Nunzia Stivaletta And Roberto Barbieri

Dipartimento di Scienze della Terra e Geologico-Ambientali, Université di Bologna, Via Zamboni 67, 40126 Bologna, Italy

Abstract Microbial life in hot and cold desert environments inhabits endolithic niches. The endolithic microorganisms include bacteria, fungi and lichens. To protect themselves from the inhospitable conditions, such as high UV radiation, dryness, and rapid temperature variations, microorganisms migrate into fractures or in pore spaces where the necessary nutrient, moisture, and light are sufficient for survival. Examples of endolithic communities are well documented from the Negev Desert, Antarctica and the Artic regions, and the Atacama Desert. The most common substrates are porous, crystalline sandstones with calcium carbonate cements and sulfate (gypsum) and other evaporite mineral crusts. The detection of sulfate on the Martian surface has sparked off considerable interest in the astrobiological potential of the evaporite deposits of continental environments, which may potentially host (or may have hosted) endolithic microorganisms.

1. Introduction

Fossil endoliths are known in the rock record back to the Late Proterozoic. The oldest example of fossil endoliths occurs in silicified pisoids of the Eleonora Bay Formation in East Greenland that contain organically preserved cyanobacteria resembling Hyella gigas (Campbell, 1982; Knoll et al., 1986). Wierzchos and Ascaso (2002) for the first time documented the fossilization of cryptoendolithic microfossil communities in sandstones from a cold desert environment, the Ross Desert on Antarctica. Since extremely cold and dry sites may be considered terrestrial environmental analogues of Mars, the endolithic communities have remarkable astrobiological significance and can be expected in Martian surface and rocks (Wynn-Williams and Edwards, 2000; Wierzchos and Ascaso, 2002), in which strong limiting factors for life include the instability of superficial liquid water and the intense solar (UV) radiation.

Lithobionthic microbial life in terrestrial ecosystems can flourish on the rock surface (epiliths), at the rock-soil interface (hypoliths) and inside the rocks (endoliths). The endolithic mode of life includes several different ecological niches: chasmoendoliths live in cracks or fracture in rocks, euendoliths penetrate actively soluble carbonate and phosphate substrates and cryptoendoliths occupy pre-existing fissures and structural cavities in the rocks, such as the pore spaces between grain boundaries or spaces produced and vacated by euendoliths (Golubic et al., 1981). Endolithic strategies are performed by bacteria, fungi and lichens. Some microorganisms are partially epilithic and partially endolithic (e.g. lichens), whereas others penetrate carbonate substrates, as euendoliths, and colonize preexisting structural cavities (Golubic, 1981). Endolithic and hypolithic microorganisms inhabit regions where high ultraviolet radiation, aridity, and huge daily temperature range typify the environment, such as in deserts. In such inhospitable conditions, the endolithic microorganisms migrate into fractures or in pore spaces where the necessary nutrient, moisture, and light are sufficient for survival. Examples of endolithic communities have been described from the Negev Desert (Friedmann et al., 1967), Antarctic (Friedmann and Ocampo, 1976) and Artic regions (Omelon et al., 2006a) and the Atacama Desert (McKay et al., 2003; Wierzchos et al., 2006).

2. Microbial Life in Arid Environments

In arid environments microorganisms must be able to withstand rapid desiccation and high levels of ultraviolet radiation. The Atacama Desert (Fig. 1), the driest desert on Earth, represents a paradigmatic example that offers the possibility of testing the ability of microorganisms to survive in extremely dry conditions (Dose et al., 2001; Navarro-Gonzales et al., 2003; McKay et al., 2003; Maier et al., 2004; Drees et al., 2006; Warren-Rhodes et al., 2006; Wierzchos et al., 2006; Connon et al., 2007). The only inhabitants in hypersaline continental lakes of arid environments, such as sabkhas, are extremely halophilic organisms, including halophilic Archaea (halobacteria), halophilic cyanobacteria, and green algae (Grant et al., 1998). Invertebrates, such as the brine shrimp Artemia salina may locally be abundant. When waters approach saturation (30% NaCl), however, halobacteria, the most halophilic biota (Rodriguez-Valera et al., 1981), dominate.

In sites with limited or scarce water the microorganisms live either inside porous rocks (endolithic mode life) or below the translucent rocks partially embedded in the soil (hypolithic mode life), where they take advantage of the standing moisture just below the surface or between single grains or minerals. The extracellular polymeric substances (EPS), which are important for cell aggregation and protection, have also a beneficial role by reducing water loss of single cells (Potts, 1994; Gerdes, et al., 2000). Besides tolerating the desiccating conditions and extreme temperatures, microorganisms inhabiting mineral soils of hot and cold deserts are subjected to osmotic stress due to the high salt concentrations from accumulated sodium, calcium, magnesium, chloride, sulfate and nitrate; to prevent the loss of cellular water under high osmolarity in hypersaline conditions, halophiles generally accumulate high solute concentrations within cytoplasm (Madigan et al., 2003). The UV radiation flux of arid environments can also be lethal for microorganisms. Microbes are vulnerable to radiation, particularly at an

Figure 1. Atacama Desert (Chile). (A) Panoramic view of Laguna Chaxa (Salar de Atacama). Note the salt crusts due to the intense evaporation of the ephemeral water. (B) Endolithic microorganisms (arrow) beneath a salt crust in Laguna Chaxa.

early growth stage, when screening pigments have not yet been developed. These pigments help protect cells from the chemical damage of proteins, DNA and membranes (Cockell, 2000). For example, carotenoids (e.g., 5-carotene) absorb the UVA (320-380 nm) and the UVC radiations range (<280 nm), which are lethal to DNA that absorbs at 254 nm (Wynn-Williams et al., 2002).

In the Yungay area, located in the driest belt of the Atacama Desert, evaporite (halite) minerals have been recently found colonized by cyanobacteria identified as Chroococcidiopsis morphospecies and associated heterotrophic bacteria (Wierzchos et al., 2006).

This colonization is selective and seems to be dependent on the mineral composition of the particles that make up a given surface. In the case of halite, colonization occurs just a few millimeters beneath the surface between distinct halite crystals. The hygroscopic nature of halite, which retains water when the relative humidity of air is more than 70-75% (Wierzchos et al., 2003), appears to sustain microbial colonization. If the surface consists of quartz grains, however, no colonization has been observed beneath and between grains, as reported by McKay et al. (2003) on the basis of four years of climate observations in the Atacama Desert.

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