Mierob Ecol (1990) 19:111-118

MICROBIAL ECOLOGY 9 Springer-VerlagNew York Inc. 1990

Water Relations and Photosynthesis in the Cryptoendolithic Microbial Habitat of Hot and Cold Deserts Robert J. Palmer, Jr.* and E. Imre Friedmann Polar Desert Research Center and Department of BiologicalScience, Florida State University, Tallahassee, Florida 32306-2043, USA

Abstract. Two cryptoendolithic microbial communities, lichens in the Ross Desert of Antarctica and cyanobacteria in the Negev Desert, inhabit porous sandstone rocks of similar physical structure. Both rock types adsorb water vapor by physical mechanisms unrelated to biological processes. Yet the two microbial communities respond differently to water stress: cryptoendolithic lichens begin to photosynthesize at a matric water potential of - 4 6 . 4 megaPascals (MPa) [70% relative humidity (RH) at 8~ resembling thallose desert lichens. Cryptoendolithic cyanobacteria, like other prokaryotes, photosynthesize only at very high matric water potentials [ > - 6 . 9 MPa, 90% RH at 20~

Introduction Cryptoendolithic microbial communities (those hidden inside rocks [ 12]) occur in desert regions worldwide [10]. In the ice-free Ross Desert (McMurdo Dry Valleys) of Antarctica, sandstone rocks harbor diverse microbial populations [3, 5-7]. The most prevalent of these is the lichen-dominated community. It Comprises lichens with green algae (Trebouxia) as phycobionts, nonlichenized algae and fungi, a few cyanobacteria, and heterotrophic bacteria [6, 7, 28]. The Community occupies a zone that begins ~ 1 m m below the surface, extends about 5 m m into the rock, and is vertically stratified in response to a light gradient [22]. Field measurements [9, 15] have shown that, during summer, tnsolation warms rock surfaces above the freezing point. If snow is present, rocks can become permeated with liquid water [4]. During dry periods, miCrobial metabolism could be supported by moisture retained inside the rock [9, 16]. The duration of metabolic activity has been calculated on the basis of rock temperature and water availability [9]. In contrast to the complex endolithic ecosystem found in Antarctica, a much simpler community exists within sandstone rocks in the southern Negev Desert of Israel. Cyanobacteria, primarily Chroococcidiopsis sp., and heterotrophic bacteria form a green layer up to 2 m m thick, beginning less than 1 m m below * Present address. Insdtut •r AltgemeineMikrobiologie,Christian-Aibrechts-Universtit~it,D-2300

Kiel, FRG.

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the rock surface [2, 8, 11 ]. Endolithic prokaryotes seem best adapted to survive the temperature fluctuations and nearly continuous drought in this extreme hot desert habitat [5], where total rainfall averages less than 20 m m per year [17]. Although its natural habitat is nearly always dry, experiments with Chroococcidiopsis sp. isolated from this locality have shown that this cyanobacterium incorporates COz only when matric water potentials are above - 1 0 megaPascals (MPa) [26]. This water potential range is equivalent to relative humidity (RH) >93% at 34~ In the present paper, we investigate the response of these communities to matric water stress and the possible role of the physical structure of the endolithic habitat in the water economy of enclosed microorganisms.

Methods

Material Collection and Storage In the Ross Desert, Beacon sandstone rocks colonized by the lichen-dominated cryptoendolithic community were collected from Linnaeus Terrace (77~ 16 l~ in the McMurdo Dry Valleys, South Victoria Land, Antarctica, during the austral summers of 1984, 1985, and 1986. They were shipped frozen to Tallahassee and stored at - 2 6 ~ in the dark. In the Negev Desert, Nubian sandstone rocks colonized by Chroococcidiopsis sp. were collected in the Timna National Park (30 km north of Eilat, Israel) during the summers of 1984 and 1985 and the spring of 1987. Rocks were flown to Tallahassee and stored at 20~ in the dark. Storage time ranged from less than 3 months (some of the Negev samples) to 2 years (1984 Antarctic samples). This variation, unavoidable because of our dependence on availability of material, is not likely to have affected our results significantly. Both communities are adapted to spending long periods of time in a desiccated state, and conditions of storage were not very different from those prevailing in nature. Furthermore, the results were normalized to chlorophyll, which would correct for possible changes in viability.

C02 Fixation Twenty-four to 48 hours before experiments, Antarctic rocks were transferred to 8~ and Negev rocks to 20"C. Experiments and handling of Antarctic rocks were carried out at 8"C. Rocks with heavy cryptoendolithic lichen growth but no obvious green Hemichloris zone (see [6, 7] for description of zonation and photographs of colonized rocks) were broken into pieces of approximately 1 em 3, and areas lacking visible colonization were removed. Therefore, the samples used in these studies were representative of cryptoendolithic lichens with little interference from other microorganisms. The method used to create defined matric water potentials has been previously described [25]. Experimental chambers were filled with a single layer of rock pieces ( ~ 8-10 cm 2 upper rock surface area/chamber) and equilibrated in darkness at saturating RH for 2, 12, 24, or 48 hours (hydration time-course experiment) or at lower RH for 24 hours (water-stress experiments). Following equilibration, lights were turned on [ 150 t~mol photons photosynthetically active radiation (PAR)/m2/ sec], and, after 5 min, 100-1,000/zl [ - 1 • 106 counts per minute (CPM)/chamber] of ~4CO2-air [ 1] was injected and circulated for 10 rain. After an additional 50 min of incubation, the rocks were removed, crushed, transferred to 50-ml beakers, covered with 5-10 ml of chilled 95% (vol/ vol) methanol, and extracted for 36 hours at 8~ in darkness. The extracts were removed by filtration and assayed spectrophotometrically [21 ] for chlorophyll content. Five hundred milliliters of each extract was acidified with 50/zl of 1 N HC1 to remove unincorporated HCO~-, then added

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to 5 ml of scintillationcocktail for radioactivity measurement in a Packard 2045 liquid scintillation spectrometer. Incorporation was normalized to chlorophyll (chl) content. After removal of the rnethanolic extract, the crushed rocks were washed once with 95% methanol, then dried overnight at 65oc. Methanol-insoluble cellular material was separated from coarse rock grains by sifting (sieve mesh size, 0.15 ram). The material passing through the sieve was weighed, and 100-rag portions were acidified with 200 ~1 of 0.1 N HC1 each and added to 5 ml of scintillation fluid. Total radioactivity of methanol-insoluble fractions was normalized to chlorophyll content. No difference in normalized incorporation was apparent when whole crushed rock was assayed rather than sifted material. This point is also significant because crushed rock was used as the methanolinsoluble fraction in experiments with the Negev rocks (see below). Quenching, which could arise .from the assay of solid material, was not detected by the method of external standard. No difference in counting efficiency between crushed rock and sieved material was seen in the Antarctic samples, and none would be expected for Negev samples. The mean incorporation values were compared by t test, and statistical significance (P level) of each comparison is given below. Experiments and handling of Negcv rocks were carried out at 20~ Experimental procedures were identical to those for Antarctic rocks with the exception that, for radioactivity measurement of methanol-insolublematerial, crushed rock was acidified and added to scintillation fluid because the cyanobacteria adhered to sand grains.

Adsorption o f Water by Rocks Fist-sized pieces of colonized Beacon and Nubian sandstones were sculpted with a rasp until the Volumes (measured by displacement of water) and surface areas (measured by the weight of cutout tracings of all faces) were nearly identical [for Beacon and the Nubian sandstone, respectively, dry (60"C) weights, 294.99 and 313.16 g; volumes, 105 and 109 cm3; and total surface areas, 173.4 and 176.2 crn2]. The rocks were equilibrated overnight (16 hours) in water or in an atmosphere of controlled RH above a salt solution [23], then weighed. In an experiment designed to determine whether biological material contributes to water-vapor adsorption, the rocks were heated to 550~ for 8 hours to remove organic matter, and water-vapor adsorption experiments were repeated.

Results The Ross Desert Cryptoendolithic Lichen Community D a r k c o n t r o l s at 100% R H s h o w e d t h a t CO2 u p t a k e i n the d a r k r e a c h e d 9% o f t h a t i n t h e light. A t 80% R H , u p t a k e i n t h e d a r k d r o p p e d to t r a c e levels, i.e., less t h a n twice b a c k g r o u n d ( d a t a n o t p r e s e n t e d ) . R e s u l t s p r e s e n t e d in T a b l e s 1 a n d 2 are n o t c o r r e c t e d for d a r k u p t a k e . T h e i n f l u e n c e o f h y d r a t i o n t i m e at 100% R H o n COz i n c o r p o r a t i o n i n the light is s h o w n i n T a b l e 1. I n c o r p o r a t i o n c o u l d be d e t e c t e d after 2 h o u r s o f h y d r a t i o n . It rose t h r e e f o l d (P < 0.005) after 12 h o u r s h y d r a t i o n a n d a g a i n b y m o r e t h a n h a l f (P < 0.05) after 24 h o u r s h y d r a t i o n . H o w e v e r , i n c o r p o r a t i o n .dropped b y a b o u t h a l f (P < 0.005) after 48 h o u r s h y d r a t i o n . I n c o r p o r a t i o n ~nto l o w - m o l e c u l a r - w e i g h t ( m e t h a n o l - e x t r a c t a b l e ) m e t a b o l i t e s was always higher t h a n i n c o r p o r a t i o n i n t o h i g h - m o l e c u l a r - w e i g h t s u b s t a n c e s (pellet, i n s o l u b l e macromolecules). T a b l e 2 s u m m a r i z e s effects o f m a t r i c w a t e r stress o n p h o t o s y n t h e s i s . T w e n t y four h o u r s h y d r a t i o n t i m e was used b e c a u s e this p e r i o d gave o p t i m u m i n c o r -

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Table 1. Effect of hydration time on COz incorporation by the Ross Deserl eryptoendolithic lichen community a

Hydration time at 100% RH (hours)

N

2 12 24 48

6 4 6 6

CPM/~zg chl/hour Extract 218 1,007 1,848 808

(226) (384) (578) (381)

Pellet 192 446 499 275

(122) (148) (121) (63)

Total 437 1,453 2,348 1,083

(324) (518) (661) (431)

a Rocks were equilibrated at 100% RH for 2, 12, 24, or 48 hours before ~4CO2 was injected; SD in parentheses

poration in the time-course study. Incorporation was highest at 98% RH ( - 2 . 6 MPa) and dropped by nearly h a l f ( P < 0.005) at 100% RH, a result consistent with COz-diffusion limitation of lichen photosynthesis (saturation effect [20]). Incorporation at 90% R H ( - 13.7 MPa) and at 80% R H ( - 2 9 . 0 MPa) was not significantly different from that at saturation. A significant decrease (P < 0.0005) was seen at 70% R H ( - 4 6 . 4 MPa); incorporation varied between trace levels and 463 CPM/ttg chl/hour, and the mean was lower by a factor o f at least 6 than at higher humidities. At 60% R H ( - 6 6 . 4 MPa), incorporation was at trace levels.

The Negev Desert Cryptoendolithic Cyanobacteriat Community After 24 hours hydration at 100% RH, COz uptake in the dark was at trace levels (data not presented). As in Antarctic cryptoendolithic lichens, COz incorporation in light (Table 3) reached its m axi m um after 24 hours hydration. In contrast to results with the Ross Desert community, fixation by the Negev Desert community into pellet substances was always equal to or greater than fixation into extracts. As seen in Table 4, m axi m um incorporation occurred at 100% RH, decreased rapidly (by a factor of 7; P < 0.05) at 98% RH ( - 2 . 7 MPa), and was at trace Table 2. Effect of matric water stress on CO2 incorporation by the Ross Desert cryptoendolilhic lichen community a

RH (%)

N

100 98 90 80 70 60

6 4 4 4 4 4

Total CPM/#g chl/hour 2,348 4,203 2,449 1,889 336 Trace

(661) (1,233) (847) (77) (103) < 2 • background

Rocks were equilibrated at the indicated RH for 24 hours before ~4CO2 was injected; SD in parentheses

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Table 3. Effect of hydration time on COz incorporation by the Negev Desert cryptoendolithic cyanobacterial communitya Hydration time (hours)

N

Extract

2 12 24 48

4 4 4 5

b 128(154) 498 (360) 447 (166)

CPM//zg chl/hour Pellet b 198(311) 1,365 (721) 641 (171)

Total b 325(464) 1,837 (1,104) 1,088 (315)

a Rocks were equilibrated at 100% RH for the indicated time before ~4CO2was injected; b, background; SD in parentheses levels at 95% R H ( - 6 . 9 MPa). These results are consistent with the results o f Potts and F r i e d m a n n [26] on cultured Chroococcidiopsis sp. isolated from the same habitat.

Water Adsorption by Beacon and Nubian Sandstones Table 5 shows weight gains o f Beacon and N u b i a n sandstone samples after equilibration in liquid water or after drying and 12 hours equilibration in atmospheres o f different humidity. Both rocks gained weight in h u m i d a t m o Spheres, and absolute weight gain was nearly identical before and after incineration o f organic matter. Weight gain increased as h u m i d i t y was increased.

Discussion The photosynthetic response to water stress o f Ross Desert cryptoendolithic lichens is similar to that ofepilithic thallose lichens [ 19]: both incorporate CO2 Under water stress using water v a p o r as a source o f moisture. Ross Desert cryptoendolithic lichens incorporate COz at matric water potentials as low as - 4 6 . 4 M P a (70% R H at 8~ and thus m a y have a m o r e efficient water e c o n o m y than do Negev Desert thallose lichens, which begin photosynthesis at water Potentials a r o u n d - 3 0 M P a (80% R H at 20~ [19]. As do m a n y thallose

Table 4. Effect of matric water stress on CO2 incorPoration by the Negev Desert eryptoendolithic cyanobacterial communitya RH (%)

Total CPM//~g chl/hour

100 98 95

1,837 (1,104) 260 (80) Trace

~Rocks were equilibrated at the indicated RH for 24 hours before ~4CO2was injected; N = 4; SD in parentheses

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Table 5. Weight gain (grams, % dry weight) of colonized Beacon and Nubian sandstone rocks, both before and after incineration of organic matter, after 16 hours equilibration in either liquid water or an atmosphere of defined RH

Equilibration conditions Liquid water 100% RH 97% RH 79% RH

Beacon sandstone After Before incineration incineration (g) (% dry (g) (% dry wt) wt) 14.25,4.83 0.30, 0.10 0.21, 0.07 0.07, 0.02

ND 0.29, 0.10 0.18, 0.06 ND

Nubian sandstone After Before incineration incineration (g) (% dry (g) (% dry wt) wt) 18.86, 6.02 0.31, 0.10 0.26, 0.08 0.08, 0.03

ND 0.28,0.09 0.24,0.08 ND

ND, not determined

lichens [20], Ross Desert cryptoendolithic lichens have lower photosynthetic rates at saturation than at 98% RH. This finding suggests that cryptoendolithic lichens may experience diffusion-related CO2 limitation (saturation effect), although this effect was not seen in infrared gas analysis experiments [ 15]. Both field and laboratory experiments [30, 31] d e m o n s t r a t e d that the Antarctic cryptoendolithic lichen c o m m u n i t y incorporates significant a m o u n t s o f inorganic carbon (bicarbonate and CO2) in the dark. In the present study COz uptake was up to 10% o f that in the light. In the lichen-dominated c o m m u n i t y , the bulk o f the heterotrophs consists o f fungi (lichen-forming m y c o b i o n t s and nonlichen-forming parasymbionts [7]), and laboratory experiments have shown that both are capable o f CO2 uptake in the dark [24]. Bacterial biomass a m o u n t s to ~ 0 . 1 5 % o f the fungal biomass [13], and thus the contribution o f bacteria to dark incorporation is probably not significant. In Negev Desert epilithic lichens, the hyphal network o f the thallus enhances water availability and thus photosynthetic ability under water stress [R. J. Palmer, Ph.D. Thesis, Florida State University, Tallahassee, Florida, 1987]. Cryptoendolithic lichens have no organized thallus, and the loose fungal hyphae grow between and a r o u n d crystals in the porous rock [6]. As Beacon sandstone also adsorbs water vapor, the rock substratum m a y have a role in the water e c o n o m y o f cryptoendolithic lichens similar to that o f the thallus. In contrast to lichens, the Negev Desert cryptoendolithic cyanobacterial comm u n i t y photosynthesizes only at matric water potentials approaching that o f liquid water. This finding is in agreement with results o f Ports and F r i e d m a n n [26] with Chroococcidiopsis sp. strains isolated from Negev sandstones. Although N u b i a n and Beacon sandstones adsorb water v a p o r in similar amounts, cryptoendolithic cyanobacteria do not appear to utilize this water source to the same extent that cryptoendolithic lichens do. In this respect, Negev Desert endolithic cyanobacteria follow the general pattern observed in prokaryotes: no activity at low matric water potentials [ 14, 29]. Lange et al. [18] found that free-living Nostoc sp. and lichens with cyanobacterial phycobionts require liquid water for photosynthesis. The present study and the results o f Potts and F r i e d m a n n [26] indicate that a water potential approaching that o f liquid water is sufficient for prokaryotic metabolism. Recent studies o f de W i n d e r et al. [32]

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suggest that the w a t e r - a d s o r b i n g properties o f the s u b s t r a t u m (porous sandstone or the filter disk used in e x p e r i m e n t s ) enable c y a n o b a c t e r i a to p h o t o s y n t h e s i z e Under such conditions. Besides differences in water e c o n o m y , the lichen a n d cyanobacterial c o m munities differ in that the latter partition a higher percentage o f fixed c a r b o n into high-molecular-weight substances. This preferential fixation o f c a r b o n into m a c r o m o l e c u l e s m a y reflect the m e t a b o l i c simplicity o f prokaryotes. Lichens Produce low-molecular-weight s e c o n d a r y metabolites, such as lichen acids, a n d these m a y account for the higher ratio o f fixed c a r b o n in the m e t h a n o l - s o l u b l e fraction. A further difference is the conspicuous delay in p h o t o s y n t h e s i s in the N e g e v Samples c o m p a r e d to those f r o m the Ross Desert. Such a delay in p h o t o s y n thesis (but not in respiration) after rewetting o f drought-resistant c y a n o b a c t e r i a was reported by Scherer et al. [27], and was also studied in the N e g e v cryptoendolithic c o m m u n i t y (E. I. F r i e d m a n n , M. A. Meyer, a n d L. K a p p e n , unpublished data). Although the physical structure a n d w a t e r - a d s o r b i n g capacity o f the sandStones they inhabit are similar, the cryptoendolithic lichen a n d cyanobacterial COmmunities differ in b o t h their e n v i r o n m e n t (cold vs. hot desert) a n d their Constituents (eukaryotes vs. prokaryotes). It should be noted that c r y p t o e n d o lithic lichens h a v e not been r e p o r t e d to date f r o m hot deserts, a n d c y a n o b a c terial c o m m u n i t i e s in cold desert rocks are rare a n d little u n d e r s t o o d (the relatively b e t t e r - k n o w n Hormathonema-Gloeocapsa c o m m u n i t y in the Antarctic is b o u n d to the presence o f capillary w a t e r in the rock substrate [7]). Therefore, it a p p e a r s that b o t h c o m m u n i t i e s discussed in the present study represent the d o m i n a n t types in their respective e n v i r o n m e n t s .

Acknowledgments.This work was supported

by NSF grant DPP 83-1410 and NASA grant NSG 7337 to EIF, and by NSF grant BSR 8612256 to EIF and RIP. We thank Dr. Anne B. Thistle for critical reading of the manuscript.

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in the Ross Desert of Antarctica: continuous nanoclimate data, 1984 to 1986. Polar Biol 7: 237-287 10. Friedmann EI, Ocampo-Friedmann R (1984) Endolithic microorganisms in extreme dry environments: analysis ofa lithobiontic microbial habitat. In: Reddy CA (ed) Current perspectives in m i c r o b i a l ecology. A m e r i c a n Society for Microbiology, W a s h i n g t o n , DC, pp 177-185 11. Friedmann EI, Ocampo-Friedmann R(1985) Blue-green algae in arid cryptoendolithic habitats. Arch Hydrobiol Suppl 71:349-350 12. Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Petrol 51:475-478 13. Greenfield LG (1988) Forms of nitrogen in Beacon sandstone rocks containing endolithic microbial communities in Southern Victoria Land, Antarctica. Polarforschung 58:211-218 14. Griffin DM, Luard EJ (1979) Water stress and microbial ecology. In: Shilo M (ed) Strategies of microbial life in extreme environments. Verlag Chemie, Weinheim, New York, pp 49-64 15. Kappen L, Friedmann EI (1983) Ecophysiology oflichens in the dry valleys of Southern Victoria Land, Antarctica. II. CO2 gas exchange in cryptoendolithic lichens. Polar Biol 1:227-232 16. Kappen L, Friedmann EI, Garty J (I 981) Ecophysiology oflichens in the dry valleys of Southern Victoria Land, Antarctica. I. Microclimate of the cryptoendolithic lichen habitat. Flora 171: 216-235 17. Katznelson I (1958) Rainfall in Palestine (in Hebrew). Meterological Papers 8:37-70 18. Lange OL, Kilian E, Ziegler H (1986) Water vapor uptake and photosynthesis of lichens: performance differences in species with green and blue-green algae as phycobionts. Oecologia 71:104-110 19. Lange OL, Schulze E, Koch W (1970) Experimentell-/Skologische Untersuchungen an Flechten der Negev-Wfiste. II. CO2-Gaswechsel und Wasserhaushalt von Ramalina maciformis (Del.) Bory am natfirlichen Standort w/ihrcnd der sommerlichen Trockenperiode. Flora 159:38-62 20. Lange OL, Matthes U (1981) Moisture-dependent CO2 exchange of lichens. Photosynthetica 15:555-574 21. Meeks JC, Castenholz RW (1971) Growth and photosynthesis in an extreme thermophile, Synechococcus lividus (Cyanophyta). Archiv Mikro 78:25-41 22. Nienow JA, McKay CP, Friedmann EI (1988) The cryptoendolithic microbial environment in the Ross Desert of Antarctica: light in the photosynthetically active region. Microb Ecology 16:271-289 23. O'Brien FEM (1948) The control of humidity by saturated salt solutions. J Sci Instrum 25: 73-76 24. Palmer RJ Jr, Friedmann EI (1988) Incorporation of inorganic carbon by Antarctic cryptoendolithic fungi. Polarforschung 58:189-192 25. Palmer RJ Jr, Nienow JA, Friedmann EI (1987) Control of matric water potential by temperature differential. J Micro Methods 6:323-326 26. Ports M, Friedmann EI (1981) Effects of water stress on cryptoendolithic cyanobacteria from hot desert rocks. Arch Microbiol 130:267-271 27. Scherer S, Ernst A, Chen TW, Brger P (1984) Rewetting of drought-resistant blue-green algae: time course of water uptake and reappearance of respiration, photosynthesis and nitrogen fixation. Oecologia 62:418-423 28. Siebert J, Hirsch P (1988) Characterization of selected coccal bacteria isolated from Antarctic rock and soil samples from the McMurdo-Dry Valleys (South-Victoria Land). Polar Biol 9: 37-44 29. Troller JA (1980) Influence of water activity on microorganisms in food. Food Technology May:76-80, 82 30. Vestal JR (1987) Carbon metabolism of the cryptoendolithic microbiota from the Antarctic desert. Appl Env Microbiol 54:960-965 31. Vestal JR, Friedmann EI (1983) In situ carbon metabolism by the cryptoendolithic microbial community in the Antarctic cold desert. Antarct J US 17(1982 review):190-191 32. de Winder B, Matthijs HCP, Mur LR (in press) The role of water retaining substrata on the photosynthetic response of three drought tolerant phototrophic microorganisms isolated from a terrestrial habitat. Arch Microbiol

Water relations and photosynthesis in the cryptoendolithic microbial habitat of hot and cold deserts.

Two cryptoendolithic microbial communities, lichens in the Ross Desert of Antarctica and cyanobacteria in the Negev Desert, inhabit porous sandstone r...
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