Adaptation to the extreme conditions of the Atacama Desert
Microbial activity is limited primarily by water stress, although other factors such as carbon limitation, high salinity, and UV irradiation may also impose constraints on life (Jones et al. 2018). For the Atacama Desert, the limiting factors for fungi growth in this seemingly hostile environment are manifold.
The Yungay region, at the hyper-arid core of the Atacama Desert, is nearly 60 km from the Pacific coast (24040 S, 69540 W; 1000 m of altitude). This region contains Mars-like soils and it is mostly devoid of rocks and pebbles (Navarro-Gonzalez et al. 2003).
Yungay is one of the driest areas of the region, based on more than a decade of continuous climate and moisture data collection (McKay et al. 2003; Navarro-Gonzalez et al. 2003; Robinson et al. 2015). In addition, Yungay contains a large field of evaporitic rocks (halites with [95% of NaCl), which are abundantly colonized by lithobiontic communities predominately comprised of cyanobacteria (Wierzchos et al. 2006).
Go´mez-Silva (2010) provided the first observations of epilithic meristematic fungi able to colonize halites under extreme desiccating conditions at this location. Further studies on the abundance of lithobiontic fungi at Yungay were carried out using twelve 25-m2 quadrats, randomly placed among the Yungay halite field, including a total of 1308 halite rocks, with an average of 109 halites per quadrat.
This survey indicated that only 0.7% of the halite rocks were colonized by epilithic fungi. Interestingly, the fragmentation of colonized halites demonstrated the presence of endolithic colonization as well as epilithic colonization.
Preliminary taxonomic identification of the meristematic inhabitants of Yungay halites showed that they belong to the genera Penicillium and Aspergillus. A second report on the presence of melanized fungi at the hyper-arid core of Atacama described the presence of aNeucatenulostroma species of gypsum-inhabiting fungus at a site approximately 45 km south of Yungay, and nearly 60 km from the Pacific coast (Culka et al. 2017).
Adaptation to high amounts of solar radiation can be observed through melanin accumulation. This seems to be one of the most evident adaptive strategies used by these Atacama extremotolerant fungi to tolerate highly desiccating conditions as well as high levels of solar radiation.
Melanins (eumelanin, pheomelanin, and allomelanins) are chemically stable pigments with antioxidative action against free radicals and peroxides. They also provide photoprotection against UV radiation and promote growth under highly saline conditions.
Diversity, occurrence, and distribution of fungi in the Atacama Desert
A number of factors influence diversity, occurrence, and distribution of fungi in the Atacama Desert, including salinity, UV radiation, water availability, and temperature. Rundel (1978) provided the first studies of fungi in the Atacama Desert comparing the occurrence of lichenized fungal species for the coastal Atacama region to the Baja California region of Mexico.
Lichenized fungi are one of the most common fungi present in extreme environments such as the Atacama Desert and represent a rich source of fungal diversity. Twenty-three specimens of lichenized fungi were collected at the Lauca National Park (18140 4000S, 69210 1400W, 2300–4500 m of altitude, ET climate according to Ko¨ppen classification, temperature average of 4.9 C, and precipitation average of 282 mm) and identified by Villar et al. (2005) using Raman spectroscopy.
These include six different species of the genera Acarospora, Candelariella, Rhizocarpa, Rhizoplaca, and Xanthoria. Follmann (2008) described two new species of lichenized fungi (Lecanographa azure and Roccellina ochracea) characterized as crustaceous, obligatory terricolous ecotypes, found among fog oases in the Atacama Desert.
Biotechnology of extremophiles fungi from the Atacama Desert
Fungal microorganisms are well known as producers of different and useful compounds for biotechnology. They have the metabolic pathways capable of synthesizing enzymes, proteins, polysaccharides, and other biologically active natural products. In recent years, the capability of extremophilic fungi to produce compounds for use in biotechnological processes has been increasing; however, bioprospecting studies on fungal communities from the Atacama Desert are scarce.
According to Santiago et al. (2011), the search for extremophile fungi may represent a useful strategy for finding new eukaryotic metabolic pathways and, consequently, compounds for biotechnological use. Gonc¸alves et al. conducted the first bioprospecting study for bioactive compounds from fungi associated with rocks of the Atacama Desert and included data on antimicrobial, anticancer, leishmanicidal, trypanocidal, and antiviral activities.
In this study, 28.3% of fungal extracts, including those produced by members of the genera Alternaria, Aspergillus, Fusarium, Hypoxylon, Neosartorya, and Penicillium displayed activity against at least one of the different targets screened. Twenty extracts showed activity against human breast cancer and some extracts displayed selective antimicrobial activities against S. aureus, Candida albicans, and dengue virus.
The extract of Penicillium chrysogenum showed antimicrobial activity and analyses by NMR spectroscopy and gas chromatography-flame ionization detection (GC-FID) demonstrated the presence of linoleic and linolenic fatty acids, as well as ergosterol endoperoxide. The a-linolenic fatty acid inhibited the growth of Cryptococcus neoformans and the ergosterol endoperoxide was active against methicillin-resistant Staphylococcus aureus.
The biological activity of fungal extracts from rocks of the Atacama Desert was also evaluated against Paracoccidioides brasiliensis, the agent responsible for paracoccidioidomycosis, a systemic human mycosis endemic in Latin America (Mendes et al. 2016). Among the extracts tested, Aspergillus felis demonstrated the best results, with a minimum inhibitory concentration (MIC) of 15.6 mg/mL against P. brasiliensis Pb18.
Following this result, A. felis was grown in five different types of culture media and extracted with various solvents to optimize its antifungal activity. The best result of MIC against P. brasiliensis was 1.9 LG/mL and did not show any cytotoxicity at the concentrations tested in normal mammalian cell (Vero) extract.
This particular sample was produced in potato dextrose agar culture and extracted with dichloromethane. Bioassay-guided fractionation using analytical C18RP-high-performance liquid chromatography allowed the identification of cytochalasins as the antifungal agents in the extracts from A.
Atacama Desert fungi: eukaryotic models for astrobiology studies
The existence of these communities of microorganisms able to survive under extreme conditions such as the Atacama Desert has led to ex-situ research on the
behavior of organisms under extra-terrestrial conditions. Thus, eukaryotic organisms, especially extremophilic fungi, are promising models for astrobiology
The yeasts Cryptococcus friedmannii, Exophiala sp., Holtermanniella watticus, and Rhodosporidium toruloides, isolated from the top layer of soil at Sairecabur volcano, were evaluated for resistance to UVB, UVC, and environmental-UVC radiation, as well as high NaCl concentrations, and high temperature (Pulschen et al. 2015).
Exophiala sp. and R. toruloides showed high resistance to UV-C and UV-B, with values similar to those shown by the bacteria Deinococcus radiodurans (Pulschen et al. 2015). Since the discovery of salt deposits on Mars, halotolerant has become an interesting subject of astrobiological studies (Osterloo et al. 2008). The yeast Holtermanniella Atticus was the most salt tolerant.
It was able to grow in 2.25 mol/L of NaCl. Additionally, H. Atticus and C. friedmannii were able to grow at – 3 and – 6.5 C, respectively, and at a maximum temperature of 25 C (Pulschen et al. 2015). These preliminary results suggest that the Atacama Desert may shelter fungal species that fulfill the requirements for a promising eukaryotic model for astrobiological studies.
Author: Iara F. Santiago . Vı´vian N. Gonc¸alves . Benito Go´mez-Silva . Alexandra Galetovic . Luiz H. Rosa