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The Ajellomycetaceae, a new family of vertebrate-associated Onygenales

     Department of Botany, Brandon University, Brandon, Manitoba, R7A 6A9 Canada

James A. Scott

     Department of Public Health Sciences, University of Toronto, Toronto, Ontario, M5T 1R4, Canada, and Sporometrics Inc., Toronto, Ontario, M6K 1Y9 Canada

Françoise A. Naveau

     Euroscreen, Brussels, B-1070 Belgium

Lynne Sigler

     University of Alberta Microfungus Collection and Herbarium, Devonian Botanic Garden, Edmonton, Alberta, T6G 2E1 Canada

Jason Bachewich
Andrea Angus

     Department of Botany, Brandon University, Brandon, Manitoba, R7A 6A9 Canada

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION TAXONOMY LITERATURE CITED

 

Phylogenies inferred from the analysis of DNA sequence data have shown that the Onygenales contains clades that do not correspond with previously described families. One lineage identified in recent molecular phylogenetic studies includes the dimorphic pathogens belonging to the genera Ajellomyces, Emmonsia and Paracoccidioides. To evaluate the degree of support for this lineage and determine whether it includes additional taxa, we examined relationships among the members of this clade and selected saprobic onygenalean taxa based on maximum-parsimony analyses of partial nuclear large RNA subunit (LSU) and internal transcribed spacer (ITS) sequences. A clade distinct from the Onygenaceae was found to encompass Ajellomyces (including the anamorph genera Blastomyces, Emmonsia and Histoplasma) and Paracoccidioides brasiliensis. The members of this lineage are saprobic and pathogenic vertebrate-associated taxa distinguished by their globose ascomata with coiled appendages, muricate globose or oblate ascospores, and lack of keratinolytic activity. Anamorphs are solitary aleurioconidia or irregular alternate arthroconidia. Based on molecular data and on morphological and physiological similarities among these taxa, we propose the new family, Ajellomycetaceae.

Key words: Ajellomyces, Blastomyces dermatitidis, Histoplasma capsulatum, molecular systematics, rDNA sequences, taxonomy

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION TAXONOMY LITERATURE CITED

 
The Onygenales is a monophyletic lineage within the Ascomycota encompassing species with gymnothecial or cleistothecial ascomata, evanescent asci, unicellular ascospores and aleurio- or arthroconidial anamorphs. As circumscribed by Currah (1985, 1994), the order includes four families separated on the basis of anamorph connections, ascospore ornamentation and the ability to enzymatically degrade cellulose or keratin. Keratinolytic activity, as demonstrated through hair degradation tests or inferred from the occurrence of taxa on keratin-rich substrates, defines the Arthrodermataceae and Onygenaceae, whereas the remaining nonkeratinolytic and cellulolytic members of the order have been assigned to the Gymnoascaceae and Myxotrichaceae, respectively.

With the exception of the Myxotrichaceae, a group now recognized to be more closely allied to the Leotiales (Currah 1997, Sugiyama et al 1999), Currah’s concept of the Onygenales has been supported by the results of studies of the ecology, molecular systematics and morphology of members of this order. The Gymnoascaceae, a family once thought to represent a heterogeneous assemblage of taxa with affinities to the Arthrodermataceae and Eurotiales (Currah 1985, 1994), forms a monophyletic group in phylogenies based on the analysis of nuclear ribosomal RNA (rRNA) gene sequences (Sugiyama and Mikawa 2001, Sugiyama et al 1999, Untereiner et al 2002). The Arthrodermataceae, which encompasses taxa with smooth ascospores and anamorphs assigned to Chrysosporium Corda, Epidermophyton Sabour., Microsporum Gruby and Trichophyton Malmsten, also is represented as a well-supported lineage in analyses of nuclear rRNA and chitin synthase gene sequences (Herr et al 2001, Leclerc et al 1994, Sugiyama et al 1999). The phylogenetic structure of the Onygenaceae, a family that includes species with pitted ascospores and anamorphs placed in Blastomyces Gilchrist & Stokes (= Chrysosporium fide Carmichael 1962), Coccidioides G.W. Stiles, Chrysosporium, Emmonsia Ciferri & Montemartini, Histoplasma Darling, Malbranchea Sacc. and Paracoccidioides Almeida, is resolved less clearly. Recent sequence-based phylogenies indicate that the family is polyphyletic (Gibas et al 2002, Herr et al 2001, Sugiyama and Mikawa 2001, Sugiyama et al 1999, Untereiner et al 2002).

One clade recognized consistently in molecular phylogenetic studies of the Onygenaceae includes a group of medically important taxa encompassing the dimorphic systemic pathogens. Taxa identified as members of this clade in phylogenies inferred from nuclear small subunit (SSU) rRNA, nuclear large subunit (LSU) rRNA and internal transcribed spacer (ITS) sequences include Ajellomyces capsulatus (anamorph Histoplasma capsulatum Darling), A. crescens (anamorph Emmonsia crescens), A. dermatitidis (anamorph Blastomyces dermatitidis Gilchrist & Stokes) and species of the anamorph genera Emmonsia and Paracoccidioides (Herr et al 2001, Peterson and Sigler 1998, Sugiyama et al 1999, Vidal et al 2000). Spiromastix Kuehn & Orr, a nonpathogenic member of the Onygenaceae, recently was positioned within this clade based on the comparison of nuclear LSU sequences (Sugiyama and Mikawa 2001). This finding was corroborated by Untereiner et al (2002) in an investigation that examined phylogenetic relationships of species of Ajellomyces McDonough & Lewis, Polytolypa Scott & Malloch and Spiromastix inferred from the analysis of nonmolecular characters and sequences from the nuclear LSU and mitochondrial SSU rRNA genes. Based on the results of their study, Untereiner et al (2002) transferred Spiromastix grisea Currah & Locquin-Linard to Ajellomyces and restricted Spiromastix (typified by S. warcupii) to species isolated from soil that possess oblate ascospores and peridial appendages that are wavy to helical but with only 1–2 turns per helix. Polytolypa hystricis, a species described from porcupine dung (Scott et al 1993), also was shown to be closely related to Ajellomyces and Spiromastix, but its phylogenetic position was not sufficiently resolved to propose its transfer to either genus (Untereiner et al 2002).

In the present investigation, we examined the phylogenetic structure of the Onygenaceae sensu lato based on the analysis of nuclear LSU and ITS rDNA sequences for an expanded set of taxa. Our results provide further evidence for the recognition of the clade encompassing Ajellomyces (including the anamorph genera Blastomyces, Emmonsia and Histoplasma) and Paracoccidioides that we describe formally as a new family.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION TAXONOMY LITERATURE CITED

 
Fungal isolates. – Isolates and sequences employed in this study are listed in TABLE I. Cultures sequenced during this investigation were maintained at room temperature on modified Leonian’s agar (MLA) (Malloch 1981).

Data analysis. – Sequences were edited and assembled into larger consensus sequences using Sequencher 3.0 software (Gene Codes Corp., Ann Arbor, Michigan). Multiple alignments were produced using Clustal X version 1.7 (Thompson et al 1994). The final multiple alignments were adjusted manually after visual inspection and areas of sequence ambiguity were eliminated. The first alignment (TreeBase SN1748-5533), which included partial LSU rDNA sequences (924 bp) for 61 taxa, was analyzed to determine the phylogenetic positions of species assigned presently to the Arthrodermataceae, Gymnoascaceae and Onygenaceae sensu lato. The second alignment (TreeBase SN1748-5534) consisted of the combined ITS-LSU rDNA sequences (1149 bp) of 21 taxa. Outgroup taxa were Auxarthron californiense (21-taxon phylogeny) and Byssochlamys nivea, Eurotium herbariorum and Petromyces alliaceus (61-taxon phylogeny).

Phylogenetic relationships were inferred from aligned sequences using the maximum parsimony (MP) method found in PAUP* (beta version 4.0b10) (Swofford 2002). Gaps were treated as missing in all analyses. Heuristic searches of the 21- and 61-taxon datasets were performed employing tree bisection-reconstruction (TBR) branch swapping with the MulTrees and steepest descent options activated. Heuristic searches of the ITS-LSU alignment for new optimal trees were conducted using 1000 random-addition-sequence replicates. Constraint trees for the 21-taxon alignment were constructed using MacClade 3.05 (Maddison and Maddison 1992), imported into PAUP* and compared to the most-parsimonious tree (MPT) inferred from MP analysis using the Kishino-Hasegawa test. Phylogenies inferred from a pruned 12-taxon alignment also were generated from exhaustive searches of the ITS and combined ITS-LSU datasets.

Bremer support (Bremer 1994) was determined heuristically by searching for trees up to five steps (61-taxon phylogeny) or 10 steps (21-taxon phylogeny) longer than the MPT and is given as the number of additional steps necessary for the collapse of a particular clade. Bootstrap support (Felsenstein 1985) for internal branches was evaluated from 100 (LSU dataset) or 1000 (ITS-LSU dataset) heuristic searches, and groups with a frequency of greater than 50% were retained in the bootstrap consensus trees. Congruence between the ITS and LSU datasets for the 21-taxon dataset was measured based on 1000 searches using the partition-homogeneity test (PHT) (Farris et al 1995) included in PAUP*.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION TAXONOMY LITERATURE CITED

 
Sequences employed in the molecular datasets ranged from 1146 to 1212 bp (ITS-LSU) and 552 to 953 bp (LSU) in length before deletion of ambiguous or unalignable bp (data not shown). The larger LSU dataset (61 taxa, 924 bp) contained sequences of 58 members of the Onygenales and consisted of 192 phylogenetically informative characters. MP analysis of this dataset produced three MPT 969 steps in length (L) with a consistency index (CI) of 0.362 and a retention index (RI) of 0.698. The strict consensus of these trees (FIG. 1) contained a large, well-supported clade (bootstrap support 100%) corresponding to the Onygenales. Three major lineages within the Onygenales receiving bootstrap support ( 70%) included the Ajellomyces-Paracoccidioides clade (73%), the Spiromastix-Malbranchea sp. clade (86%), and a large, well-supported group (94%) encompassing these subclades: Amauroascus kuehnii-Auxarthron-Malbranchea aurantiaca (79%), Amauroascus niger-Coccidioides (74%), Aphanoascus-Chrysosporium keratinophilum (98%), Ascocalvatia-Onygena (100%), Am. purpureus-Neogymnomyces-Renispora (75%) and the Arthrodermataceae (85%). Less robustly supported groups (<70%) within the largest lineage were the Apinisia-Am. albicans subclade (69%) and the Gymnoascaceae (64%). The position of Polytolypa hystricis was unresolved in the strict consensus.

View larger version (46K): [in this window] [in a new window]   FIG. 1. Phylogenetic relationships of the Onygenales inferred from partial LSU rDNA sequence data. This is the strict consensus of 3 MPT (L = 969 steps) generated from an heuristic analysis of 924 bp for 61 taxa (CI = 0.362, RI = 0.698). Bootstrap values greater than 50% calculated from 100 replicates are given above either the branches or the diagonal lines adjacent to branches. Bremer support is shown either below the branches or the diagonal lines adjacent to branches. An asterisk indicates clades retained in trees five steps longer than the MPT. A "T" designates strains derived from the type specimen. Outgroup taxa are Byssochlamys nivea, Eurotium herbariorum and Petromyces alliaceus.

View larger version (26K): [in this window] [in a new window]   FIG. 2. Phylogenetic relationships within the Ajellomycetaceae inferred from the combined dataset (ITS and partial LSU rDNA sequences). This is the single MPT (L = 803) generated from an heuristic analysis of 1149 bp for 21 taxa (CI = 0.654, RI = 0.632). Bootstrap values greater than 50% calculated from 1000 replicates are given either above branches or to left of the diagonal lines adjacent to branches. Bremer support is shown either below the branches or the diagonal lines adjacent to branches. An asterisk indicates clades retained in trees 10 steps longer than the MPT. A "T" designates strains derived from the type specimen. Outgroup taxon is Auxarthron californiense.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION TAXONOMY LITERATURE CITED

 
As circumscribed currently, the Onygenaceae sensu lato includes keratinolytic and keratinophilic taxa with pitted or punctate ascospores and a variety of types of peridial hyphae (Currah 1985, 1994). The family has been considered to be relatively homogeneous, but this study and other recent molecular phylogenetic studies indicate that the Onygenaceae is polyphyletic and confirm that ascomatal and ascospore morphology are of limited value as predictors of phylogenetic relationship (Sugiyama and Mikawa 2001, Sugiyama et al 1999, 2002). Analyses of rDNA sequence data divide the Onygenaceae into a number of clades. One of these clades, represented by species of Ajellomyces (encompassing the anamorphic genera Blastomyces, Emmonsia and Histoplasma), Lacazia and Paracoccidioides is resolved in phylogenies inferred from nuclear SSU (Herr et al 2001, Sugiyama et al 1999), LSU (Sugiyama and Mikawa 2001) and combined LSU-SSU rDNA sequences (Sugiyama et al 2002). The Ajellomyces clade was shown in a recent nuclear SSU rDNA phylogeny to be sister of the Arachnomycetales, a lineage encompassing species of Arachnomyces Massee & Salmon, and of the Eurotiales (Gibas et al 2002), but its position relative to these taxa and to other members of the Onygenales was not resolved. A second clade identified in phylogenies inferred from rDNA sequences encompasses Polytolypa hystricis, species of Malbranchea and members of the genus Spiromastix (Sugiyama and Mikawa 2001, Sugiyama et al 2002, Untereiner et al 2002). The largest clade representing the Onygenaceae contains the dimorphic pathogen Coccidioides immitis and the remaining members of the family (FIG. 1, this study; Sugiyama and Mikawa 2001, Sugiyama et al 2002).

Within the Ajellomyces clade, the vertebrate pathogenic members of the genus form a moderately well-supported group. The teleomorphic taxa (A. capsulatus, A. crescens and A. dermatitidis) are the closest relatives of anamorphic taxa from both clinical and environmental sources (Emmonsia sp., E. parva, Paracoccidioides brasiliensis) (FIG. 2). Ajellomyces dermatitidis (anamorph Blastomyces dermatitidis) is the closest relative of E. parva, and these taxa form a group that is sister of a well-supported clade that includes mating and nonmating isolates of A. crescens (FIG. 2, this study; Peterson and Sigler 1998). As shown by Peterson and Sigler (1998) and confirmed in the present study, P. brasiliensis is closely related to species of Ajellomyces but its position is not clearly resolved. The phylogenetic position of A. capsulatus (anamorph Histoplasma capsulatum) also requires further study. Ajellomyces grisea, a species transferred by Untereiner et al (2002) from the genus Spiromastix, is confirmed as a member of the strongly supported Ajellomyces clade (81–97% bootstrap support) (FIG. 2, this study; Sugiyama et al 2002, Untereiner et al 2002).

Species of Ajellomyces form globose ascomata with coiled or appendages and small, finely ornamented ascospores that appear smooth by light microscopy (Currah 1985, Kwon-Chung 1973, McDonough and Lewis 1986, Sigler 1996, 2002). Ascospores are hyaline, globose and muricate or oblate and finely punctate, <2.5 µm diam (Currah and Locquin-Linard 1987, Sigler 1996, 2002). Anamorphs are prominent and have been the primary means of recognition and identification of these taxa in the clinical setting. Conidia are smooth to slightly echinulate or tuberculate solitary aleurioconidia borne on stalks that often are slightly swollen at the end nearest to the conidium (Carmichael 1962, Sigler 1996, 2002). Intercalary arthroconidia are formed irregularly in Paracoccidioides brasiliensis (Sigler 2002).

Not every member of this lineage is pathogenic, but all are vertebrate-associated and they share similar substrates and physiological characteristics. Species of Ajellomyces and Paracoccidioides are isolated from animal hosts, dung, or more rarely soils associated with animals and animal dung (Kwon-Chung and Bennett 1992, Peterson and Sigler 1998, Sigler 2002). All exhibit growth at 35 C or higher, but growth may be strongly inhibited (Sigler 1996, 2002, Untereiner et al 2002). Ajellomyces capsulatus, A. dermatitidis and P. brasiliensis exhibit thermal dimorphism and grow in a yeast phase in vivo and in vitro at 35–37 C (Kwon-Chung and Bennett 1992, Sigler 2002). Ajellomyces and Emmonsia show varying degrees of cycloheximide resistance (Scott et al 1993, Sigler 1996, 2002). None of the members of this clade demonstrate keratinolytic activity as measured by hair degradation or by the keratin azure test (Carmichael 1962, Scott et al 1993, Scott and Untereiner 2004, Sigler unpubl data, Untereiner et al 2002).

Polytolypa hystricis and species of Spiromastix (S. tentaculatum, S. warcupii and Spiromastix sp. JCM 11276) are sister of the Ajellomyces clade, lack keratinolytic activity and share some morphological features (this study, Sugiyama and Mikawa 2001, Sugiyama et al 2002, Untereiner et al 2002). Polytolypa is similar to Ajellomyces in having tightly coiled peridial appendages that possess two to many turns per helix and ascospores which are muricate. This taxon differs in having yellow to yellow-orange ascospores that are ellipsoidal and larger (3–4 µm diam) and in producing alternate arthroconidia (Scott et al 1993). Conidia are absent in species of Spiromastix, and peridial appendages are wavy to slightly curved or helical (Currah 1985, 1988, Currah and Locquin-Linard 1988). Although we hypothesize that these taxa are closely related phylogenetically, the monophylly of Ajellomyces, Polytolypa and Spiromastix depicted in our ITS-LSU phylogeny (FIG. 2) and in the phylogenies of Untereiner et al (2002) likely reflects the choice of outgroup taxa. Resolving the phylogenetic position of P. hystricis and clarifying the relationship of Polytolypa and Spiromastix to Ajellomyces will require analyses of sequences of a greater number of coprophilous and geophilic onygenalean fungi. There is little question that a number of these "missing taxa" await discovery and formal description.

	TAXONOMY

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Ajellomycetaceae Untereiner, Scott & Sigler, fam. nov.

Type genus: Ajellomyces McDonough & Lewis, Mycologia 60:77. 1968

Ascomata gymnothecia, globosa vel irregulariter stellata, discreta vel aggregata, parva, pallide brunnea; appendices centraliter orientes ex ascogonio, contortae cum helicibus paucis ad compluribus, cum parietibus crassis, flavo-brunneae, leves; hyphae peridiales cum parietibus crassis; hyphae uniformes diametro, sinuosae vel forma inaequales et apud septum constrictae; asci solitarii, irregulariter dispositi, globosi vel subglobosi vel pyriformes, octospori, hyalini, evanescentes; ascosporae globosae vel oblatae, muricatae, hyalinae, foramina germinalia absunt; anamorphoses de aleurioconidiis vel arthroconidiis cum dehiscentia lytica.

Ascomata gymnothecia, discrete or aggregated, globose to stellate, small, tan; appendages arising centrally from ascogonium, thick-walled, coiled with few to several helices, yellowish brown, smooth; peridium composed of branched anatomizing hyphae; hyphae uniform in diameter and sinuous, or constricted at the septa and inflated centrally; asci solitary, irregularly disposed, globose, subglobose to pyriform, eight spored, hyaline, evanescent; ascospores hyaline, globose to oblate, muriculate, lacking germ pores; anamorphs aleurioconidia or irregular alternate arthroconidia with rhexolytic dehiscence.

	ACKNOWLEDGMENTS

 
We are indebted to Gary McNeely (Brandon University) for his suggestions for the improvement of this manuscript and to Michael H. Hertwig-Jaksch for assistance with the Latin diagnosis. Financing for this study was provided to the senior author in the form of an A.W. Mellon Postdoctoral Fellowship in Plant Systematics (Duke University, USA). Operating grants from the Natural Sciences and Engineering Research Council (NSERC) of Canada to Wendy Untereiner and to Lynne Sigler and a NSERC undergraduate research summer assistantship to Jason Bachewich are gratefully acknowledged.

	FOOTNOTES

 
Accepted for publication February 5, 2004.

¹ Corresponding author. E-mail: untereiner{at}brandonu.ca

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This Article Abstract Full Text (PDF) Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Untereiner, W. A. Articles by Angus, A. Search for Related Content PubMed Articles by Untereiner, W. A. Articles by Angus, A. Agricola Articles by Untereiner, W. A. Articles by Angus, A.