Metulocladosporiella

Crous, et al., Mycol. Res. 110: 269. 2006. Fig. 30.

Fig. 30. Metulocladosporiella spp. A. Disease symptoms on Musa sp (indicated by the arrows). B–K. Asexual morph. B–D. Macronematous conidiophores. B. Metulocladosporiella musicola (CBS 121396). C. Metulocladosporiella musicola (ex-type CBS 110960). D. Metulocladosporiella musae (CPC 33937). E–G. Conidiogenous apparatus. E, F. Metulocladosporiella musae (CPC 33937). G. Metulocladosporiella musicola (ex-type CBS 110960). H. Lobed bases of macronematous conidiophore of Metulocladosporiella musae (CPC 33937). I–K. Micronematous conidiophores. I, J. Metulocladosporiella musae (CPC 33937). K. Metulocladosporiella musicola (CBS 121396). Scale bars = 10 μm.

Classification: Eurotiomycetes, Chaetothyriomycetidae, Chaetothyriales, Herpotrichiellaceae.

Type species: Metulocladosporiella musae (E.W. Mason) Crous, et al., basionym: Cladosporium musae E.W. Mason. Lectotype designated by Crous et al. (2006a): IMI 7521 (slide). Epitype and ex-epitype strain designated by Crous et al. (2006a): CBS H-14788, CBS 161.74 = ATCC 36973.

DNA barcodes (genus): LSU, ITS.

DNA barcodes (species): ITS, tef1. Table 10. Fig. 31.

Table 10. DNA barcodes of accepted Metulocladosporiella spp.

Species Isolates1 GenBank accession numbers2 References
ITS cal tef1
Metulocladosporiella chiangmaiensis CBS 143918T MG934443 MG934522 MG934476 Present study
M. malaysiana CBS 143919T MG934444 MG934523 MG934477 Present study
M. musae CBS 161.74ET DQ008137 MG934478 Crous et al. (2006a), present study
CBS 113863 DQ008138 MG934524 MG934479 Crous et al. (2006a), present study
CPC 33937 MG934445 MG934525 MG934480 Present study
M. musicola CBS 110960T DQ008127 MG934526 MG934481 Crous et al. (2006a), present study
CBS 110962 MG934446 MG934527 MG934482 Crous et al. (2006a), present study
CBS 110964 MG934447 MG934528 MG934483 Crous et al. (2006a), present study
CBS 113860 DQ008130 MG934529 MG934484 Crous et al. (2006a), present study
CBS 113861 DQ008131 MG934530 MG934485 Crous et al. (2006a), present study
CBS 113862 DQ008132 MG934531 MG934486 Crous et al. (2006a), present study
CBS 113864 DQ008133 MG934532 MG934487 Crous et al. (2006a), present study
CBS 113865 DQ008134 MG934533 MG934488 Crous et al. (2006a), present study
CBS 113873 DQ008135 MG934534 MG934489 Crous et al. (2006a), present study
CPC 18124 MG934448 MG934535 MG934490 Present study
CPC 32807 MG934449 MG934536 MG934491 Present study
CPC 32849 MG934450 MG934537 MG934492 Present study
CPC 32970 MG934451 MG934538 MG934493 Present study
M. musigena CBS 143920T MG934452 MG934539 MG934494 Present study
M. samutensis CBS 143921T MG934453 MG934540 MG934495 Present study
1

CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; CPC: Culture collection of Pedro Crous, housed at the Westerdijk Fungal Biodiversity Institute. T and ET indicate ex-type and ex-epitype strains.

2

ITS: internal transcribed spacers and intervening 5.8S nrDNA; cal: partial calmodulin gene; tef1: partial translation elongation factor 1-alpha gene.

Fig. 31. RAxML phylogram obtained from the combined ITS (667 bp), cal (524 bp) and tef1 (454 bp) sequence alignment of taxa belonging to Metulocladosporiella. The tree was rooted to Cladosporium tenuissimum CBS 125995ET. The novelties proposed in this study are indicated in bold. RAxML bootstrap support (BS) values above 70 % and Bayesian posterior probability scores above 0.95 are shown at the nodes. GenBank accession numbers are indicated in Table 10. T and ET indicate ex-type and ex-epitype strains, respectively. TreeBASE: S21899.

Mycelium internal and external on substrate, hyphae branched, septate, hyaline, subhyaline to pale olivaceous, thin-walled. Stromata lacking. Conidiophores macronematous, mononematous, occasionally with intermixed micronematous conidiophores, solitary or in loose groups, arising from hyphae, erect, with a long, subcylindrical, simple stipe and a branched terminal part; stipe septate, medium to brown, smooth or almost so, usually swollen at base; branched part loose to dense, metuloid, of short to long branchlets and ramoconidia, tips paler than stipes, subhyaline to pale olivaceous. Conidiogenous cells integrated, terminal, occasionally intercalary, polyblastic, sympodial; conidiogenous loci (conidial scars) subconspicuous to conspicuous, subdenticulate, truncate, unthickened to slightly thickened, and somewhat darkened-refractive. Conidia and ramoconidia in simple and branched chains, ellipsoid, ovoid, subcylindrical, or fusiform, 0–1-septate, subhyaline to pale olivaceous, thin-walled, smooth; hila truncate, unthickened to slightly thickened or slightly darkened-refractive; secession schizolytic. Sexual morph unknown (adapted from Crous et al. 2006a).

Culture characteristics: Colonies on PDA and OA under near-ultraviolet light with smooth, regular margins and sparse to moderate aerial mycelium. On PDA surface pale mouse grey to mouse grey or dirty white-grey, greyish sepia, smoke grey to grey olivaceous, or olivaceous; reverse greenish black, cinnamon to isabelline with centre fuscous black, or grey olivaceous to dark grey olivaceous or olivaceous black.

Optimal media and cultivation conditions: SNA under near-ultraviolet light at 25 °C to induce sporulation.

Distribution: Africa, America, Asia and Oceania.

Hosts: Musa spp. (Musaceae).

Disease symptoms: Leaf spots; Cladosporium speckle disease of banana.

Notes: Metulocladosporiella was introduced by Crous et al. (2006a) to accommodate two cladosporium-like species causing speckle disease on banana. Metulocladosporiella can be distinguished from Cladosporium and allied genera by the presence of apically branched, brown conidiophores with paler tips and chains of pale, smooth, often subhyaline conidia.

 The phylogenetic analysis based on the ITS and LSU sequences demonstrated that Metulocladosporiella belongs in Chaetothyriales. Morphologically, the conidiogenous loci and conidial hila resemble those of Cladophialophora, which is another member of this order. However, Cladophialophora produces unbranched, micro- to semimacronematous conidiophores, and concolourous conidia. Moreover, Cladophialophora includes human pathogenic species (Crous et al. 2006a). In the present study, the recommended barcodes for species delimitation are ITS and tef1.

 Hitherto, all species described in Metulocladosporiella are pathogens of banana and occur in countries where this crop is cultivated (Jones, 2000, Crous et al., 2006a).

Reference: Crous et al. 2006a (morphology and phylogeny).


Metulocladosporiella chiangmaiensis

Y. Marín, Cheew. & Crous, sp. nov. MycoBank MB824031. Fig. 32.

Fig. 32. Metulocladosporiella chiangmaiensis (ex-type CBS 143918). A. Colony on PDA. B. Colony on OA. C–E. Macronematous conidiophores. F. Conidiogenous apparatus. G. Lobed bases of macronematous conidiophore. H–K. Micronematous conidiophores. Scale bars: C = 50 μm; D = 20 μm; others = 10 μm.

Etymology: Name from Chiang Mai, the province in Thailand where this fungus was collected.

Mycelium internal and external, superficial; hyphae 1.5–3.5 μm wide, branched, septate, occasionally slightly constricted at septa, with small swellings, hyaline, subhyaline to pale olivaceous, thin-walled, smooth, hyphae occasionally aggregated, forming ropes; with numerous intermixed micronematous conidiophores, erect from vegetative mycelium, intercalary, straight to flexuous, unbranched, subhyaline, usually with simple terminal conidial chains. Macronematous conidiophores 85–1050 μm long, arising from superficial hyphae, erect, solitary to loosely aggregated, composed of a subcylindrical stipe, 5.5–9.5(–10.5) μm wide, 3–18 septate, swollen or lobed at base, 8–17(–18.5) μm diam, with short, rhizoid, subhyaline to pale brown hyphae growing from base, medium to brown in lower half, paler towards apex, tips pale brown or even subhyaline, thick-walled below, thin-walled towards apex, smooth; apex persistently branched, branched part composed of usually fairly compact, closely arranged subcylindrical branchlets; primary branches (13–)17–45(–55) × 3–5.5 μm, 0(–1)-septate, giving rise to 1–3 secondary branches, or to conidiogenous cells; secondary branches 13–28 × 2.5–5(–5.5) μm, 0(–1)-septate, giving rise to 1–2(–3) conidiogenous cells; conidiogenous cells 9–17 × 3–5 μm, subcylindrical, terminal or occasionally intercalary, sympodial, polyblastic, conidiogenous loci 1–1.5(–2) μm wide, subconspicuous to conspicuous, subdenticulate, somewhat protuberant, truncate, wall unthickened to somewhat so, darkened-refractive. Conidia 5.5–10(–12.5) × 2.5–4 μm, in simple and branched acropetal chains, ellipsoid-ovoid, fusoid, subcylindrical, aseptate, subhyaline to pale brown, thin-walled, smooth, with 1–3(–4) hila, 1–1.5 μm diam, up to 2 μm diam at base of ramoconidia, truncate, unthickened or almost so, and somewhat darkened-refractive, secession schizolytic; ramoconidia 7–15(–17) × 3–4.5 μm.

Culture characteristics: Colonies on PDA reaching 25–28 mm diam after 2 wk at 25 °C, moderate aerial mycelium, velvety, umbonate; surface greyish sepia, halo surrounding centre vinaceous buff, and margins hazel; reverse cinnamon to isabelline, centre fuscous black. Colonies on OA reaching 32–35 mm diam after 2 wk at 25 °C, sparse aerial mycelium, flat except margins due to aerial mycelium; surface hazel, centre brown vinaceous, margins smoke grey; reverse livid vinaceous, centre brown vinaceous, margins pale brown vinaceous.

Material examined: Thailand, Chiang Mai Province, Mae Klang Luang, N 18° 32.465', E 98° 32.874', from leaves of Musa sp. (Musaceae), 6 Oct. 2008, P.W. Crous & R. Cheewangkoon (holotype CBS H-23393, culture ex-type CBS 143918= CPC 18646).

Notes: Metulocladosporiella chiangmaiensis is related to M. musigena. Both species are known from Thailand, and produce more micronematous conidiophores than any other species in the genus. However, M. chiangmaiensis produces longer macronematous conidiophores and shorter conidia than M. musigena, which produces conidiogenous cells directly from the apex of its macronematous conidiophores, which is not the case in M. chiangmaiensis.


Metulocladosporiella malaysiana

Y. Marín & Crous, sp. nov. MycoBank MB824032. Fig. 33.

Fig. 33. Metulocladosporiella malaysiana (ex-type CBS 143919). A. Colony on PDA. B. Colony on OA. C–F. Macronematous conidiophores. G. Conidiogenous apparatus. H. Lobed bases of macronematous conidiophore. I, J. Micronematous conidiophores. Scale bars: C, D = 20 μm; others = 10 μm.

Etymology: Name refers to Malaysia, the country from where it was isolated.

Mycelium internal and external, superficial; hyphae 1–3.5 μm wide, branched, septate, occasionally constricted at septa, with swellings, hyaline, subhyaline to pale brown, thin-walled, smooth, hyphae occasionally aggregated, forming ropes; occasionally with intermixed micronematous conidiophores, erect from vegetative mycelium, intercalary, straight to flexuous, unbranched, subhyaline, usually with simple terminal conidial chains. Macronematous conidiophores 57–565 μm long, arising from superficial hyphae, erect, solitary to loosely aggregated, composed of a subcylindrical stipe, 5–8 μm wide, (1–)2–11-septate, swollen or lobed at base, 7–15 μm diam, with short, rhizoid, subhyaline to pale brown hyphae growing from base, medium to brown in lower half, paler towards apex, tips pale brown or even subhyaline, thick-walled below, thin-walled towards apex, smooth; apex persistently branched, composed of fairly compact, closely arranged subcylindrical branchlets; primary branches (12–)16–44(–60) × 3.5–5.5 μm, 0–1(–2)-septate, giving rise to 1–2(–3) secondary branches, or to conidiogenous cells; secondary branches 11.5–26.5(–39) × 3–4.5 μm, 0(–1)-septate, giving rise to 1–2(–3) conidiogenous cells; conidiogenous cells 10–23 × 2.5–4.5 μm, subcylindrical, terminal or occasionally intercalary, sympodial, polyblastic, conidiogenous loci 1–2 μm wide, subconspicuous to conspicuous, subdenticulate, somewhat protuberant, truncate, wall not to slightly thickened, darkened-refractive. Conidia 5.5–13.5(–14.5) × (2.5–)3–4.5(–5) μm, in simple and branched acropetal chains, ellipsoid-ovoid, fusoid, subcylindrical, aseptate, subhyaline to pale brown, thin-walled, smooth, with 1–3 hila, 0.8–1.4 μm diam, up to 2 μm diam at base of ramoconidia, truncate, not to slightly thickened, and somewhat darkened-refractive, secession schizolytic; ramoconidia 7–13(–14) × 3–4.5(–5) μm.

Culture characteristics: Colonies on PDA reaching 23–27 mm diam after 2 wk at 25 °C, moderate aerial mycelium, giving cottony appearance, umbonate, margins fringed; surface olivaceous, mycelium smoke grey; reverse grey olivaceous to dark grey olivaceous. Colonies on OA reaching 30–34 mm diam after 2 wk at 25 °C, sparse aerial mycelium, umbonate, margins fringed; surface olivaceous, mycelium smoke grey to grey olivaceous; reverse dark grey olivaceous.

Material examined: Malaysia, from leaves of Musa sp. (Musaceae), 2010, M.H. Wong (holotype CBS H-23394, culture ex-type CBS 143919 = CPC 18131).

Notes: Metulocladosporiella malaysiana is related to M. samutensis. These can be easily distinguished based on the length of the macronematous conidiophores (57–565 in M. malaysiana vs. 200–1120 μm in M. samutensis), and the almost total absence of secondary branches in M. samutensis. Moreover, M. malaysiana produces fewer micronematous condiophores than the other species of Metulocladosporiella.


Metulocladosporiella musigena

Y. Marín, Cheew. & Crous, sp. nov. MycoBank MB824033. Fig. 34.

Fig. 34. Metulocladosporiella musigena (ex-type CBS 143920). A. Colony on PDA. B. Colony on OA. C–F. Macronematous conidiophores. G–I. Conidiogenous apparatus. J, K. Lobed bases of macronematous conidiophore. L, M. Micronematous conidiophores. Scale bars: C–F = 20 μm; G–M = 10 μm; K applies to J, K.

Etymology: Name refers to Musa, the host from which it was isolated.

Mycelium internal and external, superficial; hyphae 1–4 μm wide, branched, septate, occasionally slightly constricted at septa, with small swellings, hyaline, subhyaline to pale olivaceous, thin-walled, smooth, hyphae occasionally aggregated, forming ropes; with a great amount of intermixed micronematous conidiophores, erect from vegetative mycelium, intercalary, straight to flexuous, unbranched, subhyaline, usually with simple terminal conidial chains. Macronematous conidiophores (115–)170–780 μm long, arising from superficial hyphae, erect, solitary to loosely aggregated, composed of a subcylindrical stipe, 4.5–7.5 μm wide, 5–14 septate, swollen or lobed at base, 7.5–14.5(–18.5) μm diam, with short, rhizoid, subhyaline to pale brown hyphae growing from base, medium to brown in lower half, paler towards apex, tips brown, pale brown or subhyaline, thick-walled below, thinner-walled towards apex, smooth; apex usually persistently branched, branched part composed of usually fairly compact, closely arranged subcylindrical branchlets, or sometimes giving rise directly to conidiogenous cells; primary branches 19–32.5(–43.5) × 3–4.5 μm, 0(–1)-septate, giving rise to 1–3 secondary branches, or to conidiogenous cells; secondary branches 15.5–31(–38) × 3–4.5 μm, 0(–1)-septate, giving rise to 1–3 conidiogenous cells; conidiogenous cells 13.5–28(–39.5) × 2.5–5 μm, subcylindrical, terminal or occasionally intercalary, sympodial, polyblastic, conidiogenous loci 1–2 μm wide, subconspicuous to conspicuous, subdenticulate, somewhat protuberant, truncate, wall unthickened to somewhat so, darkened-refractive. Conidia 5–15.5(–19.5) × 2–3.5 μm, in simple and branched acropetal chains, ellipsoid-ovoid, fusoid, subcylindrical, aseptate, subhyaline to pale brown, thin-walled, smooth, with 1–3(–4) hila, 0.8–1.2 μm diam, up to 1.7 μm diam at base of ramoconidia, truncate, unthickened or almost so, and somewhat darkened-refractive, secession schizolytic; ramoconidia 8–20.5 × 2.5–4 μm.

Culture characteristics: Colonies on PDA reaching 21–24 mm diam after 2 wk at 25 °C, moderate aerial mycelium, powdery, umbonate; surface smoke grey to grey olivaceous; reverse grey olivaceous to olivaceous black. Colonies on OA reaching 31–34 mm diam after 2 wk at 25 °C, moderate aerial mycelium, powdery, umbonate, slightly lobate; surface dark olivaceous, mycelium smoke grey to grey olivaceous; reverse dark slate blue.

Material examined: Thailand, Chiang Mai Province, Mae Rim District, Queen Sirikit Botanic Garden, from Musa sp. (Musaceae), 19 Jul. 2008, P.W. Crous & R. Cheewangkoon (holotype CBS H-23395, culture ex-type CBS 143920 = CPC 31490).

Notes: Metulocladosporiella musigena produces macronematous conidiophores directly producing conidiogenous cells at the apex, or composed of fairly compact branches, which are not observed in the other species of the genus. Moreover, it is characterised by the production of an excessive number of micronematous conidiophores.


Metulocladosporiella samutensis

Y. Marín, Luangsa-ard & Crous, sp. nov. MycoBank MB824034. Fig. 35.

Fig. 35. Metulocladosporiella samutensis (ex-type CBS 143921). A. Colony on PDA. B. Colony on OA. C. Macronematous conidiophores. D–F. Conidiogenous apparatus. G. Lobed bases of macronematous conidiophore. H–J. Micronematous conidiophores. Scale bars: C = 20 μm; others = 10 μm.

Etymology: Name from Samut Songkhram, the province in Thailand from where it was isolated.

Mycelium internal and external, superficial; hyphae 1.5–4 μm wide, branched, septate, occasionally slightly constricted at septa, with small swellings, hyaline, subhyaline to pale brown, thin-walled, smooth, hyphae occasionally aggregated, forming ropes; with intermixed micronematous conidiophores, erect from vegetative mycelium, intercalary, straight to flexuous, unbranched, subhyaline to pale brown, usually with simple terminal conidial chains. Macronematous conidiophores (200–)425–1000(–1120) μm long, arising from superficial hyphae, erect, solitary to loosely aggregated, composed of a subcylindrical stipe, 5.5–7.5(–8) μm wide, (4–)8–21(–29)-septate, swollen or lobed at base, 7–14.5(–20.5) μm diam, with short rhizoid subhyaline to pale brown hyphae growing from base, medium to brown in lower half, paler towards apex, tips pale brown or occasionally subhyaline, thick-walled below, thinner towards apex, smooth; apex giving rise directly to 1–2(–3) conidiogenous cells, or branched, branched part composed of loosely arranged subcylindrical branchlets; primary branches 24.5–39(–44) × 3–4(–5) μm, 0–1-septate, giving rise to 1–2(–3) conidiogenous cells, or rarely 1–2 secondary branches; conidiogenous cells (12–)14–25(–32) × 3.5–5 μm, subcylindrical, terminal or occasionally intercalary, sympodial, polyblastic, conidiogenous loci 1–2 μm wide, subconspicuous to conspicuous, subdenticulate, somewhat protuberant, truncate, wall unthickened to somewhat so, darkened-refractive. Conidia 4.5–12.5(–13.5) × 3–4 μm, in simple and branched acropetal chains, ellipsoid–ovoid, fusiform, subcylindrical, aseptate, subhyaline to pale brown, thin-walled, smooth, with 1–3 hila, 1–1.5(–2) μm diam, truncate, unthickened or almost so, and somewhat darkened-refractive, secession schizolytic; ramoconidia 8–13.5(–15.5) × 3–5 μm.

Culture characteristics: Colonies on PDA reaching a diameter of 34–36 mm after 2 wk at 25 °C, moderate aerial mycelium, powdery because of macroconidia, margins fringed; surface smoke grey to grey olivaceous, margins olivaceous; reverse olivaceous grey. Colonies on OA reaching a diameter of 39–40 mm after 2 wk at 25 °C, moderate aerial mycelium, powdery because of macroconidia, margins fringed; surface smoke grey to grey olivaceous, margins grey olivaceous; reverse olivaceous grey.

Material examined: Thailand, Samut Songkhram Province, from Musa sp. (Musaceae), 8 Jun. 2008, P.W. Crous (holotype CBS H-23396, culture ex-type CBS 143921 = CPC 33939).

Notes: Metulocladosporiella samutensis can easily be distinguished from other species of Metulocladosporiella by the production of conidiogenous cells directly from the apex, or loosely arranged primary branches, being almost totally absent of secondary branches.

Authors: Y. Marin-Felix, R. Cheewangkoon, J. Luangsa-ard & P.W. Crous