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Facilitation of endolithic microbial survival in the hyperarid coreof the Atacama Desert by mineral deliquescence Alfonso F. Davila, 1 Benito Go´mez-Silva, 2 Asuncio´n de los Rios, 3 Carmen Ascaso, 3 Hector Olivares, 2 Christopher P. McKay, 1 and Jacek Wierzchos 4 Received 24 July 2007; revised 12 November 2007; accepted 21 December 2007; published 27 March 2008. [ 1 ] The hyperarid core of the Atacama Desert is considered the dry limit for life onEarth. Soils in this region have very low abundance of heterotrophic bacteria and are practically barren of photosynthetic microorganisms because of the extreme dryconditions ( 2 mm a 1 rainfall). However, relatively abundant endolithic communities of cyanobacteria ( Chroococcidiopsis ) occur within halite crusts in paleolake evaporiticdeposits. By means of continuous monitoring of the microclimate conditions(temperature, relative humidity, water vapor density, wetness, and photosyntheticallyactive radiation) inside and around the halite crusts, we demonstrate here that water vapor condenses within the pore space of the halite at relative humidity (RH) levels that otherwise hinder the occurrence of liquid water in the surrounding environment. Water condensation occurs at RH >75%, which corresponds to the deliquescence point of halite.We have estimated a total of 57 deliquescence events (i.e., water condensation) withinthe halite crusts, as opposed to only 1 liquid water event outside. These wet eventsresulted in a total of 213.8 h of potential photosynthetic activity for the endolithicmicroorganisms versus only 6 h for organisms outside the halite crusts. Halite crusts maytherefore represent the last available niche for photosynthetic activity in extreme aridenvironments on Earth. Citation: Davila, A. F., B. Go´mez-Silva, A. de los Rios, C. Ascaso, H. Olivares, C. P. McKay, and J. Wierzchos (2008), Facilitationof endolithic microbial survival in the hyperarid core of the Atacama Desert by mineral deliquescence, J. Geophys. Res. , 113 , G01028,doi:10.1029/2007JG000561. 1. Introduction [ 2 ] The Atacama Desert (Chile) ranks as the driest desert on Earth, with long-term mean annual rainfall as low as afew millimeters in its driest zone [ McKay et al. , 2003].Heterotrophic bacteria are virtually absent in soils from thishyperarid region [ Navarro-Gonza´lez et al. , 2003] and arealso highly depleted in organic molecules partially becauseof nonbiological oxidation processes [ Navarro-Gonza´lez et al. , 2003; L. E. Fletcher et al., Variability of organicmaterial in the hyperarid soils of the Atacama Desert,submitted to Journal of Geophysical Research , 2006]. Evenhypolithic cyanobacteria, found in hyperarid stony deserts,are extremely rare in the hyperarid core of the AtacamaDesert and exist in small spatially isolated islands amidst amicrobially depleted soil [ Warren-Rhodes et al. , 2006].The absence of soil and hypolithic bacteria is due to theextremely low availability of liquid water, which almost exclusively arrives in the form of fog and dew [ Warren- Rhodes et al. , 2006]. While the Antarctic Dry Valleysrepresent a cold extreme for microbial physiology and the Negev Desert represents a hot limit, the hyperarid core of the Atacama Desert represents the dry limit of photosyn-thetic activity and of primary production [ Warren-Rhodeset al. , 2006].[ 3 ] The recent finding of diverse endolithic microorgan-isms inhabiting halite crusts in the driest part of theAtacama Desert [ Wierzchos et al. , 2006] shows, however,that even in such extreme arid conditions, ecological nichesexist where life can grow in relative abundance and diver-sity. These halite crusts have a large spatial distribution andcharacteristic irregular shapes, which are the result of winderosion and partial dissolution and reprecipitation of evap-oritic deposits, during rare and transient wet events. Thecrusts are composed nearly exclusively of halite (96–99%)with minor amounts of gypsum (1–3%) and traces ( 1%)of sylvine and quartz [ Wierzchos et al. , 2006]. Colonies of endolithic photosynthetic cyanobacteria of the genus Chroococcidiopsis can be found 3–7 mm beneath the crust surface, distributed within pores and cracks [ Wierzchoset al. , 2006]. These colonies appear in association withrod-shaped heterotrophic bacteria, suggesting that the crustscan host relatively complex communities.[ 4 ] The endolithic environment provides microorganismswith mineral nutrients and more favorable moisture regimes JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 113, G01028, doi:10.1029/2007JG000561, 2008 Click Here for Full Article 1 NASA Ames Research Center, Moffett Field, California, USA. 2 Departmento Biome´dico e Instituto del Desierto, Universidad deAntofagasta, Antofagasta, Chile. 3 Instituto de Recursos Naturales, CCMA, CSIC, Madrid, Spain. 4 Servei de Microscopia Electronica, Universitat de Lleida, Lleida,Spain.Copyright 2008 by the American Geophysical Union.0148-0227/08/2007JG000561$09.00 G01028 1 of 9 than if they were exposed directly to the atmosphere, as wellas protection against harmful radiation [ Golubic et al. ,1981; Billi et al. , 2000]. However, halite crusts are likelyone of the most challenging environments for life on Earth.Any liquid water within the pore space of the halite will besaturated with NaCl ( 32% weight per volume), resultingin a water activity a w 0.75. The endolithic communitieshave to face large temperature oscillations, occasionallymore than 50 C in a day cycle, and long periods (severalyears) without rain [ McKay et al. , 2003]. The abundance of microorganisms within the halite crusts and their paucity inthe surrounding soil suggest that halite may possess partic-ular physical and/or chemical properties that enable theoccurrence and preservation of microbial ecosystems insuch extreme conditions. Halite is a highly hygroscopicmineral and readily absorbs water vapor at the so-calleddeliquescence relative humidity (DRH). When DRH isreached, water vapor condenses into saturated aqueoussolutions on the crystal surface and/or within the pore space between crystals. The relative humidity at which saltsdeliquesce is dependent on temperature and is characteristicto each salt mineral or assemblage of salt minerals. In thecase of halite, DRH 75% at T = 25 C [ Cohen et al. , 1987; Ebert et al. , 2002], equivalent to a water vapor density ( W d )of 20 g/m 3 . Rock deliquescence may play an important role in the occurrence of life in this hyperarid desert, whererain and fog are not significant sources of moisture. Halitecrystals are also an effective scatterer of UV radiation when precipitated as a mass of small crystals [ Cockell and Raven ,2004], and their translucent properties enable the penetra-tion of photosynthetic light to depths of millimeters tocentimeters.[ 5 ] Here we test the hypothesis that the hygroscopic properties of halite can potentially enable the survivabilityof endolithic microorganisms in extreme hyperarid condi-tions. We report a series of measurements of relativehumidity (RH), W d , T , wetness, and photosyntheticallyactive radiation (PAR), obtained both inside and outsidecolonized halite crusts, for a period of 1 year in thehyperarid core of the Atacama Desert. 2. Site Description and Methods [ 6 ] The study site is located in the Yungay area of theAtacama Desert (24 049 0 S, 69 591 0 W, Figure 1a). Yungayis located 60 km from the coast at an altitude of 1000 m,and it is flanked by two mountain chains, the coastalmountains to the west ( 1000–3000 m high) and theDomeyko Mountains to the east ( 4000 m high)(Figure 1b). Like the rest of the Atacama, Yungay receivesnegligible rain. In addition, the coastal mountains block most of the marine fog, the so-called camanchaca, fromreaching Yungay except in very rare episodes; this is theonly source of humidity.[ 7 ] Geomorphologically, the study site is covered by 50– 60-cm-high halite crusts with an irregular and rough surfaceand a brownish color that is the result of desert sand anddust trapped on the halite surface. These halite fields arecommon in the central Atacama and are the result of theevaporation of paleolakes and the subsequent precipitationof massive salt deposits [ Pueyo et al. , 2001]. Many of thehalite crusts contain a 2–5-mm-thick layer of endolithiccolonization, 3–7 mm below the crust surface [ Wierzchoset al. , 2006]. There is virtually no vegetation surroundingthe study site, and the water table is typically at 25 mdepth.[ 8 ] To study the microweather conditions simultaneouslyinside and around the halite crusts, we used a HOBO 1 microweather station with a data logger equipped withtwo RH/ T sensors (measurement range, 0–100%/ 40 C– 75 C and error, ±0.7 C/±0.7 C at 25 C), one PAR sensor for wavelengths of 400–700 nm (measurement range 0– 2500 m mol m 2 s 1 ), and one leaf wetness sensor (measure-ment range 0 (totally dry) to 100% (totally wet)). The datalogger is waterproof, has an operating range of 20 C– 70 C, and has a typical use of 1 year. The station wasemplaced on 16 June 2006. The data presented in this studycorrespond to 1 year of continuous measurements. Weadapted the HOBO 1 Micro Station to measure the RH and T simultaneously outside and within a natural halite crust,colonized with endolithic microorganisms. To that end, alarge ( 20 kg) halite crust was taken from the Yungay areaand was transported to the facilities at the University of Antofagasta. Two holes were drilled on top of the crust withthe same diameters as the PAR (3.2 cm) and the RH/ T sensor (1.6 cm diameter). The PAR sensor was placed facingupward to obtain radiation readings at the level of the crust surface. The RH/ T sensor was introduced 1 cm into thehalite crust parallel to the rock surface to obtain readingsclose to the colonization zone. Once introduced, the sensor itself sealed the orifice. The crust was transported back to thehalite field in the Yungay area and was placed in exactly thesame spot where it was taken from. The leaf wetness sensor was initially placed within the rock, but after anomalousreadings, probably due to salt, it was extracted and placedadjacent to the halite crusts. The external RH/ T sensor was placed on the soil adjacent to the halite crusts containing theinternal sensor and in the shadow. The temperature regis-tered from this sensor was therefore a function of the air temperature and the radiation heat from the soil. The datalogger, together with the batteries, was placed underneaththe crust. All sensors were set to take a measurement every10 min. Absolute humidity (AH) and W d values inside andoutside the rock were derived from the relative humidityand the temperature data. First, the saturation vapor pres-sure ( P s , in Pascals) for each data point was obtainedfollowing the Tetens formula [ Buck , 1981] P s ¼ 610 : 78exp 17 : 2694 T c T c þ 237 : 3 ; where T c is the temperature in degrees Celsius. W d (in g m 3 )is then obtained from W d ¼ 1000 AH T c R w ; where AH = RH ð Þ P s ð Þ 100 is the absolute humidity and R w =461.5 (J kg 1 K 1 ) is the gas constant for water vapor. 3. Results [ 9 ] Mean, maximum, and minimum values of the keymicroclimatic data outside and within the halite are shown G01028 DAVILA ET AL.: DELIQUESCENCE AND MICROBIAL SURVIVAL2 of 9 G01028 in Table 1. Also listed in Table 1 are the mean seasonal data,the number of wet events, and the total hours of metabolicactivity. 3.1. Temperature [ 10 ] Daily temperature values outside and within thehalite crust were similar during the study period. Air temperatures close to the soil surface ( T a ) were relativelyhigh during the day (maximum T a = 51.79 C) and relativelylow, often below the freezing point of water, during thenight (minimum T a = 3.37 C). Maximum T a values werereached between 1200 and 1600 LT, and minimum valueswere reached shortly before sunrise, between 0600 and0700 LT. The maximum T a values were not extreme whencompared to other desert environments such as DeathValley, where air temperature exceeds 50 C for many daysin the summer. Halite temperatures ( T h ) were similar to the T a values. The maximum registered temperature within thehalite crust was 48.49 C, and the minimum was 3.85 C. Figure 1. (a) Location of the area of study. (b) East-west transect across Yungay shown in Figure 1a.Yungay is located between two mountain ranges 1000–4000 m high, which constrain the arrival of westerly humid sea breeze and easterly dry winds. G01028 DAVILA ET AL.: DELIQUESCENCE AND MICROBIAL SURVIVAL3 of 9 G01028 Maximum and minimum T h values were reached approxi-mately at the same time of the day as T a values. Themaximum difference recorded between simultaneous T a and T h readings was 13.24 C ( T a = 18.28 C and T h =31.52 C). T a values showed larger daily oscillations than T h values, with higher maxima and lower minima. Meandaily temperatures were always between 0 and 10% higher inside the halite crust. Mean annual temperature valueswere also similar outside and within the halite crust (18.60 C and 19.5 C, respectively). Finally, the tempera-ture data showed a clear seasonality, with spring andsummer temperatures approximately 7 C higher than meanautumn and winter temperatures. 3.2. Relative Humidity [ 11 ] The mean annual and seasonal air relative humidity(RH a ) and halite relative humidity (RH h ) showed compara- ble values, albeit slightly higher in the spring and summer months. On the other hand, daily RH values outside andinside the crust showed clear and occasionally significant differences. Figure 2 shows three episodes during which theRH h values remained relatively high and constant for 1– 3 d, while the RH a values showed a normal daily variation,with maximum values at night and minimum values duringthe day. These events occurred when the RH h reached avalue >75%, which corresponds to the DRH of halite[ Cohen et al. , 1987; Ebert et al. , 2002], which we interpret as water condensation (wet halite events (WHE)) within the pore space of the halite crusts. Four recorded WHE had arelatively high intensity and lasted between 30–60 h,whereas most WHE had a lower intensity (between 1 and6.5 h) and a higher frequency (53 a 1 ), for a total of 57 WHE throughout the year. The longest recorded period between two consecutive WHE was 50 d. On the other hand, RH a reached values above 85% on nine occasions(22 h) and above 90% on only two occasions (13.2 h). A Table 1. Comparison of Key Environmental Parameters MeasuredSimultaneously Inside and Outside the Halite Crusts a Parameter Outside Crust Inside Crust Mean annual RH, % 37.16 35.20Mean autumn and winter RH, % 35.30 34.10Mean spring and summer RH, % 39.02 36.61Maximum annual RH, % 100 100Minimum annual RH, % 1.75 0.75Mean annual W d , g cm 3 4.40 5.18Mean autumn and winter W d , g cm 3 3.85 4.79Mean spring and summer W d , g cm 3 4.96 5.57Maximum annual W d , g cm 3 25.42 45.21Minimum annual W d , g cm 3 0.26 0.52Mean annual T , deg C 18.63 19.51Mean autumn and winter T , deg C 15.81 16.87Mean spring and summer T , deg C 21.45 22.16Maximum annual T , deg C 51.79 48.49Minimum annual T , deg C 3.37 3.85Autumn and winter wet events b 1 27Spring and summer wet events b 0 30Conditions suitable for photosynthesis, h a 1c <75 ± 15 d 213.8 a Mean, maximum, and minimum values of the key meteorological dataand number of possible photosynthetic events outside and within the halitecrusts. b RH h > 75% inside the crusts, and RH a > 90% outside the crusts. c RH h > 75% and PAR > 0 inside the crusts. d Warren-Rhodes et al. [2006]. Figure 2. Three episodes of long-duration moist conditions inside the halite crust and no water condensation outside. Because of mineral deliquescence, water vapor condenses within the pore space of the halite at RH h > 75%. Occasionally, this results in relatively long episodes (1–3 d) of liquid water availability within the crusts (black solid line). At the same time, the air relative humidity follows thetypical daily variation (gray dashed line), with maximum values during the night and a minimum duringthe day, and does not reach condensation levels. G01028 DAVILA ET AL.: DELIQUESCENCE AND MICROBIAL SURVIVAL4 of 9 G01028 relatively intense humidity event, likely due to heavy fogand/or dew, occurred on 20 August 2007 starting at 2300 LTand lasted 13 h.[ 12 ] Taking the PAR data, we have estimated the number of hours throughout the year during which the minimumconditions for photosynthetic activity are met (presence of accessible liquid water in halite and PAR > 0). Assumingthat water always condenses above the DRH of halite(>75%), this results in 213.8 h a 1 of potential photosyn-thetic activity for the halite endoliths (Table 1 and Figure 3). 3.3. Water Vapor Density [ 13 ] Water vapor density is a measure of the amount of water vapor in the air and provides important clues regard-ing the srcin of moisture and humidity in the area of study.The mean and minimum W d inside and outside the rock were very similar, whereas the maximum W d showed clear differences (Table 1). Figure 4 shows a typical dailyvariation of W d both inside and outside the halite crusts.Two maxima occur, one after sunset and one after sunrise,and a daily minimum occurs soon after noon. W d remainsrelatively constant during the night and early morning,when westerly winds dominate; a slight decrease in W d isoften observed before sunrise, a phenomenon likely due todew formation in the soil and within the halite crusts. Right after sunrise, as the soil is heated, dew evaporates, whichresults in a transient increase of W d . As the daily temper-ature continues to increase, the moisture in the soil and thehalite crusts dissipates, dry easterly winds become dominant,and W d reaches a minimum between 1600 and 1700 LT.The arrival of westerly, humid sea breeze in the late hoursof the day increases W d and closes the daily cycle. Our datashow that halite efficiently retains water vapor. This is particularly important in the early hours after sunrise, when W d inside the crusts is significantly higher than outside.This difference ( D W d ) between W d inside and outside therock occurs between 0700 and 1200 LT and can reachvalues as high as 35 g m 3 (Figure 4). 3.4. Photosynthetically Active Radiation [ 14 ] The central Atacama, where Yungay is located, isfree of clouds for most of the year. PAR profiles have adaily maximum between 1200 and 1300 LT, typically 2– 3 h earlier than the maximum daily temperature. Themaximum value recorded was 2.37 mmol m 2 s 1 , and theyearly mean value was 1.10 mmol m 2 s 1 . The daily onset of PAR oscillates seasonally between 0600 and 0730 LT,and the daily offset oscillates between 1800 and 2030 LT.The maximum values of PAR were recorded during thesummer. 3.5. Leaf Wetness [ 15 ] The wetness sensor successfully recorded data between 28 February 2007 and 16 June 2007. During thefirst month, dew occurred daily between 2000 and 0900 LT but dissipated immediately at sunrise. Dew events became Figure 3. Possible episodes of photosynthetic activity for halite endoliths during 1 year due to mineraldeliquescence. Each line represents a period of time when RH h > 75% and PAR > 0 simultaneously. Thethree long episodes in Figure 2 occurred during the first 90 d of measurements. A total of 57 episodes provided 213.8 h for possible photosynthetic activity for the endoliths, while outside the halite cruststhere was only one episode, which lasted 6 h (not shown). These episodes appear to be relatively shorter and more frequent in the spring and summer months (approximately days 90–280) than in the autumnand winter months (approximately days 0–90 and 280–365). First and last days of measurements were16 June 2006 and 16 June 2007, respectively. G01028 DAVILA ET AL.: DELIQUESCENCE AND MICROBIAL SURVIVAL5 of 9 G01028
