Fungal diversity in the Atacama Desert

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Diversity, occurrence, and distribution of fungi in the Atacama Desert

The Atacama Desert is an ancient temperate hyperarid desert, which runs nearly 1000 km along the Pacific coast of South America from 30S to 20S. This region has an annual mean temperature of 14–16 C with an increase in precipitation along the North-to-South latitude gradient (McKay et al. 2003).
Its extreme aridity can be attributed to the constant temperature inversion caused by the cool, northflowing Humboldt Current and the presence of the strong Pacific anticyclone (Rundel et al. 1991; Clarke 2006). Several studies on microbes living in extreme conditions such as those found in the Atacama Desert have been conducted over the last few years.

The Atacama Desert is a natural laboratory for conducting studies on microbial diversity. Indeed, Atacama is a hotspot for extremophiles and extremotolerant 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 colonised by epilithic fungi (Fig.a).

Interestingly, fragmentation of colonised halites demonstrated the presence of endolithic colonization as well as epilithic colonization (Fig.b). 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 melanised 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 microorganisms where the chemical and physical limits for life may be studied. Fungi are a diverse and ubiquitous group of microorganisms present in virtually all environments of the planet (Blackwel 2011).

However, the diversity and richness of fungi seem to range according to biotic and abiotic parameters, depending mainly on the availability of organic matter and liquid water. In extreme environments, such as those present in the Atacama Desert, we find rare and unique fungal species and strains with special morpho-physiological and genetic characteristics that allow them to tolerate conditions such as high temperatures, low availability of water and nutrients, and exposure to high levels of UV radiation. Despite the few mycological studies in the Atacama Desert, fungal species of Ascomycota and Basidiomycota have been studied in their respective ecosystems, with predominance of Ascomycota (Conley et al. 2006; Azua-Bustos et al. 2012; Ortiz et al. 2014; Gonc¸alves et al. 2016; Pulschen et al. 2015; Gonza´lez-Teuber et al. 2017; Martinelli et al. 2017). In this review, we present information on the diversity, ecology, adaptive strategies, and biotechnological potential of the fungi of the Atacama Desert.

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 colonised by lithobiontic communities predominately comprised of cyanobacteria (Wierzchos et al. 2006). Go´mez-Silva (2010) provided the first observations of epilithic tolerate highly desiccating conditions as well as high levels of solar radiation. Melanins (eumelanins, pheomelanins, 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 (Gessler et al. 2014).

An instructive parallel between halites and quartz rocks as the two lithic habitats for microbial life indicates that Yungay halites are an appropriate shelter for epilithic and endolithic communities and hypolithic colonization of quartz rocks is favoured at environments that are more humid. Low water availability has a negative impact on prokaryotic lithobionts under desiccating conditions as observed at Yungay. Less than 0.1% of the total quartz rocks surveyed at Yungay showed evidence of hypolithic colonization. However, this type of colonization increased to nearly 38% in quartz fields near Copiapo´ (27010 S, 70170 W), along an increasing north tosouth rainfall gradient (Warren-Rhodes et al. 2006). Endoliths obtain liquid water from atmospheric water vapour by NaCl-dependent deliquescence and capillarity condensation mechanisms (Wierzchos et al. 2006; Davila et al. 2008; Wierzchos et al. 2012). Given that eukaryotes are more complex but retain a lower genomic plasticity than prokaryotes, eukaryotic life is less suited to colonise habitats under the severe limitations imposed by the extreme desiccating conditions and high solar radiation found at Yungay. \Not surprisingly, fungal abundance and diversity increased in habitats without limitations of liquid water availability, such as hypersaline waters and mats (Edgcomb and Bernhard 2013).

Particularly interesting is the case of Salar de Llamara, a non-fossil salt flat (21230 S, 69370 W; 800 m altitude) that extends inland from the eastern slopes of the coastal range into the Atacama central depression. Here, the mean relative humidity is approximately 1.4 times higher than that of Yungay (De los Rı´os et al. 2010), as a consequence of the evaporation of small water bodies within Llamara and the recurrent inflows of oceanic fog events. Llamara microbial mats represent habitats where liquid water availability and solar radiation are no longer limiting factors for survival.

In fact, the presence of fungi at Llamara was demonstrated by culture-independent methods in samples obtained from the deeper and hotter mats at one of the Llamara ponds. Analysis of these samples showed that that 60% of the eukaryotic rRNA sequences retrieved belonged to the phylum Ascomycota (Saghaı¨ et al. 2017). Based on our current work, we have detected and isolated an orange-red member of the genus Fusarium from the Llamara mats (Fig.). This fungus is halotolerant and can grow optimally in Czapeck medium supplemented with 2% NaCl. Gessler et al. (2014) reviewed fungal tolerance to high salinity. Temperature, nevertheless, becomes a critical environmental stressor to microbial communities inhabiting Llamara mats, making these mats a potential source of thermotolerant and thermophilic fungi.

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 lichenised fungal species for the coastal Atacama region to the Baja California region of Mexico. Lichenised 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 (Table).

lichenised fungal species along two altitudinal transects at Alto Patache, with Amandinea efflorescens, Diploicia canescens, Myriospora smaragdula, and Rhizocarpon simillimum reported as new species. The majority of studies on non-lichenised fungi from the Atacama Desert have employed culturebased methodologies. Table 2 includes all fungi recovered at different locations and substrates from the Atacama Desert. The first study that reported fungi from Atacama Desert was published by Cameron et al. (1965), which found Penicillium propagules in soil near Antofagasta (24370 000S, 69320 000W, BWk climate according to Ko¨ppen classification, temperature average of 17.9 C, and precipitation average of 1 mm). Later, Conley et al. (2006) reported the first study on fungi recovery from the Atacama Desert that was focused on the search of nematodes and followed a protocol similar to that employed by NavarroGonzalez et al. (2003). Their unsuccessful search for

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 lichenised fungi (Lecanographa azurea and Roccellina ochracea) characterised as crustaceous, obligatory terricolous ecotypes, found among fog oases in the Atacama Desert. Microbial communities likely play dominant roles in the ecological processes of desert ecosystems (Makhalanyane et al. 2015). Few studies have been conducted on the functional ecological role of fungi from the Atacama Desert, and what we propose about the behaviour of fungi in this environment is derived from studies undertaken in other parts of the world or studies of species that have already been reported to be present in the Atacama Desert.

Author: F. Santiago . Vı´vian N. Gonc¸alves . Benito Go´mez-Silva . Alexandra Galetovic . Luiz H. Rosa