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Atacama Desert Soil Microbiology

The Atacama Desert is an ancient temperate desert (mean annual temperature of 14–16°C) that extends across 1,000 km from 30°S to 20°S along the Pacific coast of South America (McKay et al. 2003; Fig. 6.1). As discussed by Rundel et al. (1991) and Miller (1976) the desert owes its extreme aridity to the climatic regime dominated by a constant temperature inversion due to the cool north- flowing Humboldt Current and the presence of the strong Pacific anticyclone.

The position of the Pacific anticyclone is generally stable with a small shift of a few degrees south in the summer (Trewartha 1961). Geological and soil mineralogical evidence suggests that extreme arid conditions have persisted in the Southern Atacama for 10–15 million years (Myrs; Ericksen 1983; Houston and Hartley 2003; Clarke 2006) making it one of the oldest deserts on Earth.

The driest parts of the Atacama Desert are located between approximately 22°S to 26°S in the broad valley formed by the coastal range and the medial range (the Cordillera de Domeyko) (Fig. 6.2). One of the most striking and unusual features of the Atacama Desert is the presence of large nitrate deposits . Early in the last century, nitrate mining operations were conducted in this area (Woodcock and Hill 1901), but, currently, there are no permanent human settlements in this hyperarid region.

Although nitrate deposits are found in many deserts, significant accumulations are found only in the Atacama. Current understanding suggests that the nitrate is of atmospheric (lightning) origin based on stable isotope evidence (as suggested by Böhlke et al. (1997) ) and that lightning-related nitrate production is not unusually intense over the Atacama.

What is unusual is that there are no removal mechanisms due to the lack of water activity and resultant lack of microbial denitrification. Over the history of the Atacama (10–15 Myr or more) the accumulation has resulted in large concentrated deposits. Within the driest part of the Atacama there exists a region with “Mars -like” soil s (Navarro-González et al. 2003).

There are three characteristics that make these soils Mars-like: first, there are very low levels of organic material and the organics that are present are refractory. They do not decompose at the temperatures reached by the Viking GCMS (500°C).

Second, there are very low levels of soil bacteria, and, in some locations, these are undetectable either by culture or DNA amplification (Navarro-González et al 2003), or by Limulus Amebocyte Lysate, a sensitive and specific assay to screen for the presence of endotoxin (lipopolysaccharide) from Gram-negative bacteria (M. Turnbull, personal communication). Third, the soil contains an oxidizing agent with the ability to oxidize at equal rates l- and d- amino acids, as well as l- and d- sugars. Soils to the south of the arid core region do not show these characteristics.

Atacama Soil Organics

Soil organicsare a mixture of recognizable biological material whose components have been altered to the degree that it no longer retains its original structural or chemical organization (Oades 1989). At any given time the amount of soil organics reflects the long-term balance between input and loss rates (Olson 1963).

The input of soil organics increases with mean annual precipitation and temperature, whereas their residence time decreases with mean annual precipitation and mean annual temperature (Lieth 1973; Amundson 2001). Soil organics are ultimately degraded to carbon dioxide through microbial respiration and abiotic processes (Bunt and Rovira 1954; Parsons et al. 2004). Organics in surface samples of Atacama Desert soils have been studied in detail using dry analytical methods, namely pyrolysis-gas chromatography-mass spectrometry (pyr-GC-MS) at atmospheric pressure in an inert atmosphere by Navarro-González et al. (2003).

Samples exposed to flash heating at 500°C in a He atmosphere revealed that the most arid zone of the Atacama, the Yungay area(~24°S) is depleted of organic molecules. At a higher temperature pyrolysis (750°C), only formic acid and benzene are detectable. In contrast, samples from less arid sites (28°S) release a complex mixture of organic compounds upon pyrolysis at 750°C (formic acid, propenenitrile, butadiene, butene, pentadiene, methylfuran, benzene, methylbenzene, benzenenitrile, ethylbenzene, dimethylbenzene, and styrene).

Isolation and Detection of Heterotrophic Bacteria

There is currently a limited amount of published information on the levels of heterotrophic bacteriaand their identity from the Atacama Desert. Studies to date have estimated that desert soil populationsranged from 0 to 107 colony-forming units per gram (CFU/g).

This wide range of values is not surprising considering the extent of the desert, the various levels of precipitation, as well as the chemical compositions and elevations of various sample sites. Apparent differences in population size might also correspond to differences in efficiency of the recovery methods used.

Population size estimates were obtained using both culture-dependent(Cameron 1969a,b; Navarro-González et al. 2003; Maier et al. 2004; Lester et al. 2007) and culture-independent approaches (Glavin et al. 2004; Drees et al. 2006). The culturedependent approaches which involve the growth of viable cells on artificial culture media are for the most part in agreement and conclude that the bacterial numbers contained within the soils from the most arid region of the Atacama are extremely low and in most cases close to or below the detection limit of the methods applied.

Cyanobacteria-Dominated Microbial Consortia

Liquid water is a paramount condition for life on our planet. Long-term mean annual rainfall in the Atacama Desert is only a few millimeters in its driest core (24°–25°S, 69–70°W) and increases with latitude (McKay et al. 2003). At this biotic extreme environment, desert pavement (surface soils mantled by gravels) is colonized by hypolithicor endolithicbacterial consortiaforming biofilmson or within rock substrates such as quartz (Warren-Rhodes et al. 2006), halite (Wierzchos et al. 2006), and gypsum (J. Wierzchos and B. Gómez-Silva, unpublished results), as has been reported in other hot and cold deserts (Friedmann 1982; Schlesinger et al. 2003).

The cyanobacterium Chroococcidiopsis sp. is the ubiquitous primary producer of these communities inhabiting porous and translucent stones which retain sufficient moisture and filter excessive solar radiation. Abundance of colonized stones correlates positively with the increase in the latitudinal rainfall gradient, as does microbial community diversity estimated on the basis of the recovery of 16S rRNA gene-defined genotypes (Warren-Rhodes et al. 2006).

At wetter sites, microbial consortia contain genotypes belonging to cyanobacteria (Chroococcidiopsis sp. and Nostoc sp.), Alpha- and Gammaproteobacteria , Acidobacteriales, and Phormidium. Based on radiocarbondata from hypolithic biofilms and soils, microbial activity shows a sharp decline from wetter sites (27°S, 70°W) to the driest site at Yungay (24°S, 70°W), with steady-state residence times of one year and over 3,000 years, respectively (Warren-Rhodes et al. 2006; Fig. 6.3).

At Yungay, a site with Mars-like soils (Navarro-González et al. 2003), cyanobacterial colonization of stones may be at least 12,000 years old, comparable to Antarctic cryptoendolithic consortia (Bonani et al. 1988). Across the latitudinal precipitation gradient, total organic carbon of hypolithic soils is five to fifteenfold greater than organic carbon of nonhypolithic surface soils (Warren-Rhodes et al. 2006).

Patchiness of Transition from High- to Low-Density Populations

As discussed above, the distribution of soil bacteria in the extreme arid core region of the Atacama has considerable variability. This is in contrast with the more uniform, and higher, density of soil bacteria in the wetter regions of the Atacama. The transition between bacteria-rich soils and Mars-like soils is not yet understood.

We have considered several possibilities: the transition could be gradual with the number of organisms and the concentration of organic material dropping off monotonically with the decrease in water availability; the transition could be sharp, analogous to a tree-line on a mountain slope; the transition could be patchy with ‘islands’ of bacteria-rich soil in otherwise Mars-like terrain. Preliminary data suggest that the transition is patchy .

Relevance to Exobiology

The Atacama Desert, one of the oldest and driest deserts on Earth, provides an analogue for life in dry conditions on early or present Mars. We have used this analogue to explore the limits of life under Mars-like conditions for heterotrophic bacteria (Navarro-González et al. 2003) and for phototrophic cyanobacteria (Warren-Rhodes et al. 2006). The core of the Atacama is the end member in mineralogical comparisons between Mars and Earth soils and represents soils that differ qualitatively from soils in wetter desert environments (Ewing et al. 2006).

Our biological and chemical results suggest that, if the Viking lander had landed in the arid core region of the Atacama, it would have been unable to detect any evidence of life. Indeed, the lander instruments would have produced results similar to what they produced on Mars.

 

Author: Benito Gomez-Silva, Fred A Rainey, Kimberley Warren-Rhodes, Christopher P. McKay

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