, Volume 14, Issue 5, pp 443–452 | Cite as

A novel subaerial Dunaliella species growing on cave spiderwebs in the Atacama Desert

  • A. Azúa-BustosEmail author
  • C. González-Silva
  • L. Salas
  • R. E. Palma
  • R. Vicuña
Original Paper


Strategies for life adaptation to extreme environments often lead to novel solutions. As an example of this assertion, here we describe the first species of the well-known genus of green unicellular alga Dunaliella able to thrive in a subaerial habitat. All previously reported members of this microalga are found in extremely saline aquatic environments. Strikingly, the new species was found on the walls of a cave located in the Atacama Desert (Chile). Moreover, on further inspection we noticed that it grows upon spiderwebs attached to the walls of the entrance-twilight transition zone of the cave. This peculiar growth habitat suggests that this Dunaliella species uses air moisture condensing on the spiderweb silk threads as a source of water for doing photosynthesis in the driest desert of the world. This process of adaptation recapitulates the transition that allowed land colonization by primitive plants and shows an unexpected way of expansion of the life habitability range by a microbial species.


Dunaliella Atacama Desert Evolution Cave Adaptations Water 



Transmission electron microscopy


Scanning electron microscopy


Confocal laser scanning microscopy


Above sea level



This work was supported by the Millennium Institute of Fundamental and Applied Biology (Chile). We also thank Alejandro Munizaga and Ximena Verges for technical support with microscopy and members of Rafael Vicuña’s Lab for critical comments and insights which helped to improve this manuscript.

Supplementary material

792_2010_322_MOESM1_ESM.tif (152 kb)
Figure S1.- Relative humidity (RH) profile inside the cave. A two week period is shown. The values were recorded every 10 minutes by an automatic RH microsensor placed between a spiderweb and the cave wall. (TIFF 151 kb)
792_2010_322_MOESM2_ESM.tif (865 kb)
Figure S2.- Confocal Laser Scanning Microscopy (CLSM) micrographs of the cave inhabiting subaerial Dunaliella. A) CLSM micrograph of aqueous suspension of Dunaliella atacamensis cells extracted from the spiderwebs, showing the pyrenoid (p). B) CLSM differential interference contrast (DIC) image merged with the red autofluorescence emitted by the chlorophyll of the cell chloroplast (c). (TIFF 865 kb)
792_2010_322_MOESM3_ESM.tif (154 kb)
Figure S3.- Absorption spectra of photosynthesis related pigments of the cave inhabiting Dunaliella. The inset shows a picture of chlorophyll a (left) and carotenoid (right) extraction. (TIFF 154 kb)

Supplemental Movie S1 of Dunaliella atacamensis colinized spiderwebs in situ. (AVI 4.61 MB)


  1. Aasen AJ, Eimhjellen KE, Liaaen-Jensen S (1969) An extreme source of β-carotene. Acta Chem Scand 23:2544–2545CrossRefPubMedGoogle Scholar
  2. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRefGoogle Scholar
  3. Azua-Bustos A, González-Silva C, Mancilla RA, Salas L, Palma RE, Wynne JJ, McKay CP, Vicuña R (2009) Ancient photosynthetic eukaryote biofilms in an Atacama Desert coastal cave. Microb Ecol 58:485–496CrossRefPubMedGoogle Scholar
  4. Ben-Amotz A (1980) Glycerol production in the alga Dunaliella. In: San Pietro A (ed) Biochemical and photosynthetic aspects of energy production. Academic Press, New York, pp 91–208Google Scholar
  5. Ben-Amotz A, Avron M (1989) The biotechnology of mass culturing of Dunaliella for products of commercial interest. In: Cresswell RC, Ress TAV, Shah N (eds) Algal and cyanobacterial biotechnology. Longman Scientific and Technical Press, London, pp 90–114Google Scholar
  6. Benoit JB, Lopez-Martinez G, Michaud MR, Elnitsky MA, Lee RE Jr, Denlinger DL (2007) Mechanisms to reduce dehydration stress in larvae of the Antarctic midge, Belgica antarctica. J Insect Physiol 53:656–667CrossRefPubMedGoogle Scholar
  7. Berden-Zrimec M, Drinovec L, Molinari I, Zrimec A, Umani SF, Monti M (2008) Delayed fluorescence as a measure of nutrient limitation in Dunaliella tertiolecta. J Photochem Photobiol B 92:13–18CrossRefPubMedGoogle Scholar
  8. Borowitzka LJ, Brown AD (1974) The salt relations of marine and halophilic species of the unicellular green alga, Dunaliella. The role of glycerol as a compatible solute. Arch Microbiol 96:37–52CrossRefGoogle Scholar
  9. Borowitzka MA, Silva CJ (2007) The taxonomy of the genus Dunaliella (Chlorophyta, Dunaliellales) with emphasis on the marine and halophilic species. J Appl Phycol 19:567–590CrossRefGoogle Scholar
  10. Borowitzka LJ, Borowitzka MA, Moulton TP (1984) The mass culture of Dunaliella for fine chemicals: from laboratory to pilot plant. Hydrobiologia 116(117):115–121CrossRefGoogle Scholar
  11. Brock TD (1975) Salinity and the ecology of Dunaliella from Great Salt Lake. J Gen Microbiol 89:285–292Google Scholar
  12. Brown AD (1990) Microbial water stress physiology. Principles and Perspectives. Wiley, Chichister, pp 93–95Google Scholar
  13. Brown AD, Borowitzka LJ (1979) Halotolerance of Dunaliella. In: Levandowsky M, Hutner SH (eds) Biochemistry and physiology of protozoa. Academic Press, New York, pp 139–190Google Scholar
  14. Cáceres L, Delatorre J, Gómez-Silva B, Rodríguez V, McKay CP (2004) Atmospheric moisture collection from a continuous air flow through a refrigerated coil tube. Atmos Res 71:127–137CrossRefGoogle Scholar
  15. Cagle GD, Pfister RM, Vela GR (1972) Improved staining of extracellular polymer for electron microscopy: examination of Azotobacter, Zoogloea, Leuconostoc, and Bacillus. Appl Microbiol 24:477–487PubMedGoogle Scholar
  16. Cereceda P, Osses P, Larraín H, Farias M, Schemenauer RS (2002) Advective, orographic and radiation fog in the Tarapacá region, Chile. Atmos Res 64:261–271CrossRefGoogle Scholar
  17. Cereceda P, Larrain H, Osses P, Farías M, Egaña I (2007) The climate of the coast and fog zone in the Tarapacá region, Atacama Desert, Chile. Atmos Res 64:301–311Google Scholar
  18. Cereceda P, Larrain H, Osses P, Farías M, Egaña I (2008) Spatial and temporal variability of fog and its relation to fog oases in the Atacama Desert, Chile. Atmos Res 67:312–321CrossRefGoogle Scholar
  19. Chapman RL, Delwiche CF, McCourt RM (2002) Green algal conquest of the land: many conquests, one victory? J Phycol 38(S1): 3–3(1)Google Scholar
  20. Chen H, Jiang JG (2009) Osmotic responses of Dunaliella to the changes of salinity. J Cell Physiol 219:251–258CrossRefPubMedGoogle Scholar
  21. Colomb A, Yassaa N, Williams J, Peeken I, Lochte K (2008) Screening volatile organic compounds (VOCs) emissions from five marine phytoplankton species by head space gas chromatography/mass spectrometry (HS-GC/MS). J Environ Monit 10:325–330CrossRefPubMedGoogle Scholar
  22. Delwiche CF, Karol KG, McCourt RM (2002) One small step: why did the charophytes have the right stuff? J Phycol 38(S1):6–6(1)Google Scholar
  23. Demergasso C, Escudero L, Casamayor EO, Chong G, Balagué V, Pedrós-Alió C (2008) Novelty and spatio-temporal heterogeneity in the bacterial diversity of hypersaline Lake Tebenquiche (Salar de Atacama). Extremophiles 12:491–504CrossRefPubMedGoogle Scholar
  24. Espejo R (2001) Climatological and microbiological characteristics of the Camanchaca phenomenon at Cerro Moreno, Antofagasta, Chile. In: Proceedings of the second international conference on fog and fog collection, pp 463–466Google Scholar
  25. Evangelista V, Evangelisti M, Barsanti L, Frassanito AM, Passarelli V, Gualtieri P (2007) A polychromator-based microspectrophotometer. Int J Biol Sci 3:251–256PubMedGoogle Scholar
  26. 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 56:43–61Google Scholar
  27. Fassel TA, Edmiston CE Jr (1999) Ruthenium red and the bacterial glycocalyx. Biotech Histochem 74:194–212CrossRefPubMedGoogle Scholar
  28. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  29. Gómez PI, González MA (2004) Genetic variation among seven strains of Dunaliella salina (Chlorophyta) with industrial potential, based on RAPD banding patterns and on nuclear ITS rDNA sequences. Aquaculture 233:149–162CrossRefGoogle Scholar
  30. González MA, Gómez PI, Montoya R (1999) Comparison of PCR-RFLP analysis of the ITS region with morphological criteria of various strains of Dunaliella. J Appl Phycol 10:573–580CrossRefGoogle Scholar
  31. González MA, Coleman AW, Gómez PI, Montoya R (2001) Phylogenetic relationship among various strains of Dunaliella (Chlorophyceae) based on nuclear ITS rDNA sequences. J Phycol 37:604–611CrossRefGoogle Scholar
  32. González MA, Gómez PI, Polle JEW (2009) Taxonomy and phylogeny of the genus Dunaliella. In: Ben-Amotz A, Polle JEW, Subba Rao DV (eds) The alga Dunaliella, biodiversity, physiology, genomics and biotechnology. Science Publishers, Enfield, pp 15–44Google Scholar
  33. Gouveia L, Oliveira AC (2009) Microalgae as a raw material for biofuels production. J Ind Microbiol Biotechnol 36:269–274CrossRefPubMedGoogle Scholar
  34. 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 162:421–424CrossRefGoogle Scholar
  35. Hepperle D, Nozaki H, Hohenberger S, Huss VA, Morita E, Krienitz L (1998) Phylogenetic position of the Phacotaceae within the Chlamydophyceaeas revealed by analysis of 18S rDNA and rbcL sequences. J Mol Evol 47:420–430CrossRefPubMedGoogle Scholar
  36. Hosseini Tafreshi A, Shariati M (2009) Dunaliella biotechnology: methods and applications. J Appl Microbiol 107(1):14–35CrossRefPubMedGoogle Scholar
  37. 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 23:1453–1464CrossRefGoogle Scholar
  38. Kaçka A, Dönmez G (2008) Isolation of Dunaliella spp. from a hypersaline lake and their ability to accumulate glycerol. Bioresour Technol 99:8348–8352CrossRefPubMedGoogle Scholar
  39. Kaplan A, Reinhold L (1999) CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50:539–570CrossRefPubMedGoogle Scholar
  40. Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353CrossRefPubMedGoogle Scholar
  41. 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 37:161–165CrossRefGoogle Scholar
  42. 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 64:273–284CrossRefGoogle Scholar
  43. Lewis LA (2002) Numerous transitions to land in green plants: the ‘other’ land plants. J Phycol 38(S1):22–22(1)Google Scholar
  44. Liska AJ, Shevhenko A, Pick U, Katz A (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol 136:2806–2817CrossRefPubMedGoogle Scholar
  45. Massyuk NP (1973) New taxa of the genus Dunaliella Teod. I. Ukr Bot Zh 30:175Google Scholar
  46. McCourt RM, Delwiche CF, Karol KG (2004) Charophyte algae and land plant origins. Trends Ecol Evol 19:661–666CrossRefPubMedGoogle Scholar
  47. Mishra A, Jha B (2009) Isolation and characterization of extracellular polymeric substances from micro-algae Dunaliella salina under salt stress. Bioresour Technol 100:3382–3386CrossRefPubMedGoogle Scholar
  48. Nakada T, Misawa K, Nozaki H (2008) Molecular systematics of Volvocales (Chlorophyceae, Chlorophyta) based on exhaustive 18S rRNA phylogenetic analyses. Mol Phylogenet Evol 48:281–291CrossRefPubMedGoogle Scholar
  49. Olmos J, Paniagua J, Contreras R (2000) Molecular identification of Dunaliella sp. utilizing the 18S rDNA gene. Lett Appl Microbiol 30:80–84Google Scholar
  50. Olmos-Soto J, Paniagua-Michel J, Contreras R (2002) Molecular identification of β-carotene hyper-producing strains of Dunaliella from saline environments using species specific oligonucleotides. Biotechnol Lett 24:365–369CrossRefGoogle Scholar
  51. Or D, Phutane S, Dechesne A (2007) Extracellular polymeric substances affecting pore-scale hydrologic conditions for bacterial activity in unsaturated soils. Vadose Zone J 6:298–305CrossRefPubMedGoogle Scholar
  52. Oren A (2005) A hundred years of Dunaliella research: 1905–2005. Saline Syst 1:2CrossRefPubMedGoogle Scholar
  53. Osaki S (1989) Thermal properties of spider’s thread. Acta Arachnologica 37:69–75CrossRefGoogle Scholar
  54. 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 20:69–74Google Scholar
  55. Raja R, Hema-Iswarya S, Balasubramanyam D, Rengasamy R (2007) PCR identification of Dunaliella salina (Volvocales, Chlorophyta) and its growth characteristics. Microbiol Res 162:168–176CrossRefPubMedGoogle Scholar
  56. 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 13:1–50Google Scholar
  57. 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 69:5679–5684CrossRefPubMedGoogle Scholar
  58. Smith BM, Morrissey PJ, Guenther JE, Nemson JA, Harrison MA, Allen JF, Melis A (1990) Response of the photosynthetic apparatus in Dunaliella salina (green algae) to irradiance stress. Plant Physiol 93:1433–1440CrossRefPubMedGoogle Scholar
  59. Sterling C (1970) Crystal-structure of ruthenium red and stereochemistry of its pectic stain. Am J Bot 57:172–175CrossRefGoogle Scholar
  60. Swofford DL (2002) PAUP*: phylogenetic analyses using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Inc, Publishers, SunderlandGoogle Scholar
  61. Teodoresco EC (1905) Organisation et développement du Dunaliella, nouveau genre de Volvocacée-Polyblepharidée. Beih z Bot Centralbl Bd. XVIII:215–232Google Scholar
  62. Vehoff T, Glisovi A, Schollmeyer H, Zippelius A, Salditt T (2007) Mechanical properties of spider dragline silk: humidity, hysteresis, and relaxation. Biophys J 93:4425–4432CrossRefPubMedGoogle Scholar
  63. Vismara R, Verni F, Barsanti L, Evangelista V, Gualtieri P (2004) A short flagella mutant of Dunaliella sallina (Chlorophyta, Cholorophyceae). Micron 35:337–344CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2010

Authors and Affiliations

  • A. Azúa-Bustos
    • 1
    • 3
    Email author
  • C. González-Silva
    • 2
  • L. Salas
    • 1
  • R. E. Palma
    • 4
  • R. Vicuña
    • 1
    • 3
  1. 1.Departamento de Genética Molecular y Microbiología, Facultad de Ciencias BiológicasPontificia Universidad Católica de ChileSantiagoChile
  2. 2.Centro de investigación del Medio Ambiente (CENIMA)Universidad Arturo PratIquiqueChile
  3. 3.Millennium Institute of Fundamental and Applied Biology (MIFAB)SantiagoChile
  4. 4.Departamento de Ecología y Centro de Estudios Avanzados en Ecología y Biodiversidad, CASEB, Facultad de Ciencias BiológicasPontificia Universidad Católica de ChileSantiagoChile

Personalised recommendations