Cryptococcus neoformans Mates on Pigeon Guano: Implications for the Realized Ecological Niche and Globalization

Abstract

The ecological niche that a species can occupy is determined by its resource requirements and the physical conditions necessary for survival. The niche to which an organism is most highly adapted is the realized niche, whereas the complete range of habitats that an organism can occupy represents the fundamental niche. The growth and development of Cryptococcus neoformans and Cryptococcus gattii on pigeon guano were examined to determine whether these two species occupy the same or different ecological niches. C. neoformans is a cosmopolitan pathogenic yeast that infects predominantly immunocompromised individuals, exists in two varieties (grubii [serotype A] and neoformans [serotype D]), and is commonly isolated from pigeon guano worldwide. By contrast, C. gattii often infects immunocompetent individuals and is associated with geographically restricted environments, most notably, eucalyptus trees. Pigeon guano supported the growth of both species, and a brown pigment related to melanin, a key virulence factor, was produced. C. neoformans exhibited prolific mating on pigeon guano, whereas C. gattii did not. The observations that C. neoformans completes the life cycle on pigeon guano but that C. gattii does not indicates that pigeon guano could represent the realized ecological niche for C. neoformans. Because C. gattii grows on pigeon guano but cannot sexually reproduce, pigeon guano represents a fundamental but not a realized niche for C. gattii. Based on these studies, we hypothesize that an ancestral Cryptococcus strain gained the ability to sexually reproduce in pigeon guano and then swept the globe.

Cryptococcus neoformans isolation from swallow (Hirundo rustica) excreta in Iran

“…Our observation is consistent with the findings of previous investigations that reported the predominance of C. neoformans in avian excreta 14,15,19,22 .…”

ANaganishiain high places: functioning populations or dormant cells from the atmosphere?

“…For example, Cryptococcus gatti was traditionally considered to be restricted to tropical and subtropical climates; however, there is increasing evidence that it can be dispersed via the atmosphere even to colder areas such as the Northwest USA (Kidd et al 2004; Byrnes et al 2010). Other investigations into the ecological niches of these opportunistic pathogens have revealed a global distribution (Chen et al 2014) often associated with reservoirs such as guano (Nielsen et al 2007), Eucalyptus trees (Ellis and Pfeiffer 1990a), and Cassia trees (Lazera et al 2000; Granados and Castañeda 2005). Furthermore, air sampling in Australia during the flowering season of Eucalyptus camaldulensis contained C. gattii (Ellis and Pfeiffer 1990b) as did air samples collected after tree-cutting activities in Canada (Kidd et al 2007).…”

“…For most pathogenic Cryptococcus species, sexual spores are only known to be produced in the laboratory and have not been found in nature or in clinical samples (Velagapudi et al 2009); however, Nielsen et al (2007) found that Cryptococcus neoformans can mate on pigeon guano. To our knowledge, no extremophilic members of the genus Naganishia are known to have a sexual stage (Barnett et al 2000), but this could just be because the source habitat (reservoir) for this group has not yet been discovered.…”

Mating Pheromone in Cryptococcus neoformans Is Regulated by a Transcriptional/Degradative “Futile” Cycle

“…Asparagine minimum selective medium for transformant selection and for detection of laccase production was previously described (22). V8 juice and pigeon guano medium were used for mating assays as described (3,23).…”

“…Cryptococcus neoformans is a yeastlike basidiomycete human pathogen that undergoes a dimorphic transition to hyphal filamentous growth during the sexual cycle, which, in the environment, robustly occurs in a specialized niche of pigeon guano (3) as well as on plant surfaces (4). Stimulated by plant phytochemicals, sexual reproduction is believed to be important to the initiation of infections by virtue of the production of infectious spores (4 -6).…”