Environmental Isolation of Candida auris from the Coastal Wetlands of Andaman Islands, India

Abstract

Candida auris is a multidrug resistant pathogen that presents a serious global threat to human health. As C. auris is a newly emerged pathogen, several questions regarding its ecological niche remain unexplored. While species closely related to C. auris have been detected in different environmental habitats, little is known about the natural habitat(s) of C. auris. Here, we explored the virgin habitats around the very isolated Andaman Islands in the Indian Ocean for evidence of C. auris. We sampled coastal wetlands, including rocky shores, sandy beaches, tidal marshes, and mangrove swamps, around the Andaman group of the Andaman & Nicobar Islands, Union Territory, in India. Forty-eight samples of sediment soil and seawater were collected from eight sampling sites representing the heterogeneity of intertidal habitats across the east and west coast of South Andaman district. C. auris was isolated from two of the eight sampling sites, a salt marsh and a sandy beach. Interestingly, both multidrug-susceptible and multidrug-resistant C. auris isolates were found in the sample. Whole-genome sequencing analysis clustered the C. auris isolates into clade I, showing close similarity to other isolates from South Asia. Isolation of C. auris from the tropical coastal environment suggests its association with the marine ecosystem. The fact that viable C. auris was detected in the marine habitat confirms C. auris survival in harsh wetlands. However, the ecological significance of C. auris in salt marsh wetland and sandy beaches to human infections remains to be explored. IMPORTANCE Candida auris is a recently emerged multidrug-resistant fungal pathogen capable of causing severe infections in hospitalized patients. Despite its recognition as a human pathogen a decade ago, so far the natural ecological niche(s) of C. auris remains enigmatic. A previous hypothesis suggested that C. auris might be native to wetlands, that its emergence as a human pathogen might have been linked to global warming effects on wetlands, and that its enrichment in that ecological niche was favored by the ability of C. auris for thermal tolerance and salinity tolerance. To understand the mystery of environmental niches of C. auris, we explored the coastal wetland habitat around the very isolated Andaman Islands in the Indian Ocean. C. auris was isolated from the virgin habitats of salt marsh area with no human activity and from a sandy beach. C. auris isolation from the marine wetlands suggests that prior to its recognition as a human pathogen, it existed as an environmental fungus.

Candida auris: Epidemiology, Diagnosis, Pathogenesis, Antifungal Susceptibility, and Infection Control Measures to Combat the Spread of Infections in Healthcare Facilities

“…The study thus succeeded in isolating C. auris for the first time from the tropical coastal environment, outside of the usual hospital environmental settings, suggesting its association with the marine ecosystem. Interestingly, the two isolates from the salt marsh area included a multidrug-susceptible and a multidrug-resistant C. auris while all 22 isolates from the beach site were resistant to multiple antifungal drugs [118]. Additionally, all the isolates grew at higher temperatures, however, the multidrug-susceptible isolate from the salt marsh grew slower than other isolates at both 37 • C and 42 • C [118].…”

“…Another study also proposed the aquatic environment as the natural habitat of C. auris, as it was used as a prey by two free-living amoebae and proliferated when exposed to protozoal supernatants [117]. Taking a cue from these observations, Arora et al [118] explored the tropical marine ecosystems around very isolated Andaman Islands, Union Territory of India in the Indian Ocean, and isolated several Clade I C. auris from two sites, the virgin habitat of salt marsh area with no human activity and from a sandy beach [118]. The study thus succeeded in isolating C. auris for the first time from the tropical coastal environment, outside of the usual hospital environmental settings, suggesting its association with the marine ecosystem.…”

“…Interestingly, the two isolates from the salt marsh area included a multidrug-susceptible and a multidrug-resistant C. auris while all 22 isolates from the beach site were resistant to multiple antifungal drugs [118]. Additionally, all the isolates grew at higher temperatures, however, the multidrug-susceptible isolate from the salt marsh grew slower than other isolates at both 37 • C and 42 • C [118]. Based on the isolation of C. auris from tropical marine ecosystems and the observation that one multidrug-susceptible isolate (from salt marsh) grew slower at mammalian temperatures than other environmental (or clinical) strains, Casadevall et al [119] have suggested that these findings provide an environmental source for clinical isolates and that the common ancestor of C. auris has likely adapted to higher temperatures recently.…”

The Consequences of Our Changing Environment on Life Threatening and Debilitating Fungal Diseases in Humans

“…C. auris is intrinsically resistant to most of the antifungals currently in clinical use and has a reported mortality rate of 33–72% [ 131 ]. Tracing of C. auris revealed the potential origin as the Indian subcontinent [ 132 , 133 ]. From here, it appears it spread rapidly, appearing simultaneously in Africa, South America and Asia [ 132 , 134 , 135 ].…”

New Technological Developments in Identification and Monitoring of New and Emerging Infections

“…Drug-resistant Candida auris has been associated with serious blood infections in hospitalized patients ( Prestel et al, 2021 ), but the likely source has not been known. Recently, ITS primers for fungal metagenomics were used to identify Candida auris in coastal wetlands of the Andaman islands ( Arora et al, 2021 ). It is not yet known, however, if these wetlands are the main natural reservoir of Candida auris .…”