Urban Fungi Exhibit Thermal Adaptation Signs

Johns Hopkins Bloomberg School of Public Health

A new study from researchers at the Johns Hopkins Bloomberg School of Public Health finds that common fungal species may be adapting to higher temperatures in warmer sites within cities compared to cooler sites in the same city.

The findings could signify that urban fungi could one day evolve into disease-causing pathogens. The researchers note that this is a proof-of-principle study, designed to investigate whether fungal species may adapt differently across sites within the same city. While the new findings suggest that they might, the researchers emphasize that more studies, with more samples in different cities, are needed.

Fungi are primarily molds and yeasts that typically can't survive at warmer temperatures such as the body temperature of people, and only a minuscule subset of fungi can cause diseases. Many scientists worry that the warming climate may be driving fungi to adapt to rising temperatures, opening the door to new fungal pathogens that could survive in humans. One such fungal pathogen, Candida auris, a yeast first isolated from a human patient in 2009, now causes thousands of infections annually in the U.S. alone.

Fungal infections such as C. auris are often multi-drug resistant, with high mortality rates. C. auris has unusual tolerance for higher temperatures. Study senior author Arturo Casadevall , MD, PhD, MS, the Alfred and Jill Sommer Professor and Chair of the Bloomberg School's Department of Molecular Microbiology and Immunology, and others have argued that C. auris may have acquired this "thermotolerance" only recently, due in part to global warming.

Given cities are at greater risk for extreme heat, the researchers examined urban fungi for signs of heat adaptation. For their study, the researchers gathered samples using taffy-like candy to grab microbes from sidewalks from four different sites in Baltimore—a warm site, an above-average-temperature site, an average-temperature site, and a cool site.

The researchers found that fungal species isolated from relatively warm sites in Baltimore had lighter pigmentation, a trait that prevents overheating and signals possible adaptation to warmer temperatures.

The research team also found that fungal species isolated from warmer sites had greater resistance to heat exposure in a laboratory setting compared to the same species isolated from cooler sites.

The study was published online October 4 in ISME Communications.

"This study opens the door for future research into these adaptations and the identification of urban fungal species that may emerge as potential human pathogens in the near future," says study first author Daniel Smith, PhD, a postdoctoral student in the Bloomberg School's Department of Molecular Microbiology and Immunology. Smith is a member of the Casadevall laboratory.

Fungi can develop specific adaptations to help them survive in different climates by producing more heat-absorbing melanin pigmentation when they live in colder latitudes, as the Casadevall laboratory found in a 2018 study.

In the new study, the researchers looked for similar differences in fungal species isolated from warmer versus cooler places, this time within the same city.

Smith selected the four sites based on high-resolution temperature data from the National Oceanic and Atmospheric Administration and confirmed them by measuring dirt and sidewalk temperatures directly at the time of collection. After collection, he cultured the captured fungi and recorded their levels of pigmentation and their abilities to survive brief heat exposure above 55 degrees Celsius/131 degrees Fahrenheit.

The resulting data showed that molds and yeasts from the warmest site had significantly less pigmentation—and absorbed less heat experimentally—compared to molds and yeasts from the coolest site. Many fungal species also were more likely to remain viable after heat exposure if they had been sampled from one or both warm sites compared to cooler sites.

The dozens of species collected for analysis included fungi known to cause diseases. The species with apparent heat adaptations included some that are capable of causing disease in humans. The warmest-site isolate of Rhodotorula mucilaginosa, a common environmental yeast but rare human pathogen was more viable after heat exposure compared to the three isolates of this species from the coolest site. An isolate of another occasionally-pathogenic fungus, Cystobasidium minutum, isolated from a 38.4 Celsius/101 degrees Fahrenheit sidewalk, showed the greatest resistance to experimental heat stress, and was able to grow at 37 degrees Celsius/98.6 degrees Fahrenheit—human body temperature.

The researchers said they expect that the same type of study in other cities would yield similar results—with the caveat that further research is needed. The researchers note that the study has limitations, including variables such as sun exposure, foot traffic, and wildlife.

"These findings are consistent with the idea that high temperatures in an urban environment can induce fungal heat adaptations, thus narrowing the thermal barrier to human infection," Casadevall says. "These data are preliminary, and we need more and larger studies of this kind to help us understand how fungi are adapting to rising temperatures."

" Environmental fungi from cool and warm neighborhoods in the heat-island of Baltimore City show differences in thermal susceptibility and pigmentation " was co-authored by Daniel Smith, Madhura Kulkarni, Alexa Bencomo, Tasnim Syakirah Faiez, J. Marie Hardwick, and Arturo Casadevall.

Support for the research was provided in part by the National Institutes of Health (AI162381, AI152078, HL059842, AI168539, AI183596).

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