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A new synnematous species of Penicillium from soil in Taiwan

     Department of Hospital and Health Care Administration, Chia-Nan University of Pharmacy and Science, Tainan, Taiwan 71710, ROC

	ABSTRACT

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A synnematous species of Penicillium, P. calidicanium, is described and illustrated. The fungus was isolated from soil in Taiwan. Penicillium calidicanium can be placed in subgenus Biverticillium because of its symmetrical, biverticillate penicilli, ampulliform to acerose phialides, and ability to produce abundant synnemata in Czapek yeast extract agar, malt extract agar, and Czapek's solution agar. It is close to P. duclauxii and P. vulpinum, but differs in colony morphology, growth rate, morphology of the synnemata, and ornamentation of the conidial wall.

Key words: subgenus Biverticillium, taxonomy, Trichocomaceae

	INTRODUCTION

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During a survey on hyphomycetous fungi in Taiwan, a previously undescribed synnematous Penicillium species was isolated from soil in Nantou County. This species is easily distinguished from other known species of Penicillium and is described here as a new species, P. calidicanium, which is classified, according to Pitt (1979), into subgenus Biverticillium Dierckx, section Coremigenum (Biourge) Pitt and series Duclauxii Raper & Thom ex Pitt. Notable characteristics of the new fungus include its biverticillate penicilli and its ability to produce conspicuous synnemata on Czapek yeast extract agar (CYA) and malt extract agar (MEA).

Several synnematous species of Penicillium have been described. They were separated by morphological criteria, nucleotide sequences, or arbitrarily primed polymerase chain reaction analysis (Quintanilla 1984, Seifert and Samson 1986, Hsieh et al 1987, Samson et al 1989, Frisvad 1990, Holmes et al 1994, Lobuglio et al 1994).

Seifert and Samson (1986) examined type specimens of many species attributed to Coremium Link, a genus long considered a synonym of Penicillium. They proposed three new combinations to accommodate the synnematous Penicillium species. These included: P. vulpinum (Cooke & Massee) Seifert & Samson (synonym: P. claviforme Bain); P. coprophilum (Berk. & Curt.) Seifert & Samson (synonym: P. concentricum Samson, Stolk & Hadlok), and P. glandicola (Oud.) Seifert & Samson (synonym: P. granulatum Bain). In 1990, Frisvad et al reviewed 122 new names that have been described in Penicillium, Talaromyces, and Eupenicillium, since the monographic treatment of Pitt (1979). They accepted 48 taxa, including several synnematous Penicillium species (P. coalescens, P. coprophilum, P. dendriticum, P. vulpinum, and P. glandicola) (Frisvad et al 1990), and two synnematous Penicillium species, P. formosana Hsieh, Su & Tzean and P. ulaiense Hsieh, Su & Tzean, were described later by Hsieh et al (1987). Holmes et al (1993, 1994) published a description of a new postharvest disease of citrus caused by P. ulaiense and furnished a revised description for the fungus. The new species described herein is most clearly distinguished from P. ulaiense and P. formosana by morphology of the penicillus (biverticillate penicilli) and ornamentation of the conidial wall (reticulate conidia).

	MATERIALS AND METHODS

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An uncommon Penicillium was isolated from soil in Nantou County, Taiwan in 1996. The methods of pure cultures follow King et al (1979). The isolate was maintained on slants of malt extract agar (MEA) at room temperature and transferred to 9-cm Petri dishes of diagnostic media for various examinations. The identification media, description, and morphological criteria of the new taxon followed the methodology of Pitt (1979, 1988). The fungus was also inoculated and described onto malt extract agar at 37 C, 25% glycerol nitrate agar (G25N) at 5 and 37 C and Czapek's solution agar (Cz) at 5, 25, and 37 C for 7 d under dark. The concept of synnemata is used according to the definition of Hawksworth et al (1995). The morphology of the fungus was studied with scanning electron microscopy using methods described previously (Tzean and Estey 1978). Colony characters and microscopic morphological characteristics were recorded and illustrated using a Leica stereomicroscope (MZ8) and an Olympus light microscope (BX50). The Methuen Handbook of Colour is used for description of the colours (Kornerup and Wanscher 1978). Living cultures were deposited at Culture Collection and Research Center (CCRC 33728), Taiwan, ROC. Dried cultures are deposited in the Chen Fungus Collection (CFC-7) and National Museum of Natural Science, Taichung, Taiwan (Herb. TNM F12246).

	TAXONOMY

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Penicillium calidicanium J.L. Chen sp. nov. (Figs. 1–17)

View larger version (46K): [in this window] [in a new window]    FIGS. 1–4. Penicillium calidicanium. 1. Synnemata. 2. Conidial chains. 3. Penicilli. 4. Conidia. Bars: 1 = 2 mm; 2 = 100 µm; 3, 4 = 10 µm

On CYA, 25 C, 7 d, colonies growing rapidly, 36–47 mm diam, velutinous, grayish yellow (2–3B3–4), grayish green (29–30C-D4–5) to grayish blue or dull blue (23–24C-E3–4), margins low, regular, white; synnemata abundant, crowded, up to 5 mm high, clavate to elongate-clavate with pale yellow to yellow sterile stalks; mycelium white to yellow (3A3–6); sporulation moderate to abundant, grayish to grayish green (29–30C-D4–5), or grayish blue to dull blue (23–24C-E3–4); exudate clear; soluble pigment absent or dull red (10–11B-C3–4) in age (after 14 d); reverse pale yellow (4A3–8) to deep yellow or brown (6D-E6–8).

On MEA, 25 C, 7 d, colonies growing rapidly, 41–53 mm diam, plane, more or less zonate (concentric zones), grayish green to dark green (30B-F3–5); synnemata moderately abundant, crowded or scattered, up to 7 mm long, clavate to elongate-clavate with pale yellow sterile stalks; margins plane, regular, white; mycelium white; sporulation abundant, gray green to dark green (30C-F4–6); exudate clear; soluble pigment absent; reverse pale brown, yellowish brown (5D-E4–5) to brown (6C-F4–7).

On G25N, 25 C, 7 d, no germination. On Cz, 25 C, 7 d, colonies 21–27 mm diam; 14 d, colonies 57–63 mm diam, velutinous; synnemata abundant, up to 8 mm high; mycelium pale yellow to dull yellow (3A-B3–4); sporulation abundant, dark green (30D-F3–5); exudate clear to pale red (7–8A2–3); soluble pigment absent; reverse yellow (3–4A-B3–5) to dull yellow or yellow-brown (5–6D-E4–6). On CYA, MEA and Cz at 5 C or 37 C, 7 d, no germination.

Micromorphology on CYA 25 C 7 d: Conidiophores borne on surface hyphae and synnemata (often anastomosing); stipes determinate (32.5–200 µm high) or indeterminate, erect, sinuous, flexuous, finely roughened to roughened or verruculose, hyaline to subhyaline or pale olivaceous, septate, 2–4.2 µm wide; penicilli mostly biverticillate, sparsely irregularly branched; rami in groups of 2, finely roughened to roughened 12–16.8 x 2.4–3.7 µm; metula in groups of 3–8, finely roughened, subhyaline or pale olivaceous, 6.4–13.6 x 2–4 µm; phialides in verticils of 3–8, ampulliform to acerose, with short collula, finely roughened, hyaline to pale olivaceous, 5.6–10.4 x 2–3 µm; conidia mostly ellipsoidal, short-fusiform, rarely ovoid or subglobose, 2.4–3.8 x 1.6–3 µm spiral-striated transversely by LM and appearing reticulate by SEM hyaline, pale olivaceous to pale dull olivaceous, often with narrow disjunctors, borne in long disordered chains and over the entire synnematal head in closely packed columns.

Micromorphology on MEA at 25 C in 7 d: conidiophores borne from synnemata and surface hyphae, often anastomosing (especially on synnemata); stipes determinate (40–240 µm high) or indeterminate, straight, septate, finely roughened, hyaline, thick-walled, 2.8–4 µm wide; penicilli mostly biverticillate, sparely monoverticillate or terverticillate; rami in groups of 2–3, 16.8–20 x 2.4–3.2 µm; metula in groups of (2)3–8, 7–16 x 2.2–3.4 µm, finely roughened, hyaline; phialides in verticils of 3–8, ampulliform to acerose, with short collula, smooth to finely roughened, hyaline, 6.8–11.2 x 1.6–3 µm; conidia mostly ellipsoidal to fusiform, rarely subglobose, ovoid, 2.5–4.4 x 1.9–3.2 µm, finely roughened to roughened or spiral-striated, hyaline, pale green to pale dull green, borne in long disordered chains.

Specimen examined. TAIWAN. Nantou County, from soil, 31 Mar 1996, J.L. Chen, HOLOTYPE CFC-7, ISOTYPES TNM F12246.

Etymology. The specific epithet, calidicanium, refers to the hot dog-like shape of the synnemata.

Commentary. Penicillium calidicanium produces clavate or elongate-clavate synnemata (Fig. 1) with grayish to dark green capitula and pale yellow to yellow stalks, predominantly symmetrically biverticillate penicilli (Figs. 8–9, 12–15) and ellipsoidal to short-fusiform, finely roughened to roughened or spiral-striated (Figs. 10–11, 16–17) conidia. It can be placed in subgenus Biverticillium. Among the described taxa in subgenus Biverticillium, Penicillium vulpinum, and Penicillium duclauxii also produce distinct synnemata (Frisvad et al 1990, Pitt 1979, 1988, Seifert and Samson 1986). The closest species is P. vulpinum, which usually produces clavate synnemata, irregularly branched penicilli, few phialides per metula and larger, smooth conidia, all of which distinguish it from P. calidicanium (Pitt 1979, 1988, Seifert and Samson 1986). Penicillium vulpinum is like P. calidicanium in lack of colony growth on CYA at 37 C, in synnemata morphology, and in exudate color on both CYA and MEA at 25 C. Penicillium vulpinum, however, differs in growing more slowly on CYA and MEA at 25 C, and in having growth on G25N at 25 C and CYA at 5 C (Pitt 1979, 1988, Seifert and Samson 1986). In addition, P. vulpinum has a white mycelium, greenish gray sporulation, but lacks a pale to deep brown or reddish brown colonial reverse and soluble pigment on CYA and MEA at 25 C (Pitt 1979, 1988, Seifert and Samson 1986). They also differ in conidiogenous structures as summarized in Table I. Morphologically, Penicillium calidicanium and P. duclauxii are similar in lack of colony growth on CYA at 37 C, coloration of mycelium, conidiogenesis, reverse coloration, and morphology of penicilli on CYA at 25 C (Pitt 1979, 1988). However P. duclauxii is not known to produce clavate, elongate-clavate synnemata, up to 3–8 metulae per ramus and finely roughened to roughened or spiral-striated conidia on culture medium. Instead, it is characterized by acicular (needle-shaped) synnemata, 1–2 rami per penicillus, metulae in whorls of 3–5 on the ramus, phialides in compact whorls of 5–8 on metulae and ellipsoidal to apiculate, smooth to finely roughened conidia (Pitt 1979, 1988). A comparative summary of the important characteristics of Penicillium calidicanium and two closely related Penicillium species on CYA, at 25 C is presented in Table I.

View larger version (142K): [in this window] [in a new window]    FIGS. 5–11. Penicillium calidicanium. 5, 6. Colonies on CYA and MEA at 25 C, 7 d. 7. Synnema with sterile stalk. 8, 9. Biverticilate penicilli. 10, 11. Ellipsoidal to fusiform conidia with roughened (arrow) or spiral-striated (double arrow) walls. Bars: 5, 6 = 1 cm; 7 = 100 µm; 8, 9 = 10 µm; 10, 11 = 10 µm.

View larger version (191K): [in this window] [in a new window]    FIGS. 12–17. Penicillium calidicanium (from SEM). 12–14. Penicilli. 15. Detailed penicillus with finely roughened walls, and ampulliform to acerose phialides with short collula. 16, 17. Ellipsoidal to fusiform conidia with roughened or spiral-striated walls and narrow disjunctors (arrow) at both ends. Bars: 12 = 10 µm; 13 = 10 µm; 14 = 10 µm; 15 = 5 µm; 16 = 2 µm; 17 = 4 µm.

	ACKNOWLEDGMENTS

 
We are indebted to Dr. Y.M. Ju, Institute of Botany, Academia Sinica, Taipei, Taiwan, ROC, and Dr. Maren A. Klich, Southern Regional Research Center, USDA, New Orleans, USA, for critically reviewing the manuscript. We thank the National Science Council (NSC-86-2314-B-041-008) for funding this research.

	FOOTNOTES

 
¹ Corresponding author, Email: ccl51911{at}ms29.hinet.net

Accepted for publication February 21, 2002.

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS TAXONOMY LITERATURE CITED

 
Frisvad JC, Samson RA, Stolk AC., 1990 Disposition of recently described species of Penicillium. Persoonia 14:209-232

Hawksworth DL, Kirk PM, Sutton BC, Pegler DN., 1995 Ainsworth and Bisby's dictionary of the fungi. 8th ed. CAB International Mycological Institute: Cambridge University Press, England. 616 p

Holmes GJ, Eckert JW, Pitt JI., 1993 A new postharvest disease of citrus in California caused by Penicillium ulaiense. Plant Dis 77:537.

———, ———, ———. 1994 Revised description of Penicillium ulaiense and its role as a pathogen of citrus fruits. Phytopathology 84:719-727

Hsieh HM, Su HJ, Tzean SS., 1987 The genus Penicillium in Taiwan. I. Two new taxa of synnematous Penicillium. Trans Mycol Soc Repub China 2:157-168

King AD, Hocking AD, Pitt JI., 1979 Dichloran rose bengal medium for enumeration and isolation of molds from foods. Appl Environ Microbiol 37:959-964[Abstract/Free Full Text]

Kornerup A, Wanscher JH., 1978 Methuen Handbook of Colour. 3rd ed. Eyre Methuen, London. 252 p

Lobuglio KF, Pitt JI, Taylor JW., 1994 Independent origins of the synnematous Penicillium species, P. duclauxii, P. clavigerum, and P. vulpinum, as assessed by two ribosomal DNA regions. Mycol Res 2:250-256

Pitt JI., 1979 The Genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. London: Academic Press. 634 p

———. 1988 A laboratory guide to common Penicillium species. CSIRO Division of Food Processing: North Ryde, NSW, Australia. 187 p

Quintanilla JA., 1984 A new species of Penicillium from soil: P. coalescens, sp. nov. Mycopathologia 84:115-120

Samson RA, Stolk AC, Frisvad JC., 1989 Two new synnematous species of Penicillium. Stud Mycol 31:133-143

Seifert KA, Samson RA., 1986 The genus Coremium and the synnematous Penicillia. In: Samson RA, Pitt JI, eds. Advances in Penicillium and Aspergillus systematics. New York: Plenum Press. p 143–154

Tzean SS, Estey RH., 1978 Schizophyllum commune Fr. as a destructive mycoparasite. Can J Microbiol 24:780-784[Medline]

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