Taxonomy
Based on the above phylogenetic and phenotypic results, the treated species previously described in Arachniotus, Hormiscium and Sphaerosporium are proposed to be reclassified in Sporendonema, since this genus has historical nomenclatural priority. Differences in micromorphology of Sporendonema species are provided in Table 3.
Sporendonema Desm. – Annls Sci. Nat., Sér. 1 11: 246 (1827).
= Coprotrichum Bonord. - Handb. Allgem. Mykol. (Stuttgart): 76 (1851).
Type species Sporendonema casei Desm.
Sporendonema aurantiacum (Kamyschko) Kandemir & de Hoog, comb. nov. Figure 3C and D
MycoBank number: MB842801
≡ Pseudoarachniotus aurantiacus Kamyschko – Nov. Sist. Niz. Rast. 4: 224 (1967) ≡ Arachniotus aurantiacus (Kamyschko) v. Arx - Persoonia 6(3): 373 (1971).
Culture 4 − 1/2 (holotype), preserved Institute of Antibiotics, Saint-Petersburg (Leningrad), from semi-desert (slightly loam) soil, Republic of Kalmykia, Russia (Kamyschko 1967). Ex-holotype culture CBS 603.67 (= BKM F-1140 = ATCC 22394 = NRRL A-18287 = VKM F-1140 = UAMH 3529).
Notes Sporendonema aurantiacum has golden-yellow, orange-brown ascomata which contains globose asci. Ascospores are orange-yellow, globose, smooth, and discoid from the side view; without a prominent equatorial rim, golden-yellowish when mature, 4–5.5 µm in diameter and 2.5‒3.5 µm wide. A detailed description has been provided by von Arx (1971).
Sporendonema casei Desm. – Annls Sci. Nat., Sér. 1, 11: 246 (1827). Figure 4
≡Torula sporendonema Berk. & Broome – Ann. Mag. Nat. Hist., Ser. 2, 5: 460 (1850).
Holotype material is not known to be preserved. Lectotype (designated here, MBT XXX), drawings in Desmazières (1827) Plate 21A, Fig. 1. Epitype (designated here, MBT XXX): CBS 543.75, isolated from cheese, by Sochal, 1975, preserved in metabolically inactive state.
Notes Sporendonema casei is a well-known cheese-inhabiting fungus that produces orange-red spots on cheese. This slow-growing and xerotolerant fungus produces cubical conidia with rounded corners from club-shaped hyphae by enteroarthric conidiogenesis. A detailed description of S. casei has been provided by Sigler & Carmichael (1976).
Sporendonema confluens (Sartory & Bainier) Kandemir & de Hoog, comb. nov. Figure 3M
MycoBank number: MB842802
≡ Gymnoascus confluens Sartory & Bainier – Bull. Soc. Mycol. Fr. 29: 261 (1913) ≡ Arachniotus confluens (Sartory & Bainier) Apinis – Mycol. Pap. 96: 37 (1964) ≡ Gymnascella confluens (Sartory & Bainier) Currah – Mycotaxon 24: 75 (1985).
Ex-type culture
BDUN 375 from dung, UK (Apinis 1964). Alternative collection numbers ATCC 22220, CBS 352.66, IMI 100873, NRRL 5979, Orr O-3559 and UAMH 3565.
Notes The morphology of S. confluens is similar to that of S. aurantiacum with its globose,smooth ascospores. However, the latter has darker ascospores and discoid shape from the side view. Detailed description has been provided by Currah (1985) and Apinis (1964).
Sporendonema equinum (Desm.) Kandemir, Decock & de Hoog, comb. nov. Figure 5
MycoBank number: MB842804
≡ Torula equina Desm. – Annls Sci. Nat., Bot., Sér. 4, 4: 126 (1855) ≡ Oospora equina (Desm.) Sacc. & Voglino – Syll. Fung. (Abellini) 4: 22 (1886) ≡ Sphaerosporium equinum (Desm.) Crane & Schokn. – Mycologia 78(1): 86 (1986).
Holotype of Torula equina #H.G. 1510 (PC!), from old and humid horse hoofs, France (Crane & Schoknecht 1986).
Notes The genus Sphaerosporium was introduced with type species Sph. lignatile by Lewis Dawid von Schweinitz (1834) based on morphology of the fungus on dead wood in the USA. Holotype (PH) for Sph. lignatile was designated as #3036. Later, Sph. equinum, originally described as Torula equina, was added to the genus (Crane & Schoknecht 1986). Partridge & Morgan-Jones (2002) reviewed Sphaerosporium and provided generic descriptions for both Sph. lignatile and Sph. equinum. Authors noted that despite their substrate differences, these two taxa share morphological similarities suggesting a close relationship (Partridge & Morgan-Jones 2002).
However, molecular analyses do not support any relationship between Sph. lignatile and S. equinum strains (Song et al. 2019). In the current study, micromorphology of the type specimen of Torula equina ILLS 45141 was examined. Hyphae were not found but conidia as arranged in basipetal chains were abundant (Fig. 5H). Conidia were globose, with thick, smooth walls.
Additionally, we examined MUCL 46080, isolated from the rind of a sheep cheese in France, as a reference strain to evaluate morphological characteristics and physiology of Sph. equinum. Since we were not able to obtain a pure culture from the type specimen, we could not compare the type and the cheese isolates phylogenetically. Nevertheless, we propose a new name combination for the cheese isolates of the Sph. equinum since they are classified within Sporendonema, Onygenales, Eurotiomycetidae (Kandemir et al. 2022), while Sph. lignatile, type species of the genus, is classified in Pezizales, Pezizomycetidae (Song et al. 2019).
Strains UAMH 11516 (= MUCL 8097), from the skin of bat wings, and MUCL 5024, from insect pupa, were found to be phylogenetically related to the cheese isolates of Sph. equinum (Fig. 2). However, the growth rate on PDA, OA, OA/PS and MEA, the conidial shape and size, and caseinase activity were found to be different in the two groups. Therefore, a new species was described to accommodate MUCL 54024 and MUCL 58097, as follows:
Sporendonema isthmoides Decock, Kandemir, Hern.-Rest. & de Hoog, sp. nov. Figure 6
MycoBank number: MB842809
Etymology In Greek “isthmus” means “neck”, “isthmoides” being used for “resembling isthmus”, referring to the narrow conjunction between conidia in chains.
Teleomorph not observed. Vegetative hyphae hyaline, septate, smooth, 2.5–4.5 µm wide; fertile hyphae mostly smooth and some ornamented with warts (Fig. 6); conidiogenesis thallic-enteroarthric; conidia hyaline to pale yellow, yellow-orange in mass, 1-celled, lemon-shaped in chains and becoming globose when separated, truncated at one or both ends, smooth- and thick-walled, occasionally with warts; 6–8.5 × 3.5–5 µm, unequal, occasionally catenate with short chains. Colonies on PDA reaching 40 mm diam after 21 d at 24°C; flat, elevated in the center; margin regular; obverse color orange, dirty white-beige at the periphery (Fig. 6A); reverse dark brown at the center and orange-yellow at the periphery (Fig. 6B). Colonies on YpSs agar reaching 38 mm diameter after 21 d at 24°C, flat, slightly elevated at the margin, texture velvety, obverse color orange with cream-white edges (Fig. 6C, 6D); reverse orange with a cream-colored periphery (Fig. 6E). Growth temperatures: minimum 4°C and maximum 27°C. Casein not hydrolysed. Growth present at NaCl 3, 10 and 17 but not 25% (w/w).
Material examined Canada, New Brunswick, Berryton Cave, swab sample from skin of living female little brown bat (Myotis lucifugus), 2010, K. J. Vanderwolf. Dried culture UAMH 11516 (holotype), preserved in a metabolically inactive state. Alternative collection number MUCL 58097; GenBank numbers ITS: OM468607, LSU: OM515118. Additional specimen Belgium, insect pupa in the attic of a house, 2012, C. Decock, MUCL 54024. Genbank numbers ITS: OK255531, LSU: OK255535.
Notes Based on ITS and LSU locus analyses, the phylogenetically closest species to S. isthmoides is S. equinum. Conidia of S. isthmoides are with remnants of the hyphal wall as observed under the light microscope, conidia being solitary or catenulate, with one then proximal, or both truncate ends, with narrow conjunction sites between conidia in short chains (Fig. 6), smooth-walled or with some warts. The species does not have caseinase activity. Sporendonema isthmoides and S. equinum differ morphologically in conidiogenesis (thallic-enteroarthric vs holoblastic; Figs. 5 and 6), shape of conidia in chains (lemon-shaped vs. globose) and size (9.5 × 13 µm vs. 4.0 × 7.5 µm). The conidia and hyphae of S. equinum are smooth-walled, whereas some conidia and hyphae of S. isthmoides are warted. Physiologically, S. isthmoides grows faster than S. equinum on almost all tested media (PDA, OA, MEA supplemented with 3% and 10% NaCl at 24°C; Table 2), can grow on OA/PS medium and lacks caseinase activity. Differences in micromorphology of S. casei, S. equinum and S. isthmoides are illustrated in Fig. 7.
Sporendonema rubrum (Tiegh.) Kandemir & de Hoog, comb. nov. Figures 3A and 3B
MycoBank number: MB842803
≡ Gymnoascus ruber Tiegh. – Bull. Soc. Bot. Fr. 24: 159 (1877) ≡ Arachniotus ruber (Tiegh.) Schröt. – Krypt. -Fl. Schlesien (Breslau) 3.2(1–2): 210 (1893) [1908]. Neotype IMI 92796 from soil, UK (Kuehn & Orr 1964). Alternative collection numbers CBS 352.90 and ATCC 15315.
Notes Arachniotus ruber was described from coyote dung as type species of the genus Arachniotus and was outstanding with its low temperature (5°C) requirement for isolation (Currah 1985). It has hyaline asci, orange-yellow and smooth ascospores with two equatorial lines (Fig. 3N and O). A detailed description of the fungus is given by Kuehn & Orr (1964).