Genomic characterization of Parengyodontium americanum sp. nov

Abstract

Modern genome analysis and phylogenomic methods have increased the number of fungal species, as well as enhanced appreciation of the degree of diversity within the fungal kingdom. In this context, we describe a new Parengyodontium species, P. americanum, which is phylogenetically related to the opportunistic human fungal pathogen P. album. Five unusual fungal isolates were recovered from five unique and confirmed coccidioidomycosis patients, and these isolates were subsequently submitted to detailed molecular and morphological identification procedures to determine identity. Molecular and morphological diagnostic analyses showed that the isolates belong to the Cordycipitaceae. Subsequently, three representative genomes were sequenced and annotated, and a new species, P. americanum, was identified. Using various genomic analyses, gene family expansions related to novel compounds and potential for ability to grow in diverse habitats are predicted. A general description of the genomic composition of this newly described species and comparison of genome content with Beauveria bassiana, Isaria fumosorosea and Cordyceps militaris shows a shared core genome of 6371 genes, and 148 genes that appear to be specific for P. americanum. This work provides the framework for future investigations of this interesting fungal species.

Keywords: Comparative genomics; Hypocreales; Opportunistic fungal pathogen; Parengyodontium americanum.

Figure 1.

Macro- and microscopic characteristics of monosporic cultures from atypical clinical isolates recovered from different diagnosed coccidioidomycosis cases. Macro-morphological characteristics of the isolates include an irregular, undulated and raised colony-type morphology after 2 weeks of incubation at 24°C on A) Malt Extract Agar, B) Potato Dextrose Agar and C) Oatmeal Agar. The microscopic characteristics of these isolates include narrow vegetative fertile hyphae that raise phialides and/or aphanophialides, usually verticillate, which are displayed either in pairs or solitary on a lateral stalk/stem (D-M). Conidia vary from elongated cylindrical to oval and the pictures are all scaled to 10 μm.

Figure 2.

Mating Type representation of P. americanum MAT1–1 locus compared to other Clavicipitaceae species. All three P. americanum isolates harbor the MAT 1-1-1 and MAT1-1-2 genes suggesting a heterothallic mating system, and gene organization is conserved.

Figure 3.

Phylogenomic Maximum Likelihood tree representing the evolutionary placement among Hypocrealean fungi based on 319 single orthologous clusters. The P. americanum isolates CA11, CA13 and AZ2 are placed in a monophyletic clade within the Cordycipitaceae family, apart from Beauveria bassiana, Isaria fumosorosea and Cordyceps militaris. Scales represents branch length equivalent to nucleotide substitutions per site.

Figure 4.

Gene gain and loss analysis of A) Pfam, B) CAZy and C) MEROPS homolog gene family sizes among P. americanum and other Clavicipitaceae species. The species tree was inferred based on phylogenomic analyses, and used to define the identification of gene expansions and contractions of the above mentioned functional categories. Bar plots related to each tree node represents the number of ancestral orthologues in each tree taxon position.

Figure 5.

Enriched GOSlim terms for biological process and molecular function in P. americanum genomes. The Gene Ontology terms were summarized by purging redundant GO terms that were deduced by orthologous searches coupled with semantic similarity-based scatterplots using the REVIGO platform (Supek et al., 2011).