Cryptic Speciation in the Cosmopolitan and Clonal Human Pathogenic Fungus Aspergillus Fumigatus

Abstract

Abstract. Microbes and other organisms smaller than one to a few millimeters in size are hypothesized to have global populations, in contrast to the geographically restricted ranges of larger organisms. However, fungi, which routinely have reproductive propagules no larger than 10 micrometers, challenge the generality of this hypothesis because recent studies have shown that globally distributed morphological species embrace two or more geographically restricted phylogenetic species. We used the concordance of gene genealogies to recognize phylogenetic species in the globally distributed opportunistic human pathogenic fungus, Aspergillus fumigatus. Based on DNA sequence data of five loci for each of 63 individuals collected from five continents, we have delineated two phylogenetic species in this single morphological species. Unlike all other fungi examined to date, both genetically isolated groups showed a global distribution with no evidence of a correlation between genotype and geographic location. Sexual reproduction has never been observed in A. fumigatus, but when the same data were used to explore the association of alleles at the five loci for one of the phylogenetic species, evidence was found to support recombination. The discovery of a cryptic species is medically relevant because different species are likely to differ in virulence or drug resistance. The discovery of a globally distributed A. fumigatus species clade highlights the need for ecological studies of the fungus to either document global dispersal or propose alternative mechanisms by which it persists as single, global phylogenetic population.

Clinical implications of globally emerging azole resistance in Aspergillus fumigatus

“…A previous study by Rydholm et al [70], analysing the genetic structure of A. fumigatus, suggested that A. fumigatus is cosmopolitan and randomly breeding across a global scale. A subsequent study, while confirming these aspects of the population genetic structure of A. fumigatus, also found evidence of a genetic barrier to gene flow, suggesting A. fumigatus contained two (or perhaps more) cryptic and morphologically identical species [68]. More recent studies have confirmed the occurrence of a separate sexual species, A. lentulus [71] and have hinted at the existence of further genetic diversity within A. fumigatus sensu stricto.…”

“…This cluster also contained three UK isolates, one isolate from The Netherlands, and only 1/20 isolates carrying the TR 34 /L98H allele compared with 15/20 for the non-Japanese clade (figure 2). This preliminary population genomics analysis suggests that Pringle et al [68] are correct and that cryptic and morphologically identical populations of A. fumigatus sensu stricto do occur, and that this genetic structure leads to substantial linkage disequilibrium for at least two important genetic markers, the mating types and azole-resistance alleles.…”

“…Aspergillus fumigatus is one of the most frequently occurring eukaryotes on the planet owing to its high prevalence as a saphrophyte on decaying plant matter; its airborne conidia are among the most numerous eukaryotes in air and soil samples [68]. The highly aerosolized and dispersive character of A. fumigatus has led to the hypothesis that it is a truly 'globalized' organism.…”

DNA barcode identification of lichen-forming fungal species in the Rhizoplaca melanophthalma species-complex (Lecanorales, Lecanoraceae), including five new species

“…2C; Leavitt et al 2011a;Leavitt et al 2013). Additionally, genealogical concordance among independent genetic markers can provide strong evidence that distinct clades represent reproductively isolated lineages among well-separated groups (Dettman et al 2003;Pringle et al 2005). Although different datasets and operational criteria may give conflicting or ambiguous results due to the multiple evolutionary processes associated with speciation, the use of multilocus sequence data and multiple empirical methods are known to establish robust species boundaries in many lichen-forming fungal lineages (reviewed in Lumbsch and Leavitt 2011).…”

Phylogenetic studies uncover a predominantly African lineage in a widely distributed lichen-forming fungal species

“…Further, the same strongly supported monophyletic clades -'A' and 'C' -were recovered in reciprocally monophyletic clades in the independent gene trees (data not shown) (Hudson and Coyne 2002). Presence of the same clades in different single-locus genealogies can be taken as strong evidence that the clades are reproductively and evolutionarily isolated lineages representing distinct species-level lineages (Dettman et al 2003;Pringle et al 2005;de Quieroz 2007). The relationships among the clades were well supported (Fig.…”