Skip to main content
Log in

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

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

TEM:

Transmission electron microscopy

SEM:

Scanning electron microscopy

CLSM:

Confocal laser scanning microscopy

a.s.l.:

Above sea level

References

  • Aasen AJ, Eimhjellen KE, Liaaen-Jensen S (1969) An extreme source of β-carotene. Acta Chem Scand 23:2544–2545

    Article  CAS  PubMed  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

    Article  Google Scholar 

  • 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 58:485–496

    Article  CAS  PubMed  Google Scholar 

  • 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 91–208

    Google Scholar 

  • 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 90–114

    Google Scholar 

  • 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 53:656–667

    Article  CAS  PubMed  Google Scholar 

  • 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 92:13–18

    Article  CAS  PubMed  Google Scholar 

  • 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 96:37–52

    Article  CAS  Google Scholar 

  • Borowitzka MA, Silva CJ (2007) The taxonomy of the genus Dunaliella (Chlorophyta, Dunaliellales) with emphasis on the marine and halophilic species. J Appl Phycol 19:567–590

    Article  Google Scholar 

  • Borowitzka LJ, Borowitzka MA, Moulton TP (1984) The mass culture of Dunaliella for fine chemicals: from laboratory to pilot plant. Hydrobiologia 116(117):115–121

    Article  Google Scholar 

  • Brock TD (1975) Salinity and the ecology of Dunaliella from Great Salt Lake. J Gen Microbiol 89:285–292

    Google Scholar 

  • Brown AD (1990) Microbial water stress physiology. Principles and Perspectives. Wiley, Chichister, pp 93–95

    Google Scholar 

  • Brown AD, Borowitzka LJ (1979) Halotolerance of Dunaliella. In: Levandowsky M, Hutner SH (eds) Biochemistry and physiology of protozoa. Academic Press, New York, pp 139–190

    Google Scholar 

  • 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 71:127–137

    Article  Google Scholar 

  • Cagle GD, Pfister RM, Vela GR (1972) Improved staining of extracellular polymer for electron microscopy: examination of Azotobacter, Zoogloea, Leuconostoc, and Bacillus. Appl Microbiol 24:477–487

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 64:301–311

    Google Scholar 

  • 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 67:312–321

    Article  Google Scholar 

  • 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 

  • Chen H, Jiang JG (2009) Osmotic responses of Dunaliella to the changes of salinity. J Cell Physiol 219:251–258

    Article  CAS  PubMed  Google Scholar 

  • 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 10:325–330

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 12:491–504

    Article  CAS  PubMed  Google Scholar 

  • 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 463–466

  • Evangelista V, Evangelisti M, Barsanti L, Frassanito AM, Passarelli V, Gualtieri P (2007) A polychromator-based microspectrophotometer. Int J Biol Sci 3:251–256

    CAS  PubMed  Google Scholar 

  • 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 

  • Fassel TA, Edmiston CE Jr (1999) Ruthenium red and the bacterial glycocalyx. Biotech Histochem 74:194–212

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • 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 233:149–162

    Article  Google Scholar 

  • 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 10:573–580

    Article  Google Scholar 

  • 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 37:604–611

    Article  Google Scholar 

  • 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 15–44

    Google Scholar 

  • Gouveia L, Oliveira AC (2009) Microalgae as a raw material for biofuels production. J Ind Microbiol Biotechnol 36:269–274

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 47:420–430

    Article  CAS  PubMed  Google Scholar 

  • Hosseini Tafreshi A, Shariati M (2009) Dunaliella biotechnology: methods and applications. J Appl Microbiol 107(1):14–35

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Kaçka A, Dönmez G (2008) Isolation of Dunaliella spp. from a hypersaline lake and their ability to accumulate glycerol. Bioresour Technol 99:8348–8352

    Article  PubMed  Google Scholar 

  • Kaplan A, Reinhold L (1999) CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50:539–570

    Article  CAS  PubMed  Google Scholar 

  • Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • Lewis LA (2002) Numerous transitions to land in green plants: the ‘other’ land plants. J Phycol 38(S1):22–22(1)

    Google Scholar 

  • 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 136:2806–2817

    Article  CAS  PubMed  Google Scholar 

  • Massyuk NP (1973) New taxa of the genus Dunaliella Teod. I. Ukr Bot Zh 30:175

    Google Scholar 

  • McCourt RM, Delwiche CF, Karol KG (2004) Charophyte algae and land plant origins. Trends Ecol Evol 19:661–666

    Article  PubMed  Google Scholar 

  • Mishra A, Jha B (2009) Isolation and characterization of extracellular polymeric substances from micro-algae Dunaliella salina under salt stress. Bioresour Technol 100:3382–3386

    Article  CAS  PubMed  Google Scholar 

  • Nakada T, Misawa K, Nozaki H (2008) Molecular systematics of Volvocales (Chlorophyceae, Chlorophyta) based on exhaustive 18S rRNA phylogenetic analyses. Mol Phylogenet Evol 48:281–291

    Article  CAS  PubMed  Google Scholar 

  • Olmos J, Paniagua J, Contreras R (2000) Molecular identification of Dunaliella sp. utilizing the 18S rDNA gene. Lett Appl Microbiol 30:80–84

    Google Scholar 

  • 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 24:365–369

    Article  CAS  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Oren A (2005) A hundred years of Dunaliella research: 1905–2005. Saline Syst 1:2

    Article  PubMed  Google Scholar 

  • Osaki S (1989) Thermal properties of spider’s thread. Acta Arachnologica 37:69–75

    Article  Google Scholar 

  • 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 

  • Raja R, Hema-Iswarya S, Balasubramanyam D, Rengasamy R (2007) PCR identification of Dunaliella salina (Volvocales, Chlorophyta) and its growth characteristics. Microbiol Res 162:168–176

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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  CAS  PubMed  Google Scholar 

  • 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 93:1433–1440

    Article  CAS  PubMed  Google Scholar 

  • Sterling C (1970) Crystal-structure of ruthenium red and stereochemistry of its pectic stain. Am J Bot 57:172–175

    Article  CAS  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analyses using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Inc, Publishers, Sunderland

    Google Scholar 

  • Teodoresco EC (1905) Organisation et développement du Dunaliella, nouveau genre de Volvocacée-Polyblepharidée. Beih z Bot Centralbl Bd. XVIII:215–232

    Google Scholar 

  • Vehoff T, Glisovi A, Schollmeyer H, Zippelius A, Salditt T (2007) Mechanical properties of spider dragline silk: humidity, hysteresis, and relaxation. Biophys J 93:4425–4432

    Article  CAS  PubMed  Google Scholar 

  • Vismara R, Verni F, Barsanti L, Evangelista V, Gualtieri P (2004) A short flagella mutant of Dunaliella sallina (Chlorophyta, Cholorophyceae). Micron 35:337–344

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Azúa-Bustos.

Additional information

Communicated by A. Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

792_2010_322_MOESM1_ESM.tif

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

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

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)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Azúa-Bustos, A., González-Silva, C., Salas, L. et al. A novel subaerial Dunaliella species growing on cave spiderwebs in the Atacama Desert. Extremophiles 14, 443–452 (2010). https://doi.org/10.1007/s00792-010-0322-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-010-0322-7

Keywords

Navigation