Genetic Relatedness versus Biological Compatibility between Aspergillus fumigatus and Related Species

Abstract

e Aspergillus section Fumigati contains 12 clinically relevant species. Among these Aspergillus species, A. fumigatus is the most frequent agent of invasive aspergillosis, followed by A. lentulus and A. viridinutans. Genealogical concordance and mating experiments were performed to examine the relationship between phylogenetic distance and mating success in these three heterothallic species. Analyses of 19 isolates from section Fumigati revealed the presence of three previously unrecognized species within the broadly circumscribed species A. viridinutans. A single mating type was found in the new species Aspergillus pseudofelis and Aspergillus pseudoviridinutans, but in Aspergillus parafelis, both mating types were present. Reciprocal interspecific pairings of all species in the study showed that the only successful crosses occurred with the MAT1-2 isolates of both A. parafelis and A. pseudofelis. The MAT1-2 isolate of A. parafelis was fertile when paired with the MAT1-1 isolates of A. fumigatus, A. viridinutans, A. felis, A. pseudoviridinutans, and A. wyomingensis but was not fertile with the MAT1-1 isolate of A. lentulus. The MAT1-2 isolates of A. pseudofelis were fertile when paired with the MAT1-1 isolate of A. felis but not with any of the other species. The general infertility in the interspecies crossings suggests that genetically unrelated species are also biologically incompatible, with the MAT1-2 isolates of A. parafelis and A. pseudofelis being the exception. Our findings underscore the importance of genealogical concordance analysis for species circumscription, as well as for accurate species identification, since misidentification of morphologically similar pathogens with differences in innate drug resistance may be of grave consequences for disease management.

Ecology of aspergillosis: insights into the pathogenic potency of Aspergillus fumigatus and some other Aspergillus species

“…Subsequent polyphasic taxonomic re‐examination of one of the isolates from that case (isolate CM 5623) suggested that it belonged to a novel species designated as A. felis , which also causes invasive aspergillosis in dogs and cats (Barrs et al ., ). Finally, a recently refined phylogeny placed isolate CM 5623 into a separate clade and justified the proposal of yet another new cryptic representative (designated as Aspergillus parafelis ) within the broadly circumscribed species A. viridinutans (Sugui et al ., ). Notably, A. parafelis and the closely related species, Aspergillus pseudofelis and Aspergillus pseudoviridinutans , which were also proposed as novel taxa in the same study, displayed reduced susceptibility to amphotericin B, itraconazole and voriconazole, and increased virulence in different animal models with respect to the type strain of A. viridinutans (Sugui et al ., ).…”

“…Finally, a recently refined phylogeny placed isolate CM 5623 into a separate clade and justified the proposal of yet another new cryptic representative (designated as Aspergillus parafelis ) within the broadly circumscribed species A. viridinutans (Sugui et al ., ). Notably, A. parafelis and the closely related species, Aspergillus pseudofelis and Aspergillus pseudoviridinutans , which were also proposed as novel taxa in the same study, displayed reduced susceptibility to amphotericin B, itraconazole and voriconazole, and increased virulence in different animal models with respect to the type strain of A. viridinutans (Sugui et al ., ). Two implications/consequences of this are: (i) the taxonomy of the genus Aspergillus is far from being settled; and (ii) clinicians require some basic knowledge on fungal taxonomy and the cryptic species concept, as these can have consequences for disease management.…”

“…Furthermore, some cryptic species such as A. parafelis and A. pseudofelis have shown successful mating under laboratory conditions with related species, including A. fumigatus (Sugui et al ., ). In any case, despite these few exceptions of promiscuous mating, interspecies crossings in the section Fumigati of genus Aspergillus are generally infertile, which suggests that most phylogenetically distinct species are also sexually incompatible (Sugui et al ., ).…”

“…Sequence analysis of the MAT loci has also proven useful according to several studies (e.g. Barrs et al ., ; Álvarez‐Pérez et al ., ; Sugui et al ., ). This said, a polyphasic approach which includes morphological, physiological, molecular, biochemical and ecological data is likely to be the most informative for resolving taxonomic differences (Samson et al ., , ).…”

Update from the Laboratory

“…Although usually distinguishable from other Aspergillus species, such as A terreus, A niger, and A flavus, based on morphologic and phenotypic characteristics, A fumigatus is a member of the section Fumigati, which consists of at least 51 phylogentically distinct species. 157 Discrimination between members of this section is difficult due to the morphologic instability but important because several species within this section are refractory to antifungal therapy. [158][159][160] Species identification cannot always be made, however, because isolates are not always recovered from patients with invasive disease.…”