Fungi between extremotolerance and opportunistic pathogenicity on humans

Abstract

Numerous agents of infections in humans and other mammals are found among fungi that are able to survive extreme environmental conditions and to quickly adapt to novel habitats. Nevertheless, the relationship between opportunistic potential and polyextremotolerance was not yet studied systematically in fungi. Here, the link between polyextremotolerance and opportunistic pathogenicity is shown in a kingdom-wide phylogenetic analysis as a statistically significant cooccurrence of extremotolerance (e.g. osmotolerance and psychrotolerance) and opportunism at the level of fungal orders. In addition to extremotolerance, fungal opportunists share another characteristic-an apparent lack of specialised virulence traits. This is illustrated by a comparative genomic analysis of 20 dothideomycetous and eurotiomycetous black fungi. While the genomes of specialised fungal plant pathogens were significantly enriched in known virulence-associated genes that encode secreted proteases, carbohydrate active enzyme families, polyketide synthases, and non-ribosomal peptide synthetases, no such signatures were observed in human opportunists. Together the presented results have several implications. If infection of human hosts is a side effect of fungal stress tolerance and adaptability, the human body is most likely neither the preferred habitat of such species, nor important for their evolutionary success. This defines opportunism as opposed to pathogenicity, where infection is advantageous for the species' fitness. Since opportunists are generally incapable of the host-to-host transmission, any host-specific adaptations are likely to be lost with the resolution of the infection, explaining the observed lack of specialised virulence traits. In this scenario opportunistic infections should be seen as an evolutionary dead end and unlikely to lead to true pathogenicity.

Analyzing indoor mycobiomes through a large-scale citizen science study of houses from Norway

“…a Relevant traits: osmotolerant fungi (O) [3,26], allergenic fungi (A) [27,28], skin-associated fungi (S) [29], and material-colonizing fungi (M) [3,30].…”

“…a Relevant traits: plant pathogenic fungi (P), rock-inhabiting fungi (R) and lichen-forming fungi (L) [26,31].…”

Phenotypes Associated with Pathogenicity: Their Expression in Arctic Fungal Isolates

“…Fungi can efficiently adapt to new conditions and environments. High adaptability and stress tolerance often correlate with increased potential for causing opportunistic infections [14]. However, the pathogenicity potential of polar fungi is very poorly understood, although they might include potentially pathogenic strains [15].…”

“…Such adaptations might increase their capacity to survive unexpected habitat shifts, including transitions into habitats associated with humans [16,17]. In fact, some polyextremotolerant fungi (as long as they can grow at elevated temperatures) have the potential to colonize complex organisms (plants or invertebrates) and even warm-blooded animals [14,18].…”

Gliotoxin, identified from a screen of fungal metabolites, disrupts 7SK snRNP, releases P-TEFb and reverses HIV-1 latency

“…Species belonged to 28 orders (43 families) of the fungal Kingdom. The majority were of ascomycetous affinity including ascomycetous yeasts (Saccharomycetales: four species), 12 were of basidiomycetous affinity including three basidiomycetous yeasts (Trichosporonales, Tremellales), and three species of lower fungi (Mucorales) (Gostinčar et al, 2018). Rationale for choice was the expected production of a wide array of metabolites, which are known to be more pronounced in fungi living in habitats with environmental stress After opening, contents of vials were taken up in 1 mL malt peptone and distributed on Malt Extract Agar (Oxoid) culture plates.…”