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Biodiversity

The white and black fungi of the Atacama

Yeasts in the Chilean desert exhibit resistance to ultraviolet radiation levels as high as those found on Mars

Life under extreme conditions: desert microorganisms have adapted to arid terrain and ultraviolet radiation

Eduardo CesarLife under extreme conditions: desert microorganisms have adapted to arid terrain and ultraviolet radiationEduardo Cesar

In August of 2012, during the final stage of the Biotechnology program at the Federal University of São Carlos in Araras, state of São Paulo, André Pulschen was about to find four species of thick-skinned fungi from rocks collected six months earlier from high on a volcano in the Atacama Desert of northern Chile. Using an instrument that simulates the environment of other planets in a laboratory associated with the University of São Paulo (USP), he identified two species of fungi—Exophiala sp., which form colonies whose black color derives from the pigment melanin, and Rhodosporidium toruloides, which accumulate in orange-colored colonies owing to the presence of carotene—that can resist ultraviolet (UV) solar radiation as high as levels withstood by the bacterium Deinococcus radiodurans, which is used as a model organism for studying the possibility of life on Mars. The environment on the Red Planet is as arid, and the UV radiation at levels as high, as those found in the Atacama Desert. Radiation levels this high are normally fatal to microorganisms and to humans.

Cryptococcus friedmanii and Holtermanniella watticus, two other species brought from the rock walls of the Sairecabur Volcano, showed high resistance to UV radiation—an intriguing finding since they are white and therefore devoid of pigments that provide UV protection. The four species had already shown high resistance at low temperatures, as evidenced by the fact that the two white specimens continued to multiply even after a few days at -6.5 degrees Celsius (ºC). Although scientists cannot yet explain how they resist temperature variation and intense levels of UV radiation without pigment, these fungi express impressive mechanisms for adapting to the world’s driest desert, where no such biodiversity was thought to exist.

Fungi from the volcano: Exophiala sp., R. toruloides, C. friedmanii and H. watticus

Eduardo CesarFungi from the volcano: Exophiala sp., R. toruloides, C. friedmanii and H. watticusEduardo Cesar

Anyone landing at the airport in Calama, a city of 150,000 situated in the Atacama Desert, is soon struck by the intense heat and blinding light that pervade the extremely flat, reddish landscape. On the way to San Pedro de Atacama, a town of 3,000 at an elevation of 2,400 meters that serves as the base for expeditions to the region’s rare lakes, salt flats and volcanos, it is hard to spot any sign of wildlife on this arid terrain nearly devoid of hills. Residents of San Pedro confirm visitors’ observations that there is little diversity of wildlife beyond the pink flamingos in the lakes fed by Andean ice melt, Andean pigeons that pursue tourists in search of food, shy lizards, or vicunas that feed on shoots of low grass in the upper regions.

The desert stretches out over 1,000 kilometers and hosts remarkable and as yet little known forms of microscopic organisms adapted to low water availability and temperatures that can vary between 50ºC in the daytime and -15ºC at night. In 2006, a team from the U.S. space agency NASA identified 12 genera of fungi that can live in the scorching terrain of the Atacama and produce spores—structures similar to seeds, which are dispersed by wind. Now, Brazilian and Chilean researchers have found— in rock cavities or rocky walls of a volcano at an elevation of nearly 6,000 meters—fungal varieties that exhibit a heretofore unexplained resistance to adverse situations.

The El Tatio geysers with scalding-hot steam spewing from the rocks

Eduardo CesarThe El Tatio geysers with scalding-hot steam spewing from the rocksEduardo Cesar

“The microhabitat inside the rocks can be conducive to colonization, survival and dispersal of microbial life,” says Luiz Henrique Rosa, a professor at the Federal University of Minas Gerais (UFMG). From collections taken in the Atacama at altitudes ranging from 746 to 5,047 meters, teams from UFMG, USP, the Brazilian Synchrotron Light Laboratory (LNLS) and the University of Antofagasta, Chile, identified 81 varieties of fungi capable of living in fissures or cavities in rocks similar to granite, in which the temperature may vary from -45 to 60ºC. “The fungi are thought to produce enzymes that enable them to utilize the minerals, moisture from dew and organic matter inside the rocks,” he notes. In 2013, a team from the United States and Spain presented evidence of bacteria from cavities in volcanic rocks known as rhyolites, collected from sedimentary rocks in Valle de la Luna [Moon Valley], a depression in the Cordillera de la Sal [Salt Mountains], near San Pedro de Atacama.

In addition to identifying the fungi—which are organisms formed of cells that have a nucleus and are therefore more complex than bacteria—the team from UFMG put them to work. In the laboratory, Vívian Gonçalves cultured the fungi from the desert rocks and examined the extracts they produced in the culture medium. Under Rosa’s guidance, she found 23 extracts that showed activity against fungi, viruses and protozoa that cause disease in humans. In 2014, she did chemical fractionation of the extracts in a laboratory at the U.S. Department of Agriculture and isolated two substances, alpha-linolenic acid and ergosterol-5 8-endoperoxide, that exhibited antimicrobial activity.

The Valle de la Luna: visible deposits of salt

Eduardo CesarThe Valle de la Luna: visible deposits of saltEduardo Cesar

Fungi on Mars?
Fungi representative of the genus Cladosporium, found in rocks at five different altitudes, were notable for their ability to adapt to different environments. Other teams had already found that at least one species, C. halotolerans, is able to live in places with a high salt concentration. Cladosporium appears as brown or black spots, indicative of an accumulation of melanin, which protects against the damaging effects of UV solar radiation. The two species of white fungi brought from the heights of the Sairecabur Volcano indicate, however, that pigments may not be essential. Other molecular mechanisms that have not yet been identified may be just as important as pigmentation in warding off the harmful effects of the UV radiation high on the volcano. “At 5,000 meters, exposed skin can burn easily due to the ultraviolet radiation from the sun,” says Pulschen, who is now working on his doctorate at the USP Chemistry Institute.

The extreme dryness and high incidence of UV radiation give the Atacama Desert an environment similar to that of Mars. For this reason, organisms resistant to these conditions attract scientists because they represent life forms that could survive away from Earth.  Douglas Galante, an expert on the subject who is currently at LNLS, supports the idea that the thick-skinned fungi of the Atacama volcano could survive on Mars, since the environmental conditions are very similar. He thinks that a search for present-day or ancient traces of more-complex organisms such as fungi, and not just of anucleated organisms such as the bacterium Deinococcus radiodurans, as is planned, could be considered in coming expeditions to the Red Planet, “This would expand the possibilities of finding extraterrestrial life.”

This year, the Brazilian team is planning to study the bacteria that live amidst rocks continuously washed by steam from the El Tatio geysers, 90 kilometers from San Pedro de Atacama at an elevation of 4,320 meters. Steam forms when water from underground rivers comes into contact with hot rocks and exits through fissures, at a temperature of about 100ºC, forming columns as high as 10 meters. Bacteria resistant to high temperatures apparently feed on inorganic matter released by the sulfur-rich rocks.

Scientific articles
GONÇALVES, V.N. et al. Fungi associated with rocks of the Atacama Desert: taxonomy, distribution, diversity, ecology and bioprospection for bioactive compounds. Environmental Microbiology (on-line). 2015.
PULSCHEN, A.A. et al. UV-resistant yeasts isolated from a high altitude volcanic area on the Atacama Desert as eukaryotics models for astrobiology. MicrobiologyOpen. V. 4, No. 4, p. 574-88. 2015.

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