High-Up: A Remote Reservoir of Microbial Extremophiles in Central Andean Wetlands

Abstract

The Central Andes region displays unexplored ecosystems of shallow lakes and salt flats at mean altitudes of 3700 m. Being isolated and hostile, these so-called "High-Altitude Andean Lakes" (HAAL) are pristine and have been exposed to little human influence. HAAL proved to be a rich source of microbes showing interesting adaptations to life in extreme settings (poly-extremophiles) such as alkalinity, high concentrations of arsenic and dissolved salts, intense dryness, large daily ambient thermal amplitude, and extreme solar radiation levels. This work reviews HAAL microbiodiversity, taking into account different microbial niches, such as plankton, benthos, microbial mats and microbialites. The modern stromatolites and other microbialites discovered recently at HAAL are highlighted, as they provide unique modern-though quite imperfect-analogs of environments proxy for an earlier time in Earth's history (volcanic setting and profuse hydrothermal activity, low atmospheric O2 pressure, thin ozone layer and high UV exposure). Likewise, we stress the importance of HAAL microbes as model poly-extremophiles in the study of the molecular mechanisms underlying their resistance ability against UV and toxic or deleterious chemicals using genome mining and functional genomics. In future research directions, it will be necessary to exploit the full potential of HAAL poly-extremophiles in terms of their biotechnological applications. Current projects heading this way have yielded detailed molecular information and functional proof on novel extremoenzymes: i.e., DNA repair enzymes and arsenic efflux pumps for which medical and bioremediation applications, respectively, are envisaged. But still, much effort is required to unravel novel functions for this and other molecules that dwell in a unique biological treasure despite its being hidden high up, in the remote Andes.

Keywords: astrobiology; central andes; extremophiles; genomes; microbe; microbialites; stromatolites.

Figure 1

The HAAL ecosystem. (A) Geographical location of HAAL (modified from Google Earth). Names are abbreviated as shown on Table 1. Locations not abbreviated include more than one lake from the table. Symbols indicate country of origin: Stars: Peru; Squares: Bolivia; diamonds: Chile; circles: Argentina. (B–E): Typical landscape of selected HAAL. (B) Lake Verde, Catamarca (4100 m); (C) Ojos de Mar Tolar Grande, Salta (3600 m); (D) Ojos de Campo Antofalla (3350 m); (E) Laguna Socompa (3570 m).

Figure 2

(A) Mean daily total solar irradiance (in W m⁻²), adapted from NASA MERRA Monthly History Data Collections (2D); (B) Mean local noontime UV Index over the Earth's surface (adapted from NASAOMI/Aura Online Visualization and Analysis, Daily Level 3 Global Gridded Products) http://gdata1.sci.gsfc.nasa.gov, with the region under study highlighted in the left map. Data were obtained by model calculations of spectral solar irradiances employing the SMARTS (version 2.9.5) algorithm developed by Gueymard (1995) together with NASA satellite measurements of climatic variables on selected DCA microbial hotspots (Table 1): i.e., Llullaillaco salar, named LLUS in the map, (6034 m), S. Llamará, Puquio2, named SLLA2 in the map, (800 m) and S. Pocitos, named SP in the map, (3660 m). Since the temperature variation with altitude is about −0.65°C each 100 m of increase (http://eo.ucar.edu/webweather/basic5.html), the indetermination due to the difference in altitude is insignificant.

Figure 3

Leaf Area Index (LAI) (in m² m⁻²) in the decade 2000–2009 for all the Earth (right) and on the Puna of Atacama region (left) with LAI in the range of (0.39 ± 0.27) m² m⁻². For this graphic selected HAAL were highlighted (Table 1): i.e., lakes situated at altitudes equal or greater than 4000 m (L_high): LAP, LN, LVE, LA, LD, LV, and SSM (white stars) and lower than 4000 m (L_low): OCA, SG, LS, OMTG, SLLU, and SP (yellow stars). Adapted from NASA MERRA Monthly History Data Collections (2D) http://gdata1.sci.gsfc.nasa.gov/.

Figure 4

(A) Monthly averaged air temperature at 2 m above the surface (solid symbols) and skin temperature (open symbols). The skin temperature is of interest since the microorganisms are normally fixed to soil surface. (B) Daily temperature range for S. Pocitos hotspot (in red) and low-altitude site (in green). (C) Daily mean relative humidity. (D) Monthly averaged precipitation. In both figures, red dots denote S. Pocitos hotspot (3360 m) and green stars to a low-altitude site (87 m) in a similar latitudinal region for comparison. Horizontal lines denote the annual mean values for each case. Adapted from SSE/NASA (http://eosweb.larc.nasa.gov/sse).

Figure 5

Cooperative microbial communities at the HAAL. (A) Microbial mat in L. Vilama; (B) L. Negra; (C) Hydrothermal vent with mat near L. Socompa; (D) Evaporitic Mat at S. de Llamará; (E) L. Tebenquiche (Salar de Atacama); (F) Microbialite from L. Diamante; (G) L. Socompa; (H) Socompa stromatolite vertical section; (I) Scanning Electron Microscopy (SEM) image of Socompa stromatolites, showing diatoms and crystals agglutinated by organic structures.

Figure 6

Phylogenetic tree from 138 16S rRNA gene partial sequences from HAAL strains and 202 type strains from RDP (Supplementary File S1). The tree was built using methods implemented in QIIME 1.5.0 (Caporaso et al., 2010b). The sequences were aligned using PyNAST aligner (Caporaso et al., 2010a) and the model 16S rRNA genes Greengenes alignment (McDonald et al., 2012). The alignment was filtered and a maximum likelihood tree was constructed using Fasttree (Price et al., 2010). Sequences with low homology to type strains are highlighted by a dot.