Ultraviolet radiation-induced limitation to epilithic microbial growth in arid deserts – Dosimetric experiments in the hyperarid core of the Atacama Desert

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Abstract

Experiments were conducted during November 2003 in the dry core of the Atacama Desert, Yungay, Chile to test the hypothesis that UV radiation, in environments where liquid water is not available, and thus enzymatic repair of UV-induced damage is inhibited, can prevent epilithic colonization. Novel dosimeters made from the cryptoendolithic, desiccation and radiation-resistant cyanobacterium Chroococcidiopsis sp. isolated from the dry Negev desert, Israel, showed that monolayers of this organism were killed within one day. The diurnal profile of microbial loss of viability was investigated with dosimeters of Bacillus subtilis, which similarly showed cell death within one day. Soil grains obtained from south of Yungay where liquid water is more abundant and transported to the hyperarid core showed killing of indigenous vegetative organisms within one day. Gypsum and mineral grain coverings of 1 mm were sufficient to prevent measurable UV-induced damage of Chroococcidiopsis and B. subtilis after 8 d exposure. These results show that under extreme desiccation and an ambient UV flux the surface of rocks can potentially be rendered sterile, but that millimetre thick mineral coverings can protect organisms from UV-induced killing, consistent with the observed patterns of lithophytic colonization in the Atacama Desert. These data further show that UV radiation can be an important limiting factor in surface biological rock weathering in arid regions.

Introduction

Ultraviolet (UV) radiation is known to be inimical to a diversity of biological processes [1], [2]; however, active biological repair allows cells, specifically those exposed to solar radiation on the surface, to reverse the effects of damage. These processes can only be active when liquid water is available. In extremely dry deserts of the world where liquid water is unavailable, or at least available rarely, one would hypothesise that the surface could be sterilized by UV radiation as UV-induced damage, in the absence of effective repair, would be cumulative, eventually exceeding the threshold of genome stability, causing cell death.

Organisms are known to be confined to protected microenvironments in extreme deserts [3], [4], [5], [6]. They can either grow as hypolithic organisms (under rocks) or endolithic organisms (either as cryptoendolithic organisms which grow within rock interstices, or as chasmoendolithic organisms which grow within macroscopic cracks [7]). In the Atacama desert specifically, the desiccation-resistant, radiation-resistant cyanobacterium, Chroococcidiopsis sp., is known to be a dominant member of the lithophytic microbial flora and has been characterised both in hypolithic environments under quartz stones [8] and as a cryptoendolithic colonist within gypsum outcrops [9].

An important scientific question is the extent to which UV radiation plays a role in confining microbial communities to the interior or underside of rocks in extremely dry deserts and what protection is afforded by available substrates. As well as yielding insights into the factors that control the colonization of rocky environments, this question may also contribute to an understanding of which stressors limit surface weathering of minerals in arid regions and thus the contribution of arid regions to global-scale silicate weathering in general.

To test the hypothesis that UV radiation can act as a physical selection pressure against epilithic colonization in dry deserts we carried out dosimetric and soil transplantation experiments in the dry core of the Atacama Desert, Chile.

Section snippets

Field location

Ultraviolet radiation measurements were made at Yungay (University of Antofagasta Research Station) in the hyperarid Atacama Desert (24°04′50′′S, 69°5′11′′W, elevation 900–1000 m). The region is characterised by pebble-covered desert pavement. Liquid water in this region is limited to infrequent rainfall events. Between 1994 and 1998 McKay et al. measured 2.3 mm of rainfall [10]. Heavy fog and dew can provide moisture to rock surfaces. During the period from November 1, 2001 to July 10, 2002

Biological dosimetry of UV radiation with Chroococcidiopsis sp. dosimeters

The dosimeters retained viability until 12:00 (Fig. 2). However at 14:00 the viability was dramatically reduced. A small number of colonies remained viable at all exposures after 12:00.

Biological dosimetry of UV radiation with B. subtilis dosimeters

Biological dosimetry (Table 1) shows that B. subtilis spores are completely killed within one day of exposure to ambient UV radiation. Two diurnal profiles are shown in Fig. 3. One conspicuous feature of the data is the presence of a skewed UV irradiance distribution. For example, on October 31, 58% of the

Discussion

Ultraviolet radiation is more likely to be a selection pressure against surface-dwelling (epilithic) microorganisms when it is imposed concomitantly with extreme desiccation which prevents active damage repair. In a previous investigation on the exposure of organisms to UV radiation in the Atacama Desert, Dose et al. [23] showed that after 90 min exposure the viability of B. subtilis spores was reduced to ∼4% and the viability of fungal conidia was reduced to below 25%. After four days viability

Acknowledgments

We would like to thank Petra Rettberg and Kerstin Scherer of the Institute of Aerospace Medicine, Radiation Biology, DLR, Germany for processing of the Bacillus subtilis biofilms. We thank Benito Gomez of the University of Antofagasta.

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