]. The final combined alignment of Stictidaceae comprised 2530 nucleotide positions and resulted in 107 taxa. We also conducted a multi-marker phylogenetic analysis of Ostropomycetidae to check the placement of Ostropales sensu stricto following Kraichak et al. [13] and Lücking [30] for 167 taxa based on mtSSU, LSU, and ITS sequence data.
Phylogenetic analyses of both individual and combined aligned data were performed under Maximum Likelihood (ML) and Bayesian criteria. The multiple alignments of all consensus sequences, as well as the reference sequences were automatically generated with MAFFT v. 7 [41]. Terminal ends of sequences and ambiguous regions were trimmed manually using BioEdit v. 7.0.5.2 [42] and excluded from the dataset. The phylogenetic web tool “ALTER” [43] was used to convert sequence alignment from FASTA to PHYLIP for RAxML analysis and from FASTA to NEXUS format for Bayesian analysis. The estimated model of ML and Bayesian analyses were performed independently for each locus using MrModeltest v.2.2 [44]. ML was generated using the RAxML-HPC2 on XSEDE (8.2.8) in the CIPRES Science Gateway platform [45] with 1000 separate runs using the GTR+I+G model of evolution. MrBayes v. 3.1.2 was used to perform Bayesian analysis [46]. MCMC was run for 50,000,000 generations, and trees were sampled every 100th generation. The first 10% of trees that represented the burn-in phase were discarded, and only the remaining 90% of trees were used for calculating posterior probabilities (PP) for the majority rule consensus tree. The resulting trees were drawn in FigTree v1.4.0 [47]; then, they were copied to Microsoft PowerPoint 2013 and converted to jpeg files using Adobe Photoshop CS6 Extended 10.0 (Adobe Systems, San Jose, CA, USA).

2.4. Ancestral Character State Analyses

We employed ancestral character reconstruction to study the evolutionary history of selected characters [48], specifically lifestyle changes among Ostropales sensu lato and possible gains and losses of lichenization. The following lifestyle states were used: lichenized with chlorococcoid algae, lichenized with trentepohlioid algae, non-lichenized saprotrophic and lichenicolous. RASP 3.2.1 (Reconstruct Ancestral State in Phylogenies) was used to conduct ancestral character analysis, using the two approaches, Bayes Traits and Bayesian Binary MCMC [49,50]. Both approaches were performed and visualized using default settings as follows: 1,010,000 iterations for BayesTraits with a burn-in of 10,000, sampling 1000 trees and with 10 ML trees; 50,000 generations for Bayesian Binary MCMC, with 10 chains, a sample frequency of 100, a temperature of 0.1, state frequencies fixed (JC), and among-site rate variation equal.

3. Results

3.1. Phylogenetic Analyses

Ostropales sensu lato were well recovered including Graphidales, Gyalectales, Ostropales sensu stricto (=Stictidaceae), and Thelenellales (Figure 1). No conflict was detected by comparing the significantly supported relationships of the individual topologies of the three markers (mtSSU, LSU, and ITS) that were subsequently concatenated (Supplementary Figures S1–S6). In a second step, we improved the terminal resolution in Stictidaceae by using only closely related lineages as an outgroup (Figure 2). Thereby, Stictidaceae included the following sequenced genera: Absconditella, Carestiella, Cryptodiscus, Cyanodermella, Eriospora, Fitzroyomyces, Geisleria, Glomerobolus, Hormodochis, Ingvariella, Nanostictis, Neostictis, Neofitzroyomyces, Ostropa, the new genus Ostropomyces, Phacidiella, Robergea, Schizoxylon, Sphaeropezia, Stictis, Trinathotrema, and Xyloschistes. All genera were resolved as monophyletic except Stictis (Figure 2).
The best scoring RAxML tree was selected to represent the relationships among the taxa, with the final ML optimization likelihood value of −29077.976127 (Figure 2). The parameters for the GTR+I+G model of combined mtSSU, LSU, and ITS were as follows: estimated base frequencies A = 0.287442, C = 0.205916, G = 0.252694, T = 0.253948, substitution rates AC = 1.393327, AG = 2.735680, AT = 2.386601, CG = 0.840662, CT = 5.674536 and GT = 1.000000. The ML and Bayesian analyses both resulted in trees with similar topologies. Bayesian posterior probabilities from MCMC were evaluated with a final average standard deviation of split frequencies = 0.005790.

3.2. Ancestral Character State Analysis

The recently introduced genera, such as Eriospora, Fitzroyomyces, Neofitzroyomyces, Neostictis, and Phacidiella, show saprotrophic lifestyle (Figure 3). Stictis was recovered as polyphyletic, with taxa expressing a lichenized or saprotrophic lifestyle or optional lichenization. Most species of Stictis show a saprotrophic lifestyle, including the type species of the genus, Stictis radiata. Stictis urceolata, as well as the lineage formed by S. populorum and S. confusa, are lichenized with chlorococcoid green algae. Stictis mollis is optionally lichenized, with specimens being either saprotrophic (GG2445a, GG2458b) or lichenized (GG2370, GG2440b). Species of Schizoxylon also show either a saprotrophic lifestyle or optional lichenization: a lichenized specimen of S. albescens (GG2696a) was isolated from the bark of Populus tremula, while a saprotrophic specimen (GG236) was isolated from dead twigs and branches of Populus tremula. Lichenized and facultatively lichenized Stictidaceae are generally associated with chlorococcoid green algae, except for Trinathotrema stictideum, which associates with a trentepohlioid photobiont (Figure 3). The genera Absconditella and Geisleria form a lichenized lineage, while the lichenized Ingvariella is part of a distinct lineage close to the saprotrophic Xyloschistes platytropa. Lichenicolous species are nested with saprotrophic species in the genera Cryptodiscus and Sphaeropezia. Three different lifestyles (lichenized, saprotrophic, and lichenicolous) are present within the genus Cryptodiscus.
Bayesian binary MCMC and Bayes traits analyses give different results regarding the ancestral character analysis. Stictidaceae as a whole was recovered as basally non-lichenized in the Bayesian Binary MCMC tree, suggesting multiple secondary lichenizations of the lichenized lineages within the family. The results for Bayes traits were ambiguous for the basal nodes, not allowing any conclusions about the directionality of lichenization and delichenization.

3.3. Taxonomy

Ostropales Nannf., Nova Acta Regiae Societatis Scientiarum Upsaliensis, Ser. 4, 8 (2): 68 [51]
Kraichak et al. [13] and Lücking [30] reduced Ostropales sensu stricto to the single family Stictidaceae, which is a classification that is followed here.
Stictidaceae Fr., Summa vegetabilium Scandinaviae 2: 345, 372 [52]
Syn.: Ostropaceae Rehm (as ‘Ostropeae’), Rabenh. Krypt.-Fl., Edn 2 (Leipzig) 1.3 (lief. 30): 185 (1888) (1896)
Type: Stictis Pers., Observationes mycologicae 2: 73 (1800)
Stictidaceae comprises both lichenized and non-lichenized fungi [1,3,18,19,28,31,32,33,53,54,55,56,57,58,59,60,61]. Based on Fries’s classification [62], Stictis (including subgen. Propolis and subgen. Xylographa) and Cryptomyces were tentatively included in Stictidaceae. After 1830, the improvement of microscopic-based studies lead to more detailed insight into hymenial configuration. Corda [63] divided immersed, non-stromatic discomycetes into four genera in which he included Stictis with unicellular, colorless, and ovoid spores. However, species and generic-level delineation remained uncertain from 1832 to 1932. Fries [52] again assigned Cryptomyces, Propolis, Xylographa, Naevia, and Propolis to Stictidaceae, ignoring the microscopic classification by Corda. After the inclusion of many genera, Ostropales was erected by Nannfeldt [51] with a single family Ostropaceae. Later, this family was synonymized under Stictidaceae, with the type genus Stictis [33,53].
The classification of the family Stictidaceae has changed over time [1,14,15,23,33,52,53,62,63,64,65,66]. Its detailed taxonomy was first studied by Sherwood, focusing on excipular structure, ascospore type, and biology [33,53]. Stictidaceae was traditionally classified as saprotrophic lineage in Ostropales [67]. Gilenstam [68] initially included Conotrema as a lichenized genus in the family, whereas currently various lichenized lineages are distinguished, including Absconditella, Geisleria, Ingvariella, and Trinathotrema. Among these, Trinathotrema is the only genus associated with a trentepohlioid photobiont, while other lichenized genera are associated with chlorococcoid photobionts [67,69,70,71]. Winka et al. [72] accepted both lichenized and non-lichenized fungi within this family based on combined multi-gene analysis.
Presently, Stictidaceae comprises 33 genera: Absconditella, Acarosporina, Biostictis, Carestiella, Conotremopsis, Cryptodiscus, Cyanodermella, Delpontia, Dendroseptoria, Eriospora, Fitzroyomyces, Geisleria, Glomerobolus, Hormodochis, Ingvariella, Karstenia, Lillicoa, Nanostictis, Neostictis, Neofitzroyomyces, Ostropa, Ostropomyces, Phacidiella, Propoliopsis, Robergea, Schizoxylon, Sphaeropezia, Stictis, Stictophacidium, Thelopsis, Topelia, Trinathotrema, and Xyloschistes [1,14,15,64]. Generic classification in the family is challenging, given that the convergent evolution of ascoma types is frequent [19] and both apothecoid and perithecoid ascomata have evolved several times in separate lineages [33,73]. However, our updated phylogeny suggests that the only problematic genus at the moment is Stictis sensu lato.
Ostropomyces Thiyagaraja, Lücking, Ertz and K.D. Hyde, gen. nov. Index Fungorum number: IF 556555; Faces of Fungi number: FoF 09511 Etymology: name refers to the characteristics similar to Ostropa.
Type species: Ostropomyces pruinosellus Thiyagaraja, Lücking, Ertz and K.D. Hyde sp. nov.
Saprobic on bark, thallus whitish, pruinose. Sexual morph: Ascomata perithecial, solitary, immersed to erumpent. Ostiole distinct. Exciple with clear border between outer and inner layer. Hamathecium comprising filamentous paraphyses. Paraphyses septate, branched, hyaline, filamentous. Asci cylindrical, bitunicate. Ascospores overlapping uniseriate, hyaline, transversely multi-septate, cells almost of equal size, deeply constricted at the septa of each cell, easily breaking into small septate part-spores. Asexual morph: Pycnidia erumpent, globose. Pycnidial wall in transverse section shows two distinct layers. Outer layer hyaline, densely packed. Inner layer hyaline, loosely packed, cells elongate in pycnidial neck. Conidiophores lining inside and outside of pycnidia wall. Conidiogenous cells hyaline. Conidia similar in shape to ascospore, filiform, aseptate, hyaline, and guttulate at maturity.
Notes: Ostropomyces is introduced to accommodate two newly discovered species, Ostropomyces pruinosellus and Ostropomyces thailandicus, which are collected from tropical forests in Northern Thailand. The new genus is related to Ostropa, but both emerge on long stem branches in our phylogenetic analyses (Figure 2). Ostropomyces differs from Ostropa in the presence of perithecial ascomata, presence of periphysoids, which are present in the inner face of the wall, in the lack of an apical cap in the ascus and four-spored asci. In contrast, Ostropa forms orbicular ascomata opening by a transverse slit, periphysoids in the above part, a prominent apical cap in the ascus, and eight-spored or polysporous asci [33]. The new genus formed a distinct clade with high bootstrap support in the multi-gene phylogenetic analyses, whereas its relationship to Ostropa was also strongly supported (84%).
The morphological characteristics would initially suggest that O. thailandicus may represent an asexual state of O. pruinosellus. However, both lineages formed comparatively long branches in the phylogenetic analysis, indicating that they represent two closely related yet separate species—one known by its sexual morph and the other by its asexual state. Therefore, we introduce O. thailandicus and O. pruinosellus as new species in Ostropomyces. The taxa are characterized by immersed to erumpent fruiting bodies with pseudostromatic masses, orbicular in cross-section, loosely packed hyphae, with numerous periphysoids, numerous, branched, and filiform true paraphyses, long-cylindrical asci without prominent apical cap, four-spored asci, ascospores filiform, colorless, and transversely multi-septate.
Ostropomyces pruinosellus Thiyagaraja, Lücking, Ertz and K.D. Hyde, sp. nov. (Figure 4).
Index Fungorum number: IF 556556; Faces of Fungi number: FoF 09512 Etymology: The name refers to the pruinose surface of the substrate where the fungus produces ascomata.
Holotype: MFLU 20-0538
Saprobic on unidentified dead stem. Surface of the substrate where the ascomata are formed brownish white, appearing pruinose. Prothallus absent. Sexual morph: Ascomata perithecial, 310–350 μm high, 340–500 μm wide (x = 330 × 420 μm, n = 5), immersed to erumpent, solitary, margin partly protruding beyond the surface layers of stem, not carbonized, color unchanged in KOH, orbicular in cross-section, lined with numerous periphysoids. Exciple thickened, outer layer 10–45 μm thick, densely packed, darker than inner layer, inner layer 3–8 μm thick (x = 27.5 × 5.5 μm, n = 10), hyaline, of loosely packed hyphae, with numerous crystalline inclusions and periphysoids extended to the entire inner face of the wall in the 2/3 upper part of the ascomata. Hamathecium comprising paraphyses and asci. Paraphyses septate, branched, hyaline, 0.5–1.3 μm thick, generally exceeding the length of asci. Asci 165–245 × 7–11 μm (x = 205 × 9 μm, n = 40), bitunicate, cylindrical, four-spored, apical wall thickened to 2.2–3.2 μm. Ascospores 160–180 × 2–3 μm (x = 170 × 2.5 μm, n = 40), hyaline, transversely multi-septate, each cells almost of equal size, each locus 2–4 μm long, deeply constricted at each septa, easily breaking apart into small, septate, part-spores. Asexual morph: Undetermined.
Spot reactions: Asci KI-, Ascospores KI-
Material examined: Thailand, Mueang Khong, Chiang Dao District, Chiang Mai, N 97°92′86″, E 17°71′45″, 558 m elevation, on unidentified dead stem, 16 February 2019, Vinodhini Thiyagaraja, S1DA (holotype: MFLU 20-0538).
Notes: Ostropomyces pruinosellus is similar to species in Ostropa but differs in the characters listed in the genus discussion. Although the species is saprotrophic and not lichenized, the surface of the substrate where the ascomata emerges has a pruinose appearance, at first glance suggesting the presence of a thallus. However, the apparent thallus is absent. Initially, the ascomata were immersed and became erumpent at maturity.
Ostropomyces thailandicus Thiyagaraja, Lücking, Ertz and K.D. Hyde sp. nov.
Index Fungorum number: IF 556557; Faces of Fungi number: FoF 09513 Etymology: The name refers to the country where the type specimen of the new species was collected.
Holotype: MFLU 20-0539
Saprobic on dead stem. Area with pycnidia with a pruinose appearance on the surface. Prothallus absent. Sexual morph: Undetermined. Asexual morph: Pycnidia ca 100 μm diam., globose, erumpent, darkening above. Pycnidial wall in transverse section composed of two distinct layers. Outer layer 19–27 μm wide, hyaline, densely packed, darker than inner layer. Inner layer hyaline, loosely packed, 11–23 μm wide. Conidiophores reduced to 9–15 μm. Conidiogenous cells 9–15 μm, cylindrical, hyaline, lining the inside and outside of the pycnidia wall. Conidia 8–13 × 1–3 μm (x = 10.5 × 2 μm, n = 10), filiform, apical proliferation of the conidiogenous cell, aseptate, hyaline.
Spot reactions: Conidiophore KI-, Conidia KI-
Material examined: Thailand, Mueang Khong, Chiang Dao District, Chiang Mai, N 97°92′86″, E17°71′45″, 558 m elevation, on unidentified dead stem, 16 February 2019, Vinodhini Thiyagaraja, S1D1T2 (holotype: MFLU 20-0539).
Notes: The new strain was collected from Thailand on the same material from which Ostropomyces pruinosellus was isolated (Figure 5). The species are delineated based on DNA sequence data as recommended by Jeewon and Hyde [74]. The phylogenetic tree supported O. pruinosellus and O. thailandicus as two distinct species, with more than 2% differences in LSU and ITS base pair comparisons. Ostropomyces thailandicus formed pycnidial conidiomata, reduced conidiophore into conidiogenous cells, hyaline, and filiform conidia similar to other asexual fungi recorded in Stictidaceae such as Acarosporina microspora, Cyanodermella oleoligni, Stictis radiata, and S. urceolata [28,31,33,68,75].
Sphaeropeziashangrilaensis Thiyagaraja, Lücking, Ertz and K.D. Hyde, sp. nov. (Figure 6) Index Fungorum number: IF 556558; Faces of Fungi number: FoF 09514 Etymology: Refers to the location in China (Shangri-La) where the type specimen was collected.
Holotype: MFLU 20-0537
Saprobic on bark. Thallus unapparent, surface of the substrate where the ascomata are formed whitish gray, pruinose, crustose, epiphloedal. Prothallus absent. Photobiont not detected. Sexual morph: Ascomata apothecial, 345–450 μm diam., black, circular to ellipsoidal, adnate, margin 80–100 μm, slightly erumpent from the thallus, in mature apothecia rolled inward leaving a distinct opening 270–285 μm diam., dark brown, carbonized. Exciple 16–38 μm, distinct, dark brown at the base and both sides, light brown in the upper part, 57–87 μm thick. Hypothecium 11–21 μm thick, distinct, light brown. Hymenium 23–28 μm thick, hyaline. Epihymenium 3–7 μm thick, hyaline. Paraphyses 1–2.4 μm wide, hyaline, densely arranged. Asci 21–24 × 4–6 μm (x = 22.5 × 5 μm, n = 40), hyaline, clavate to obovoid, eight-spored but sometimes four-spored when immature, unitunicate, multiseriate, tip blunted, not narrowing towards the apex, tholus thickened, lacking an apical cap, with poorly developed stipe. Ascospores 4–6 × 0.7–1.0 μm (x = 5 × 0.85 μm, n = 40), hyaline, smooth–walled, fusoid to obovoid, (0–)1-septate. Asexual morph: Undetermined
Spot reactions: Ascomatal gel I-, KI-. Hymenium I-, KI-. Asci I-, KI-. Ascospores I-, KI-
Material examined: China, Yunnan Province, Shangri La, N 27°55′05.8″, E 99°36′33.4″, 3964 m elevation, on unidentified dead bark, 14 September 2018, Vinodhini Thiyagaraja, D6S51 (holotype: MFLU 20-0537)
Notes: Sphaeropezia was resurrected by Baloch et al. [18] and comprises 22 species with S. alpina as the type [34]. Sphaeropezia was originally introduced by Saccardo [76] and associated with Odontotrema with the special adaptation to a foliicolous growth and was assigned to Odontotremataceae due to shared morphological characteristics [18]. However, Sphaeropezia was placed in Stictidaceae based on molecular data and some Bryodiscus species, which had been recorded as parasites on mosses, were also transferred to Sphaeropezia [18].
Species of this genus are characterized by dark-walled, deeply urceolate apothecia, mostly erumpent at maturity, living as saprobes on wood or herbaceous material, or as putative parasites of bryophytes or lichens. They are distributed mainly in northern temperate regions [18]. The new taxon was collected from the sub-tropical region of southwestern of Shangri la, China, which is one of the world’s biodiversity hotspots [77]. Sphaeropezia shangrilaensis clustered together with S. leucocheila and formed a clade with S. capreae with high statistical support in the multi-gene phylogenetic analyses. The new taxon differs from other Sphaeropezia species in the larger pore opening in ascomata and the smaller asci (Figure 6; Table 2).
Specifically, Sphaeropezia shangrilaensis differs from S. capreae in the position of the ascomata (superficial vs. fully erumpent), the larger ascomatal pore opening (273–283 μm vs. (60–)100–150(–200)) μm, the smaller asci (21–24 × 4–5 μm vs. 55–65 × 8–10 μm), the shape of ascospores (bacilliform vs. fusoid to obvoid), and the number of ascospores per asci (4 to 8 vs. polyspored). Sphaeropezia shangrilaensis also differs from S. leucocheila in the shape of the ascomata (roundish vs. globose), the larger pore opening (273–283 μm vs. 80 μm), the smaller asci (21–24 × 4–5 μm vs. 50–55 × 6–8 μm), and the size of the ascospores (4–6 × 0.7–1.0 μm vs. 8–11.5 × 2–3 μm) [78]. Sphaeropezia shangrilaensis is only known from China while S. capreae and S. leucocheila were recorded from Sweden and New Zealand, respectively [18,78].

4. Discussion

Molecular phylogenetic studies show that lichenization occurred several times independently in both Ascomycota and Basidiomycota [4,5,6,7,9,10]. Baloch et al. [19] concluded that independent saprotrophic lineages in Ostropales sensu lato resulted from multiple losses of lichenization. Lutzoni et al. [20] also stated that non-lichenized ostropalean species were derived from a lichenized ancestor. These findings have been confirmed by other recent studies [3,12], whereas others indicated a deeper loss of lichenization in the clade leading to Stictidaceae (Figure 3). The latter was in part also supported by our own analysis using Bayesian MCMC, suggesting multiple independent relichenization in the family, although the results from Bayes traits were ambiguous.
One lichenized genus that we did not include in our analysis of Stictidaceae was Topelia. The genus comprises eleven species, but molecular data are lacking except for the type species. In our multi-gene phylogenetic analyses, T. rosea formed a comparatively long branch, and its position relative to Stictidaceae was unstable. Stictidaceae is not the only family in Ostropales sensu lato showing close relationships of lichenized and saprotrophic lineages. The predominantly lichenized family Graphidaceae now also contains the saprotrophic species Furcaspora eucalypti and Rubikia evansii, apparently derived from a lichenized ancestor [80], and Agyrium in Pertusariales was also derived through delichenization [23]. Stictidaceae itself contains a wide diversity of lifestyles, which may vary not only at genus but also at the species level [32,60,61]. The biology of some taxa (e.g., Lillicoa palicprea and Delpontia) remains unresolved [33].
Apart from lichenized and saprotrophic lineages, the lichenicolous lifestyle appeared multiple times independently within Stictidaceae, as shown previously by Pino-Bodas et al. [81]. Aptroot [82] and Cáceres et al. [80] suggested that delichenization can lead to both lichenicolous and saprotrophic lifestyles, which is supported by our analysis. Aptroot [82] stated that relichenization is a rare case, often resulting in loosely associated lichenized forms. In this respect, optionally lichenized fungi such as Stictis mollis and Schizoxylon albescens are of interest, as they seem to be derived from non-lichenized ancestors. Several species of the saprotrophic genus Acarosporina also have been recorded as parasitic, causing cankers on Quercus and Fagus in eastern North America [33]. Cyanodermella comprises saprotrophic fungi [83], and at least one species, C. asteris, has been recorded as endophytic. Several species of the lichenized genus Absconditella have been recorded as pathogens on bryophytes [84]. Thus, lifestyle switches may drive evolution in Stictidaceae and potentially drive speciation, but this needs to be tested with a much broader sampling, especially of Stictis sensu lato. Lifestyle switches are overall unusually frequent in Ostropales sensu lato, showing the evolutionary plasticity of this enigmatic group [26,85,86,87]. More detailed molecular studies and increased taxon sampling are also needed to resolve generic and species-level limits in the family [31]. Surprisingly, our phylogeny suggests that the only problematic genus at this point is the polyphyletic Stictis sensu lato.

Supplementary Materials

The following are available online at https://www.mdpi.com/2309-608X/7/2/105/s1. Figure S1. Best-scoring RAxML tree reconstructed based on analysis of a single dataset of mtSSU sequence data. Bootstrap support values for ML equal to or greater than 65% is defined above the nodes. Figure S2. Best-scoring RAxML tree reconstructed based on analysis of a single dataset of LSU sequence data. Bootstrap support values for ML equal to or greater than 65% is defined above the nodes. Figure S3. Best-scoring RAxML tree reconstructed based on analysis of a single dataset of ITS sequence data. Bootstrap support values for ML equal to or greater than 65% is defined above the nodes. Figure S4. Best-scoring RAxML tree reconstructed based on analysis of a single dataset of mtSSU sequence data. Bootstrap support values for BP equal to or greater than 0.90 is defined above the nodes. Figure S5. Best-scoring RAxML tree reconstructed based on analysis of a single dataset of LSU sequence data. Bootstrap support values for BP equal to or greater than 0.90 is defined above the nodes. Figure S6. Best-scoring RAxML tree reconstructed based on analysis of a single dataset of ITS sequence data. Bootstrap support values for BP equal to or greater than 0.90 is defined above the nodes.

Author Contributions

Conceptualization, V.T., R.L., D.E. and K.D.H.; methodology, V.T., R.L., D.E., S.C.K., D.N.W., and K.D.H.; resources, K.D.H.; writing—original draft preparation, V.T., R.L. and D.E.; data acquisition, V.T.; writing—review and editing, R.L., D.E., S.C.K., D.N.W., S.L. and K.D.H.; supervision, R.L., D.E. and K.D.H.; funding acquisition, K.D.H. All authors have read and agreed to the published version of the manuscript.

Funding

The research was funded by Thailand Research Fund (“The future of specialist fungi in a changing climate: baseline data for generalist and specialist fungi associated with ants, Rhododendron species and Dracaena species DBG6080013” and “Impact of climate change on fungal diversity and biogeography in the Greater Mekong Sub-region RDG6130001”).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Kevin D. Hyde thanks Chiang Mai University for the Award of Visiting Professor. We thank the Yunnan Provincial Human Resources and Social Security Bureau for a Yunnan Provincial Post-doctoral Grant to Fiona Worthy which financed the collecting expedition. We also thank Udeni Jayalal, Nalin Wijayawardene, and Banujan Kuhaneshwaran for their precious help during this research. S.C. Karunarathna would like to thank CAS President’s International Fellowship Initiative (PIFI) under the following grant: 2018PC0006 and the National Science Foundation of China (NSFC, project code 31750110478). Dhanushka Wanasinghe would like to thank CAS President’s International Fellowship Initiative (PIFI) for funding his postdoctoral research (number 2019PC0008), the National Science Foundation of China and the Chinese Academy of Sciences for financial support under the following grants: 41761144055, 41771063 and Y4ZK111B01. We also would like to thank Shaun Pennycook for helping in nomenclature.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Cartoon tree of major clades for Ostropales sensu lato of combined mtSSU, LSU, and ITS partial sequence data based on RAxML tree analysis.
Figure 1. Cartoon tree of major clades for Ostropales sensu lato of combined mtSSU, LSU, and ITS partial sequence data based on RAxML tree analysis.
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Figure 2. RAxML tree based on analysis of combined mtSSU, LSU, and ITS partial sequence data for Stictidaceae. Bootstrap support values for Maximum Likelihood (ML) equal to or greater than 65%, and Bayesian posterior probabilities (BP) equal to or greater than 0.90 are given as ML/BP above the nodes. The new species and the genus found in this study are displayed in blue bold.
Figure 2. RAxML tree based on analysis of combined mtSSU, LSU, and ITS partial sequence data for Stictidaceae. Bootstrap support values for Maximum Likelihood (ML) equal to or greater than 65%, and Bayesian posterior probabilities (BP) equal to or greater than 0.90 are given as ML/BP above the nodes. The new species and the genus found in this study are displayed in blue bold.
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Figure 3. Ancestral character state analysis of Stictidaceae using Bayesian Binary MCMC and Bayes Traits. Color symbols indicate: green = chlorococcoid, orange = trentepohlioid, gray = non-lichenized saprotrophic, black = lichenicolous.
Figure 3. Ancestral character state analysis of Stictidaceae using Bayesian Binary MCMC and Bayes Traits. Color symbols indicate: green = chlorococcoid, orange = trentepohlioid, gray = non-lichenized saprotrophic, black = lichenicolous.
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Figure 4. Ostropomyces pruinosellus (MFLU 20-0538). (a–c) Ascomata on substrate. (d,e) Vertical section through ascoma (in water). (f) Vertical section through exciple (in water). (g) Vertical section through ascoma (in KI). (h) Paraphyses (in water). (i–l) Asci (in water). (m) Paraphyses (in KI). (n) Asci (in KI). (o) Ascospores (in water). (p) Ascospores (in KI). Scale bars b, c = 1000 µm, d, e, g–n = 100 µm, f = 30 µm, o, p = 50 µm.
Figure 4. Ostropomyces pruinosellus (MFLU 20-0538). (a–c) Ascomata on substrate. (d,e) Vertical section through ascoma (in water). (f) Vertical section through exciple (in water). (g) Vertical section through ascoma (in KI). (h) Paraphyses (in water). (i–l) Asci (in water). (m) Paraphyses (in KI). (n) Asci (in KI). (o) Ascospores (in water). (p) Ascospores (in KI). Scale bars b, c = 1000 µm, d, e, g–n = 100 µm, f = 30 µm, o, p = 50 µm.
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Figure 5. Ostropomyces thailandicus (MFLU 20-0539, holotype). (a–c) Pycnidium on substrate. (d,e) Vertical section through pycnidia (in water). (f), Vertical section through pycnidia (in 5% KOH). (g) Conidiophores (in water). (h) Conidia (in water). (i) Vertical section through pycnidia (in KI). (j) Conidiophores (in KI). Scale bars b, c = 500 µm, d–f, i = 200 µm, g, h, j = 10 µm.
Figure 5. Ostropomyces thailandicus (MFLU 20-0539, holotype). (a–c) Pycnidium on substrate. (d,e) Vertical section through pycnidia (in water). (f), Vertical section through pycnidia (in 5% KOH). (g) Conidiophores (in water). (h) Conidia (in water). (i) Vertical section through pycnidia (in KI). (j) Conidiophores (in KI). Scale bars b, c = 500 µm, d–f, i = 200 µm, g, h, j = 10 µm.
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Figure 6. Sphaeropezia shangrilaensis (MFLU 20-0537). (a–d) Ascomata on substrate. (e,f) Vertical section through an ascoma (in water). (g) Paraphyses (in water). (h–k) Asci (in water). (l,m) Ascospores (in water). (n–r) Asci (in KI). Scale bars a = 1000 µm, b–d = 500 µm, e, f = 200 µm, g–k, n–r = 10 µm, l, m = 5 µm.
Figure 6. Sphaeropezia shangrilaensis (MFLU 20-0537). (a–d) Ascomata on substrate. (e,f) Vertical section through an ascoma (in water). (g) Paraphyses (in water). (h–k) Asci (in water). (l,m) Ascospores (in water). (n–r) Asci (in KI). Scale bars a = 1000 µm, b–d = 500 µm, e, f = 200 µm, g–k, n–r = 10 µm, l, m = 5 µm.
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Table
Table 1. Taxa used in this study for the analyses of combined mitochondrial small subunit spacers (mtSSU), large subunit nuclear rDNA (LSU), and internal transcribed spacers (ITS) sequence data and their GenBank accession numbers. The newly generated sequences are indicated in boldface.
Table 1. Taxa used in this study for the analyses of combined mitochondrial small subunit spacers (mtSSU), large subunit nuclear rDNA (LSU), and internal transcribed spacers (ITS) sequence data and their GenBank accession numbers. The newly generated sequences are indicated in boldface.
GenBank Accession Numbers
SpeciesStrainsmtSSULSUITS
Absconditella sphagnorum 1T. Laukka 52 (TUR)EU940247EU940095–
Absconditella sphagnorum 217 Feb 02 Palice (HB Palice)AY300872AY300824–
Acarosporina microsporaAFTOL-ID 78AY584612AY584643DQ782834
Carestiella socia 1GG2410AY661677AY661687AY661687
Carestiella socia 2GG2437aAY661678AY661682AY661682
Cryptodiscus cladoniicola 1RP160KY661675KY661653KY661620
Cryptodiscus cladoniicola 2RP159KY661674KY661652KY661619
Cryptodiscus epicladoniaRP208KY661680–KY661628
Cryptodiscus foveolaris 1EB155FJ904695–FJ904673
Cryptodiscus foveolaris 2EB86FJ904692–FJ904670
Cryptodiscus foveolaris 3EB147FJ904694–FJ904672
Cryptodiscus galaninaeRP314––KY661636
Cryptodiscus gloeocapsaEB93FJ904696–FJ904674
Cryptodiscus incolorEB164FJ904697–FJ904675
Cryptodiscus muriformis 1UPS F-647154MG281972MG281962MG281962
Cryptodiscus muriformis 2H.B. 6773MG281973MG281963MG281963
Cryptodiscus pallidus 1EB60FJ904700FJ904678FJ904678
Cryptodiscus pallidus 2EB173FJ904702FJ904680FJ904680
Cryptodiscus pini 1EB82FJ904704FJ904682FJ904682
Cryptodiscus pini 2EB178FJ904705FJ904683FJ904683
Cryptodiscus pini 3EB181FJ904706FJ904684FJ904684
Cryptodiscus tabularum 1CO205FJ904712FJ904690FJ904690
Cryptodiscus tabularum 2EB169FJ904711FJ904689FJ904689
Cryptodiscus tabularum 3EB77FJ904709FJ904687FJ904687
Cyanodermella asteris03HOR06-2-4–KT758843KT758843
Cyanodermella banksiaeCPC:32105–NG_064548NR_159835
Cyanodermella oleoligniDTO 301-G1KX999144KX950461KX950434
Cyanodermella viridulaEB146–MG281964MG281964
Diploschistes scruposusSFB 95KC167052–KC167001
Eriospora leucostoma 1CPC:35594–MT223890MT223795
Eriospora leucostoma 2CPC:35598–MT223891MT223796
Fitzroyomyces cyperacearum 1CPC:32209–NG_058513NR_156387
Fitzroyomyces cyperacearum 2MFLU 18-0695b–MK499361MK499349
Fitzroyomyces cyperacearum 3MFLU 18-0695a–MK499363–
Geisleria sychnogonoides 1Caceres & Aptroot 13560 (ABL)KC689751KC689752–
Geisleria sychnogonoides 2GESY7510KF220306KF220304–
Geisleria sychnogonoides 3GESY7509KF220305––
Glomerobolus gelineus 1AFTOL-ID 1349DQ247784DQ247803DQ247782
Glomerobolus gelineus 2JK 5584CDQ247783DQ247798–
Hormodochis aggregata 1CBS:145904––NR_166307
Hormodochis aggregate 2CPC:37499–MN317288MN313807
Hormodochis aggregata 3CPC:35475–MN317287MN313806
Ingvariella bispora 1DUKE 1444446HQ659175––
Ingvariella bispora 2MALich 15288HQ659173HQ659184–
Ingvariella bispora 3BCNLich 17183HQ659174HQ659185–
Myriotrema olivaceumKalb 39107KJ435181KJ435111–
Neofitzroyomyces neriiCBS:145088–MK047504MK047454
Neostictis nigricansMFLU 18-1380–MT214610MT310654
Ostropa barbara 1S F302817MG281974MG281965MG281965
Ostropa barbara 2EB85HM244752HM244773HM244773
Ostropa barbara 3G. M. 2015-04-28.1–KY608095KY608095
Ostropomyces pruinosellusMFLU 20-0538MW400963MW400966MW400964
Ostropomyces thailandicusMFLU 20-0539–MW397060MW400967
Phacidiella eucalyptiCBS 120255–MT373344MT373361
Phacidiella podocarpiCBS 138904–NG_058118NR_137934
Phaeographis spondaicaLumbsch 19633JX421280––
Porina nuculaLücking 17007-cKJ449310––
Robergea cubicularis 1G.M. 2013-05-09.1–KY611899KY611899
Robergea cubicularis 2G.M. 2017-10-12.1–MN833317MN833317
Schizoxylon albescens 1GG236AY661680AY661689AY661689
Schizoxylon albescens 2GG2696aDQ401142DQ401144DQ401144
Schizoxylon albescens 3Wedin 8365 (S)––HQ287353
Schizoxylon albescens 4Wedin 8364 (S)––HQ287352
Schizoxylon albescens 5Wedin 8356 b (S)––HQ287350
Schizoxylon albescens 6Wedin 8359 (S)––HQ287351
Schizoxylon albescens 7Wedin 8327 (S)––HQ287349
Schizoxylon albescens 8Wedin 8324 (S)––HQ287348
Schizoxylon albescens 9Wedin 8254 (S)––HQ287347
Schizoxylon berkeleyanumF209682MG281975MG281966MG281966
Schizoxylon gilenstamii 1MW9490MG281977MG281968MG281968
Schizoxylon gilenstamii 2MW9496MG281978MG281969MG281969
Sphaeropezia arctoalpinaBaloch SW057HM244736HM244760–
Sphaeropezia capreae 1GG2560AY661674AY661684–
Sphaeropezia capreae 2UPS (Gilenstam 2633a)HM244751HM244772–
Sphaeropezia cassiopesBaloch s.n. (S)HM244746––
Sphaeropezia diffindensBaloch SW020 (S)HM244747––
Sphaeropezia leucocheilaPDD 98299MK547101MK547099MK547090
Sphaeropezia lyckselensis 1Gilenstam 2651 (S)JX266156JX266158–
Sphaeropezia lyckselensis 2Gilenstam 2659HM244750HM244771–
Sphaeropezia mycoblastiWedin 8509 & Westberg (S)JX266157JX266159–
Sphaeropezia ochrolechiaeWedin 6729 (UPS)–JX266160–
Sphaeropezia shangrilaensisMFLU 20-0537MW400962MW400965MW400955
Stictis brunnescens 1EB84MG281979––
Stictis brunnescens 2Gilenstam 2359 (UPS)AY661679–AY661688
Stictis brunnescens 3SFB1100MG281981–MG281970
Stictis brunnescens 4MW8571MG281980––
Stictis brunnescens 5SFB1105MG281982–MG281971
Stictis confusa 1Wedin 7070 (UPS)DQ401141–DQ401143
Stictis confusa 2AN3222AY527365–AY527336
Stictis mollis 1GG2440bAY527342–AY527313
Stictis mollis 2GG2445aAY527347–AY527318
Stictis mollis 3GG2370AY527339–AY527310
Stictis mollis 4GG2458bAY527345–AY527316
Stictis populorum 1GG2618AY527360–AY527331
Stictis populorum 2GG2610aAY527356–AY527327
Stictis populorum 3MW7301AY527363–AY527334
Stictis radiata 1MW6493AY527338–AY527309
Stictis radiata 2GG2449aAY340532–AY527308
Stictis radiata 3AFTOL-ID 398AY584727–DQ782846
Stictis urceolata 1MFLU 19–2695–MN989186–
Stictis urceolata 2LT21500AY661676AY661686AY661686
Stictis urceolata 3AFTOL-ID 96––HQ650601
Trichothelium epiphyllumBaloch CR-127AY648901––
Trinathotrema stictideum 1F:Luecking 17541bGU380288––
Trinathotrema stictideum 2F:Luecking 28093GU380287––
Wirthiotrema glaucopallensDNA1336JF828972––
Xyloschistes platytropaH:Bjork 05-242KJ766517KJ766680–
Table
Table 2. Synopsis of recorded Sphaeropezia species.
Table 2. Synopsis of recorded Sphaeropezia species.
Species NamePosition of AscomaShape of AscomaSize of Ascoma (μm)Size of Ascoma Pore Opening (μm)Size of Asci (μm)Spore Size (μm)Ascospore ShapeNumber of SeptateKnown DistributionReference
Sphaeropezia santessoniiImmersed, partly erumpent, finally sessile-(225–) 280–380 (–440) (20–) 55–125 (–190) 40–50 (–55) × 8–13 (12·5–) 15·4–20·4 (–23·5) × (3–) 3·6–4·6(–5) Fusiform, often asymmetricaltrans-septate (3–) 6–8
(–9) to submuriform		Russian Arctic, Iceland and Peru, widespread and common in Arctic regions[79]
S. bryoriaeSuperficial Roundish to subspherical(275–) 310–410 (–440)(0–) 10–70 (–120)40–60 × 5–6 (7·4–) 7·6–8·8
(–9·2) × (2·8–)3·
1–3·5(–4·0) 		Ellipsoid1-septate (exceptionally 2-septate)USA (Washington)[79]
S. capreaeFully erumpent - (280–) 350–450 (60–) 100–150 (–200)55–65 × 8–10 (4–)5–7(–8) ×
1–1.3(–1.5) 		Bacilliform -Sweden[18]
S. leucocheilaSuperficialGlobose-urceolate Up to 30080 50–55 × 6–8 8–11.5 × 2–3 Oblong-elliptic(0–) 1-septateNew Zealand[78]
S. lyckselensisErumpent-(175–) 250–350 (–425)(25–) 40–75 (–125) 35–60 × 5–6.5 -Cylindrical oblong3-septateNorthern Sweden[18]
S. melaneliaeImmersedRoundish170–3500–2060–85 × 6·5–8·5 (12–)12·8–14·4
(–15·5) × (5·4–) 5·5–6·1 (–6·3) 		Ellipsoid(1–)3-septate, exceptionally with one longitudinal septumSweden and Alaska[79]
S. mycoblastiErumpent-(140–) 190–280 (–320) (0–) 20–50 (–70)50–70 × 7–9 (12.3–) 14.0–15.9 (–17) × (4.0–) 4.7–5.3 (–5.7)Ellipsoid to narrowly ellipsoid3-septate, (exceptionally 4-septate)USA (Oregon) and northern Sweden[18,70]
S. ochrolechiaeImmersed and become erumpent-(180–) 230–330 (–400) (0–) 5–50 (–150)50–75 × 9–14 (10·8–) 12·1–14·4 (–16·0) × (4·3–) 4·8–5·5 (–6) Ellipsoid to narrowly ellipsoid3-septateNorway, Sweden and the USA (Alaska)[79]
S. pertusariaeImmersed to erumpent-(140–) 170–260 (–310)(20–) 40–110 (–150) -(11·5–)12·5–15·4 (–16·0) × (4·5–) 4·7
–5·5 (–6·0) 		Ellipsoid1–3-septateGreat Britain (Scotland) [79]
S. rhizocarpicolaImmersed and occasionally erumpentRoundish(140–) 155–245 (–300)(30–) 30–60 (–70) 50–70 × 6·5–13 (8·0–)9·3–11·1 (–13·5) × (4·5–) 4·8–5·6(–6·5) -(1–)3-septateRussia, Kola and Peninsula[79]
S. santessoniiImmersed, -finally sessile partly erumpent -(225–) 280–380 (–440) (20–) 55–125 (–190) 40–50 (–55) × 8–13 (12·5–)15·4–20·4 (–23·5) × (3–) 3·
6–4·6 (–5) 		Fusiform, often asymmetricalTrans-septate (3–)
6–8
(–9) to submuriform		Widespread and common in Arctic regions[79]
S. sipeiImmersed, soon erumpentSub-spherical(350–) 360–480 (–590)(0–) 0–40 (–105) 55–65 × 5–7 (11·0–)12·2–13·8 (–14·5) × (4·2–) 4·5–5·0 (–5·0) Ellipsoid to narrowly ellipsoid3-septateUSA (Oregon) and Canada (British Columbia)[79]
S. thamnoliaeImmersed and occasionally sessileRoundish or slightly ellipsoid(140–) 150–200 (–290)(0–) 20–60 (–85) 30–45 × 7–10(9·0–)11·0–14·9
(–18·0) × (2·5–) 2·5–3·2 (–3·5) 		Fusiform1(–2)-septateRussian and Swedish Arctic[79]
S. shangrilaensisSlightly erumpent to superficial Roundish345–446273–283 21–24 × 4–5.54–6 × 0.7–1.0 Fusoid to obvoid(0–) 1-septateChinaThis study
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Thiyagaraja, V.; Lücking, R.; Ertz, D.; Karunarathna, S.C.; Wanasinghe, D.N.; Lumyong, S.; Hyde, K.D. The Evolution of Life Modes in Stictidaceae, with Three Novel Taxa. J. Fungi 2021, 7, 105. https://doi.org/10.3390/jof7020105

AMA Style

Thiyagaraja V, Lücking R, Ertz D, Karunarathna SC, Wanasinghe DN, Lumyong S, Hyde KD. The Evolution of Life Modes in Stictidaceae, with Three Novel Taxa. Journal of Fungi. 2021; 7(2):105. https://doi.org/10.3390/jof7020105

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Thiyagaraja, Vinodhini, Robert Lücking, Damien Ertz, Samantha C. Karunarathna, Dhanushka N. Wanasinghe, Saisamorn Lumyong, and Kevin D. Hyde. 2021. "The Evolution of Life Modes in Stictidaceae, with Three Novel Taxa" Journal of Fungi 7, no. 2: 105. https://doi.org/10.3390/jof7020105

APA Style

Thiyagaraja, V., Lücking, R., Ertz, D., Karunarathna, S. C., Wanasinghe, D. N., Lumyong, S., & Hyde, K. D. (2021). The Evolution of Life Modes in Stictidaceae, with Three Novel Taxa. Journal of Fungi, 7(2), 105. https://doi.org/10.3390/jof7020105

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