UV ‐resistant yeasts isolated from a high‐altitude volcanic area on the Atacama Desert as eukaryotic models for astrobiology

Abstract

The Sairecabur volcano (5971 m), in the Atacama Desert, is a high-altitude extreme environment with high daily temperature variations, acidic soils, intense UV radiation, and low availability of water. Four different species of yeasts were isolated from this region using oligotrophic media, identified and characterized for their tolerance to extreme conditions. rRNA sequencing revealed high identity (>98%) to Cryptococcus friedmannii, Exophiala sp., Holtermanniella watticus, and Rhodosporidium toruloides. To our knowledge, this is the first report of these yeasts in the Atacama Desert. All isolates showed high resistance to UV-C, UV-B and environmental-UV radiation, capacity to grow at moderate saline media (0.75–2.25 mol/L NaCl) and at moderate to cold temperatures, being C. friedmannii and H. watticus able to grow in temperatures down to −6.5°C. The presence of pigments, analyzed by Raman spectroscopy, correlated with UV resistance in some cases, but there is evidence that, on the natural environment, other molecular mechanisms may be as important as pigmentation, which has implications for the search of spectroscopic biosignatures on planetary surfaces. Due to the extreme tolerances of the isolated yeasts, these organisms represent interesting eukaryotic models for astrobiological purposes.

ANaganishiain high places: functioning populations or dormant cells from the atmosphere?

“…Also relevant to the present study, Vimercati et al (2016) showed that the isolate from Volcán Llullaillaco (discussed below) forms a monophyletic clade with N. friedmannii based on long-read 18S environmental sequences (1739 bp, JX099190) from Llullaillaco (Lynch et al 2012). Likewise, the Naganishia isolate from Volcán Saírecabur studied by Pulschen et al (2015) showed 100% identity with N. friedmannii over a 599 bp region of the LSU rRNA gene.…”

“…are 25–33% higher than levels measured at lower elevation sites in the Atacama (Yungay, 948 m.a.s.l. ; Pulschen et al 2015). Also of relevance to this paper is the fact that the tephra soils on these high volcanoes are among the most oligotrophic soils or sediments yet studied.…”

“…Note the low pH values at these sites.Mountain(el. )elevationm.a.s.l.pH% C% N% H 2 OrefLlullaillaco60344.20.017<dl a 0.24Lynch et al 2012 63304.60.005<dl0.25Lynch et al 2012Saírecabur39815.4nd b ndndPulschen et al 2015 50474.3ndndndPulschen et al 2015Socompa52355.20.03<dl<dlCostello et al 2009 58205.10.06<dl3.4Solon et al 2017 60304.8ndnd0.67Solon et al 2017Navajo38784.50.850.0910.7King et al 2010 a below detection limits b not determined

10.1080/21501203.2017.1344154-F0001Figure 1.Map showing the location of the three volcanoes discussed in this paper. From south to north, microbial communities on Llullaillaco (6723 m) and Socompa (6051 m) have been studied extensively via culture-independent and culturing approaches (Costello et al

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“…soil-like environments on Earth are dominated by basidiomycetous yeasts in the former Cryptococcus albidus clade most closely related to Naganishia friedmannii (Costello et al 2009; Lynch et al 2012; Solon et al 2017). In addition, these same yeasts are fairly easy to isolate from soils at elevations from 5000 (Pulschen et al 2015) to over 6000 m.a.s.l. (Vimercati et al 2016) in the Atacama region.…”

“…These findings are somewhat surprising given the extreme dryness of these sites and the fact that they contain some of the lowest levels of total carbon (<0.03%) of any soil environment yet studied on Earth (Schmidt et al 2012). In addition, high elevation sites in the Atacama region have a thin atmosphere, extreme aridity, high levels of UV radiation, low pH values, and extreme diurnal freeze-thaw cycles (Schmidt 1999; Lynch et al 2012; Cabrol et al 2014; Pulschen et al 2015). This unique combination of environmental stressors makes these high-elevation sites ideal for studying the dry-cold limits to life on Earth, as well as offering one of the best Earth analogues for the surface and near sub-surface of Mars (Lynch et al 2012; Pulschen et al 2015).…”