Novel taxa of thermally dimorphic systemic pathogens in the Ajellomycetaceae (Onygenales)

Abstract

Recent discoveries of novel systemic fungal pathogens with thermally dimorphic yeast-like phases have challenged the current taxonomy of the Ajellomycetaceae, a family currently comprising the genera Blastomyces, Emmonsia, Emmonsiellopsis, Helicocarpus, Histoplasma, Lacazia and Paracoccidioides. Our morphological, phylogenetic and phylogenomic analyses demonstrated species relationships and their specific phenotypes, clarified generic boundaries and provided the first annotated genome assemblies to support the description of two new species. A new genus, Emergomyces, accommodates Emmonsia pasteuriana as type species, and the new species Emergomyces africanus, the aetiological agent of case series of disseminated infections in South Africa. Both species produce small yeast cells that bud at a narrow base at 37°C and lack adiaspores, classically associated with the genus Emmonsia. Another novel dimorphic pathogen, producing broad-based budding cells at 37°C and occurring outside North America, proved to belong to the genus Blastomyces, and is described as Blastomyces percursus.

Keywords: Ajellomycetaceae; Blastomyces; Emergomyces; Emmonsia; genomics; phylogeny.

Fig. 1

RAxML tree constructed from concatenated dataset including five regions: ITS, LSU, TUB, TEF3 and RP 60S L1. The genera and species that are subject of this analysis are shown in bold font and represented by all analyzed strains (Table 1). Multiple sequences of other species/genera are collapsed (represented by one strain that is: type or neotype, genome sequenced or key strain from yet undescribed species). Bootstrap support (BS) from RAxML > 70% (left) and Bayesian posterior probability (PP) >0.80 are given at the nodes. Fully supported branches (100/1) are depicted as black circles. (*) Formerly Emmonsia parva. (T) – Type strain.

Fig. 2

(A) Genome sizes in megabases (Mb) and total number of protein-coding genes of the sequenced and assembled strains of Emergomyces africanus, Es. pasteurianus and Blastomyces percursus, and other previously sequenced and assembled species from the Ajellomycetaceae. * formerly Emmonsia parva (B) Conservation of core eukaryotic genes (CEGs) across Es. africanus, Es. pasteurianus, B. percursus and other compared genomes.

Fig. 3

Phylogeny of Emergomyces africanus, Es. pasteurianus and B. percursus. Maximum likelihood tree inferred from concatenated protein alignments of 2,851 core genes based on 1,000 replicates; all nodes were supported by 100% of bootstrap replicates. Novel emergent species are highlighted with red color circles.

Fig. 4

Emergomyces africanus sp. nov., CBS 126360 (type strain). (A, B) Colony on MEA after 4 weeks at 24 °C, obverse and reverse. (C–I) Conidia of mycelial phase. (J–L) Small yeast cells at 37 °C. Scale bars = 10 μm.

Fig. 5

Blastomyces percursus sp. nov., CBS 139878 (type strain). (A, B) Colony on MEA after 4 weeks at 24 °C, obverse and reverse. (C–H) Conidia of mycelial phase. (I–K) Hyphal elements in transition to yeast-like growth at 37 °C. (L) Large yeast with unipolar or bipolar budding at a broad base at 37 °C. Scale bars = 10 μm.