Molecular genetic variation in Emmonsia crescens and Emmonsia parva, etiologic agents of adiaspiromycosis, and their phylogenetic relationship to Blastomyces dermatitidis (Ajellomyces dermatitidis) and other systemic fungal pathogens

Abstract

Emmonsia crescens, an agent of adiaspiromycosis, Blastomyces dermatitidis, the agent of blastomycosis, and Histoplasma capsulatum, the agent of histoplasmosis, are known to form meiotic (sexual) stages in the ascomycete genus Ajellomyces (Onygenaceae, Onygenales), but no sexual stage is known for E. parva, the type species of the genus Emmonsia. To evaluate relationships among members of the putative Ajellomyces clade, large-subunit ribosomal and internal transcribed spacer region DNA sequences were determined from PCR-amplified DNA fragments. Sequences were analyzed phylogenetically to evaluate the genetic variation within the genus Emmonsia and evolutionary relationships to other taxa. E. crescens and E. parva are distinct species. E. crescens isolates are placed into two groups that correlate with their continents of origin. Considerable variation occurred among isolates previously classified as E. parva. Most isolates are placed into two closely related groups, but the remaining isolates, including some from human sources, are phylogenetically distinct and represent undescribed species. Strains of B. dermatitidis are a sister species of E. parva. Paracoccidioides brasiliensis and Histoplasma capsulatum are ancestral to most Emmonsia isolates, and P. brasiliensis, which has no known teleomorph, falls within the Ajellomyces clade.

FIG. 1

Phylogram representing one of the four equally parsimonious trees found in a heuristic search (PAUP 3.1.1) of the ITS1, ITS2, and 5.8S-plus-lsu rDNA sequence data. The aligned data set included 1,207 nucleotide positions for each of 43 strains. The sequence of Geosmithia lavendula was obtained from GenBank (AF033385) and was used to root the tree since this species has been phylogenetically placed among the perithecial ascomycetes (32). Unalignable segments of ITS1 and ITS2 were excised from the alignment before analysis. The number of steps between nodes is proportional to branch length, and a scale bar for 10 steps appears at the bottom. The number below each internode is the bootstrap value (1,000 replicates) for that node. Isolation data, colonial subgroups designated by roman numerals and based on growth rates and colonial features on potato dextrose agar after 28 days at 22°C (data from reference 40) and mating type (plus or minus) (40), when known, are listed to the right of the isolate numbers. B. dermatitidis isolates are a sister group to E. parva strains. E. parva strains form two phylogenetic groups closely related to B. dermatitidis. Three isolates from humans, previously identified as E. parva, are on distinct lineages and represent undescribed species. Isolates of E. crescens form a clade with two subgroupings. Strains in each subgroup were isolated from locales in Eurasia or North America. They may represent geographic variants or incipient species. Low bootstrap values on the basal branches leading to H. capsulatum and P. brasiliensis make the placement of these species in the tree equivocal. Two Emmonsia strains, UAMH 141 and UAMH 2304, previously identified as E. parva, branch basally in the tree and represent an undescribed species. HIV, human immunodeficiency virus.