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Changing Taxonomic Concepts and Their Impact on Nomenclatural Stability

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Changing Taxonomic Concepts and Their Impact on Nomenclatural Stability Journal of Medical and Veterinary Mycology (1994), 32, Supplement 1, 113-122 Changing taxonomic concepts and their impact on nomenclatural stability G. S. DE HOOG 1, L. SIGLER 2, W. A. UNTEREINER 3, K. J. KWON-CHUNG 4, E. GUI~HO 5 AND J. M. J. UIJTHOF 1 1Centraalbureau voor Schimmelcultures, Baarn, The Netherlands," 2 University of Alberta Microfungus Collection, Edmonton, and 3Department of Botany, University of Toronto, Toronto, Canada," 4Clinical Mycology Section, National Institute of Health, Bethesda, USA; and s Unitd de Mycologie, Institut Pasteur, France Experimental techniques, which are routinely applied in yeast systematics, are currently finding recognition in a growing number of filamentous taxa. Some other biochemical markers have recently been developed in hyphomycete taxonomy. The spectrum of potential criteria now comprises characters of coenzyme-Q systems, secondary metabo- lites, protein electrophoresis, serology, nuclear (n) DNA/DNA reassociation, mole% G+C of DNA, protein electrophoresis, nutritional physiology and ultrastructural and karyological data. In addition, a wide range of molecular techniques is gaining rapid acceptance in evolutionary, systematic, ecological and epidemiological studies. Depend- ing on the aim of the study, partial DNA sequencing (mainly of SS and LS ribosomal genes and their spacers, but also of other genes), PCR-ribotyping and mitochondrial (mt) DNA restriction analyses are particularly powerful; for the establishment of the taxo- nomic position of taxa, 5.8S ribosomal (r) rRNA sequencing and Southern blotting with conserved genes are useful. Together with renewed in-depth morphological studies and the elucidation of teleomorph connections and (syn)anamorph life cycles, these tech- For personal use only. niques provide tools for an improved understanding of the phylogeny and ecological role of the distinguished taxa. Taxa are increasingly being classified along natural lines. The resulting changes in the taxonomic system, and thereby its impact on nomen- clature, may be considerable. This does not help in making taxonomy any more popular among medical mycologists. However, the significance to medical mycology of an improved taxonomic system should not be underestimated. Taxonomy is now becoming enabled to describe fungi as living entities in their natural ecological niche and thereby provides a better insight into their behaviour on the human body. We are now Med Mycol Downloaded from informahealthcare.com by 192.87.37.12 on 03/26/12 beginning to realize that several fungi have a narrow ecological amplitude and hence their role as aetiological agents of human disease may be well defined and characteristic for the species. The clinical significance of found taxa can thus be evaluated with more precision. Below some examples of fungal groups, in which the taxonomic concepts are subject to rapid change, are presented. Taxonomy of the Herpotrichiellaceae: holomorphs of black yeasts The Herpotrichiellaceae is a well defined family of loculoascomycetes encompassing species characterized by their small, inconspicuous, setose ascomata, bitunicate asci with a thickened endotunica and hyaline to brown, septate ascospores. Although originally circumscribed to include a number of genera differentiated on the basis of Correspondence address: Dr G. S. de Hoog, Centraalbureau voor Schimmelcultures, PO Box 273, 3740AG, Baarn, The Netherlands. 113 114 DE HOOG ET AL. 65~Exophiala salmonis t ~ Exophia/a jeanselmei I Capronia pulcherrima 9~ Capronia moravica 89 I =Caproniamoravica ~- Capronia epimyces ICapronia species 1 i Capronia fungicola 97 t Tubeufia helicomyces r--- Pleospora rudis L~ ~ Leptosphaeria doliolum L~ [- Leptosphaeria microscopica Leptosphaeria bicolor - [- Chaetomium elaturn r~ [---- Hypornyces elatum I I ~ Ophiostoma ulmi / 96 I i Microascus cirrosus N ~ Neurospora crassa II - Leucostoma persoonii I I Trichophyton rubrum I t__ Histoplasma capsulatum | Eurotium rubrum IO-~DS [~ Talaromyces flavus P FIG. 1. Phylogenetic tree of partial 18S rDNA sequences of 23 fungal taxa. A heuristic search was performed using TBR (tree bisection-reconnection) branch swapping with the MULPARSand STEEPEST DESCENT options (PAUV version 3.1.1). A single, most parsimonious tree was found (169 steps, CI=0.539 excluding uninformative characters). E. rubrum Konig, Spiekermann & Bremer and T. flavus (K16cker) Stolk & Samson were employed as out-groups. Branch lengths are proportional to the number of inferred substitutions. The numbers above the branches are the frequencies with which For personal use only. clades appeared in 100 boot-strap replicates. stromal development, ascospore septation and the number of ascospores per ascus, only two genera are recognized in current taxonomic treatments of the Herpotrichiellaceae [15]. Capronica Sacc., the largest genus in the family, includes species possessing dark ascomata, pigmented ascospores and dematiaceous, conidial anamorphs, the majority of which belong to the Exophiala-Ramichloridium Rhinocladiella complex. This Med Mycol Downloaded from informahealthcare.com by 192.87.37.12 on 03/26/12 complex constitutes a group of medically significant opportunists known as 'black yeasts'. Anamorphs belonging to the genus Exophiala Carmichael are unknown outside the Herpotrichiellaceae [6], and the predominance of black yeast anamorphs within the family suggests the close phylogenetic relationship of Exophiala and associated synanamorphs to the genus Capronia. Phylogenetic analysis of partial 18S rDNA sequences of 23 taxa (Fig. 1) demon- strates that species of Capronia possessing Exophiala or Ramichloridium anamorphs and species of Exophiala for which teleomorphs are unknown form a monophyletic group within the Ascomycotina. This clade is distinct from the Pleosporales (Tubeufiaceae and Pleosporaceae) and the unitunicate pyrenomycetes. Although this analysis supports the close phylogenetic relationship of species of Capronia and Exophiala, partial 18S sequence data do not permit the elucidation of inter-familial relationships. For example, Capronia fungicola (Samuels & Miiller) Untereiner, a species with a well developed stroma and an anamorph similar to Ramichloridium anceps (Sacc. & Ellis) de Hoog, and TAXONOMIC CONCEPTS AND NOMENCLATURAL STABILITY 115 Capronia species 1, with muriform ascospores, are not delimited from species of Capronia that lack a basal stroma and sympodial conidiogenous cells and possess phragmoseptate ascospores. The phylogram indicates, however, that Capronia moravica (Petrak) M/iller et al., the type species of the Herpotrichiellaceae, and Capronia epimyces Barr, which produces an Exophiala anamorph and Phialophora synanamorph, are distinct within the Herpotrichiellaceae. The type strains of Exophiala salmonis Carmichael (CBS 157.67) and Exophiala jeanselmei (Langer.) McGinnis & Padhye var. jeanselmei (CBS 664.76) form a monophyletic group within the family (boot-strap support 65%), but the position of this clade relative to species of Capronia is unresolved. Sequence data from the more rapidly evolving rDNA internal transcribed spacers (ITS 1 and ITS 2) are presently being evaluated to address questions concerning the reliability of anamorphs and morphological characters in delimiting species of Capronia and the relationship between parasitic and saprotrophic species of Exophiala. Although teleomorphs are not known for the majority of black yeasts, the loculoascomycetous affinity of species of Exophiala has been confirmed by the produc- tion of pseudoparenchymatous ascomatal initials in isolates of E. jeanselmei var. jeanselmei and Exopthiala mansonii (Castell.) de Hoog [22]. Ascomatal initials and ascomata are not produced in vitro in the type strains of species of Exophiala [22] but immature, setose ascomata have been observed in additional isolates of Exophiala dermatitidis (Kano) de Hoog and pallid, non-setose, pseudoparenchymatous initials are formed in one isolate of E. salmonis [W. A. Untereiner, unpublished data]. Morpho- logical and cultural characteristics are inadequate for the reliable separation of species of Exophiala and it is unlikely that these taxa can be clearly delimited using traditional taxonomic methods. The in vitro production of teleomorphs or their discovery in nature would furnish criteria necessary to determine unambiguously the systematic position of Exophiala and also provide information for elucidating the life cycles of these fungi. For personal use only. Despite their occurrence on decaying plant material and on the decaying ascomata and basidiomata of other fungi, species of Capronia are unable to enzymatically degrade cellulose, lignin, starch, pectin and chitin [W. A. Untereiner, unpublished data]. Their inability to utilize these compounds supports the suggestion of Munk [16] that the members of the Herpotrichiellaceae are saprotrophs of secondary incidence (hyper- saprophytes) rather than primary degraders of plant material or mycoparasites. Species of Rhinocladiella Nannf., Ramichloridium Stahel ex de Hoog and Cladosporium Link resembling the anamorphs of some members of the genus Capronia are also found on Med Mycol Downloaded from informahealthcare.com by 192.87.37.12 on 03/26/12 decaying wood and fungal fruit-bodies, and members of the genus Exophiala are commonly isolated from these substrata. The ecology and biological activity of black yeasts in natural systems are poorly understood, and until further investigated, questions concerning the significance of pleomorphism in the life cycles
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