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Hypolithic Cyanobacteria Supported Mainly by Fog in the Coastal Range of the Atacama Desert

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Abstract

The Atacama Desert is one of the driest places on Earth, with an arid core highly adverse to the development of hypolithic cyanobacteria. Previous work has shown that when rain levels fall below ~1 mm per year, colonization of suitable quartz stones falls to virtually zero. Here, we report that along the coast in these arid regions, complex associations of cyanobacteria, archaea, and heterotrophic bacteria inhabit the undersides of translucent quartz stones. Colonization rates in these areas, which receive virtually no rain but mainly fog, are significantly higher than those reported inland in the hyperarid zone at the same latitude. Here, hypolithic colonization rates can be up to 80%, with all quartz rocks over 20 g being colonized. This finding strongly suggests that hypolithic microbial communities thriving in the seaward face of the Coastal Range can survive with fog as the main regular source of moisture. A model is advanced where the development of the hypolithic communities under quartz stones relies on a positive feedback between fog availability and the higher thermal conductivity of the quartz rocks, which results in lower daytime temperatures at the quartz–soil interface microenvironment.

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References

  1. Agam N, Berliner PR (2006) Dew formation and water vapour adsorption in semi arid environments—a review. J Arid Environ 65:572–590

    Article  Google Scholar 

  2. Alpert P (2005) The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45:685–695

    Article  Google Scholar 

  3. Bao H, Gu B (2004) Natural perchlorate has a unique oxygen isotope signature. Environ Sci Technol 38:5073–5077

    Article  PubMed  CAS  Google Scholar 

  4. Cameron RE, Blank GB (1966) Desert algae: soil crusts and diaphanous substrata as algal habits. Jet Propulsion Laboratory, California Institute of Technology, Technical Report 32-971, pp 41

  5. Cereceda P, Osses P, Larraín H, Farias M, Schemenauer RS (2002) Advective, orographic and radiation fog in the Tarapacá Region, Chile. Atmos Res 64:261–271

    Article  Google Scholar 

  6. Cockell CS, Stokes MD (2004) Widespread colonization by polar hypoliths. Nature 431:414

    Article  PubMed  CAS  Google Scholar 

  7. Davila AF, Gómez-Silva B, de los Rios A, Ascaso C, Olivares H, McKay CP, Wierzchos J (2008) Facilitation of endolithic microbial survival in the hyperarid core of the Atacama Desert by mineral deliquescence. J Geophys Res 113:G01028

    Article  Google Scholar 

  8. Davis WL, de Pater I, McKay CP (2010) Rain infiltration and crust formation in the extreme arid zone of the Atacama Desert, Chile. Planet Space Sci 58:616–622

    Article  CAS  Google Scholar 

  9. De Long EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689

    Article  Google Scholar 

  10. Dose K, Bieger-Dose A, Ernst B, Feister U, Gómez-Silva B, Klein A, Risi S, Stridde C (2001) Survival of microorganisms under the extreme conditions of the Atacama Desert. Orig Life Evol Biosph 31:287–303

    Article  PubMed  CAS  Google Scholar 

  11. Drees KP, Neilson JW, Betancourt JL, Quade J, Henderson DA, Pryor BM, Maier RM (2006) Bacterial community structure in the hyperarid core of the Atacama Desert, Chile. Appl Environ Microbiol 72:7902–7908

    Article  PubMed  CAS  Google Scholar 

  12. Erickson GE (1981) Geology and origin of the Chilean nitrate deposits. U. S. Geological Survey Professional Paper No. 1188, Washington DC, p 12

  13. Espejo R (2001) Climatological and microbiological characteristics of the Camanchaca phenomenon at Cerro Moreno, Antofagasta, Chile. Proceedings of the Second International Conference on Fog and Fog Collection, pp 463-466

  14. Farías M, Cereceda P, Osses P, Nuñez R (2005) Spatial and temporal behavior of the stratocumulus cloud, fog producer in the coast of the Atacama desert (21° south lat., 70° west long.), during one month of winter and another of summer. Investig Geogr 56:43–61

    Google Scholar 

  15. Kaseke Farai K (2009) “Non-rainfall” atmospheric water in arid doil micro-hydrology and ecology. Master of Science Thesis, University of Stellenbosch

  16. Friedmann EI, Lipkin Y, Ocampo-Paus R (1967) Desert algae of the Negev (Israel). Phycologia 6:185–200

    Article  Google Scholar 

  17. Graf A, Kuttler W, Werner J (2008) Mulching as a means of exploiting dew for arid agriculture? Atmos Res 87:369–376

    Article  Google Scholar 

  18. Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9:1613–1631

    Article  PubMed  CAS  Google Scholar 

  19. Gultepe I, Pagowski M, Ried J (2007) A satellite-fog based detection scheme using screen air temperature. Weather forecast 22:444–456

    Article  Google Scholar 

  20. Gupta S, Agrawal SC (2006) Survival of blue-green and green algae under stress conditions. Folia Microbiol Praha 51:121–128

    Article  PubMed  CAS  Google Scholar 

  21. Hartley A, Chong G, Houston J, Mather A (2005) 150 million years of climatic stability: evidence from the Atacama Desert, Northern Chile. J Geol Soc Lond 162:421–424

    Article  Google Scholar 

  22. Higo A, Suzuki T, Ikeuchi M, Ohmori M (2007) Dynamic transcriptional changes in response to rehydration in Anabaena sp. PCC 7120. Microbiology 153:3685–3694

    Article  PubMed  CAS  Google Scholar 

  23. Houston J, Hartley AJ (2003) The central Andean west-slope rainshadow and its potential contribution to the origin of hyper-aridity in the Atacama Desert. Int J Climatol 23:1453–1464

    Article  Google Scholar 

  24. Kappen L, Lange OL, Schulze ED, Evenari M, Buschbom V (1979) Ecophysiological investigations on lichens of the Negev Desert: IV. Annual course of the photosynthetic production of Ramalina maciformis (Del.) Bory. Flora 168:85–105

    Google Scholar 

  25. Katra I, Lavee H, Sarah P (2008) The effect of rock fragment size and position on topsoil moisture on arid and semi-arid hillslopes. Catena 72:49–55

    Article  Google Scholar 

  26. Kemper WD, Nicks AD, Corey AT (1994) Accumulation of water in soils under gravel and sand mulches. Soil Sci Soc Am J 58:56–63

    Article  Google Scholar 

  27. Kraus R, Trimborn P, Ziegler H (2001) Delta13C and deltaD values of Opuntia atacamensis depending on different environmental conditions in the Atacama Desert of Northern Chile. Isot Environ Health Stud 37:161–165

    Article  CAS  Google Scholar 

  28. Lalley JS, Viles HA (2006) Do vehicle track disturbances affect the productivity of soil-growing lichens in a fog desert? Funct Ecol 20:548–556

    Article  Google Scholar 

  29. Lange OL, Bertsch A (1965) Photosynthese der Wustenflechte Ramalina maciformis nach Wasserdampfaufnahme aus dem Luftraum. Naturwissenschaften, 52:215–216. In: Hillel D (1982) Negev, Land, water and life in a desert environment. Praeger Publications, New York

  30. Lange OL, Allen Green TG, Melzer B, Meyer A, Zellner H (2006) Water relations and CO2 exchange of the terrestrial lichen Teloschistes capensis in the Namib fog desert: measurements during two seasons in the field and under controlled conditions. Flora 201:268–280

    Google Scholar 

  31. Larrain H, Velásquez F, Cereceda P, Espejo R, Pinto R, Osses P, Schemenauer RS (2002) Fog measurements at the site ‘Falda Verde’ North of Chañaral (Chile) compared with other North Chilean fog stations. Atmos Res 64:273–284

    Article  Google Scholar 

  32. Li XY (2002) Effects of gravel and sand mulches on dew deposition in the semiarid region of China. J Hydrol 260:151–160

    Article  Google Scholar 

  33. Louw GN, Seely MK (1982) Ecology of desert organisms. Longman House, Essex

    Google Scholar 

  34. Malek E, McCurdy G, Giles G (1999) Dew contribution to the annual water balances in semi-arid desert valleys. J Arid Environ 42:71–80

    Article  Google Scholar 

  35. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Dymock D, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799

    PubMed  CAS  Google Scholar 

  36. McKay CP, Friedmann EI, Gómez-Silva B, Cáceres-Villanueva L, Andersen DT, Landheim R (2003) Temperature and moisture conditions for life in the extreme arid region of the Atacama Desert: four years of observations including the El Niño of 1997-1998. Astrobiology 3:393–406

    Article  PubMed  CAS  Google Scholar 

  37. Navarro-González R, Rainey FA, Molina P, Bagaley DR, Hollen BJ, de la Rosa J, Small AM, Quinn RC, Grunthaner FJ, Cáceres L, Gomez-Silva B, McKay CP (2003) Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life. Science 302:1018–1021

    Article  PubMed  Google Scholar 

  38. Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332

    PubMed  Google Scholar 

  39. Or D, Phutane S, Dechesne A (2007) Extracellular polymeric substances affecting pore-scale hydrologic conditions for bacterial activity in unsaturated soils. Vadose Zone J 6:298–305

    Article  PubMed  CAS  Google Scholar 

  40. Osses P, Farías M, Nuñez R, Cereceda P, Larraín H (2005) Coastal fog, satellite imagery, and drinking water: student fieldwork in the Atacama Desert. Geocarto Int 20:69–74

    Google Scholar 

  41. Pointing SB, Warren-Rhodes KA, Lacap DC, Rhodes KL, McKay CP (2007) Hypolithic community shifts occur as a result of liquid water availability along environmental gradients in China's hot and cold hyperarid deserts. Environ Microbiol 9:414–424

    Article  PubMed  CAS  Google Scholar 

  42. Rech J, Quade J, Hart W (2003) Isotopic evidence for the source of Ca and S in soil gypsum, anhydrite and calcite in the Atacama Desert, Chile. Geochim Cosmochim Acta 67:575–586

    Article  CAS  Google Scholar 

  43. Reysenbach AL, Wickham GS, Pace NR (1994) Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park. Appl Environ Microbiol 60:2113–2119

    PubMed  CAS  Google Scholar 

  44. Rundel P, Dillon MO, Palma B, Mooney HA, Gulmon SL, Ehleringer JR (1990) The phytogeography and ecology of the coastal Atacama and Peruvian deserts. Aliso 13:1–50

    Google Scholar 

  45. Schlesinger WH, Pippen JS, Wallenstein MD, Hofmockel KS, Klepeis DM, Mahall BE (2003) Community composition and photosynthesis by photoautotrophs under quartz pebbles, Southern Mojave desert. Ecology 84:3222–3231

    Article  Google Scholar 

  46. Shaw E, Hill DR, Brittain N, Wright DJ, Täuber U, Marand H, Helm RF, Potts M (2003) Unusual water flux in the extracellular polysaccharide of the cyanobacterium Nostoc commune. Appl Environ Microbiol 69:5679–5684

    Article  PubMed  CAS  Google Scholar 

  47. Smith M, Bowman J, Scott F, Line M (2000) Sublithic bacteria associated with Antarctic quartz stones. Antarct Sci 12:177–184

    Google Scholar 

  48. Thomas DN (2005) Photosynthetic microbes in freezing deserts. Trends Microbiol 13:87–88

    Article  PubMed  CAS  Google Scholar 

  49. Tracy CR, Streten-Joyce C, Dalton R, Nussear KE, Gibb KS, Christian KA (2010) Microclimate and limits to photosynthesis in a diverse community of hypolithic cyanobacteria in northern Australia. Environ Microbiol 12:592–607

    Article  PubMed  Google Scholar 

  50. Vogel S (1955) Niedere “Fensterpflanzen” in der sudafrikanischen wüste. Beitr Biol Pflanz 31:45–135

    Google Scholar 

  51. Warren-Rhodes KA, Rhodes KL, Boyle LN, Pointing SB, Chen Y, Liu S, Zhuo P, McKay CP (2007) Cyanobacterial ecology across environmental gradients and spatial scales in China’s hot and cold deserts. FEMS Microbiol Ecol 61:470–482

    Article  PubMed  CAS  Google Scholar 

  52. Warren-Rhodes KA, Rhodes KL, Pointing SB, Ewing SA, Lacap DC, Gómez-Silva B, Amundson R, Friedmann EI, McKay CP (2006) Hypolithic cyanobacteria, dry limit of photosynthesis, and microbial ecology in the hyperarid Atacama Desert. Microb Ecol 52:389–398

    Article  PubMed  Google Scholar 

  53. Wierzchos J, Ascaso C, McKay CP (2006) Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama Desert. Astrobiology 6:415–422

    Article  PubMed  Google Scholar 

  54. Whitford WG (2002) Ecology of desert systems. Elsevier Science Ltd, San Diego

    Google Scholar 

  55. Yoshimura H, Okamoto S, Tsumuraya Y, Ohmori M (2007) Group 3 sigma factor gene, sigJ, a key regulator of desiccation tolerance, regulates the synthesis of extracellular polysaccharide in cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 14:13–24

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Millennium Institute of Fundamental and Applied Biology, MIFAB (Chile). We also thank Alejandro Munizaga and Ximena Verges for the technical support with microscopy methods.

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Correspondence to Armando Azúa-Bustos.

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Supplemental Figure 1

In situ temperature profiles under quartz stones and opaque rocks. A period of 9 days during winter time of 2008 is shown. -■- quartz stones, -◊- dark opaque stones. (JPG 121 KB)

High resolution image file (TIF 109 KB)

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Azúa-Bustos, A., González-Silva, C., Mancilla, R.A. et al. Hypolithic Cyanobacteria Supported Mainly by Fog in the Coastal Range of the Atacama Desert. Microb Ecol 61, 568–581 (2011). https://doi.org/10.1007/s00248-010-9784-5

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