Skip to main content
SpringerLink
Log in

Gloeocapsopsis AAB1, an extremely desiccation-tolerant cyanobacterium isolated from the Atacama Desert

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

Abstract

The comprehensive study of microorganisms that evolved in the Atacama Desert, the driest and oldest on earth, may help to understand the key role of water for life. In this context, we previously characterized the microenvironment that allows colonization of the underside of quartzes in the Coastal Range of this desert by hypolithic microorganisms (Azua-Bustos et al. Microb Ecol 58:568–581, 2011). Now, we describe the biodiversity composition of these biofilms and the isolation from it of a new cyanobacterial strain. Based on morphologic and phylogenetic analyses, this isolate (AAB1) was classified as a new member of the Gloeocapsopsis genus. Physiological, morphological and molecular responses by isolate AAB1 show that this strain is extremely tolerant to desiccation. Our results also indicate that the isolate biosynthesizes sucrose and trehalose in response to this stressful condition. We identified two candidate genes involved in sucrose synthesis, namely sucrose 6-phosphate synthase and sucrose 6-phosphate phosphatase. Thus, the Gloeocapsopsis isolate AAB1 may represent a suitable model for understanding tolerance to low water availability.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

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

    Article  PubMed  Google Scholar 

  • Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209:1575–1584

    Article  PubMed  Google Scholar 

  • Angeloni SV, Potts M (1986) Polysome turnover in immobilized cells of Nostoc commune (cyanobacteria) exposed to water stress. J Bacteriol 168:1036–1039

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ashraf M (2010) Inducing drought tolerance in plants: recent advances. Biotechnol Adv 28:169–183

    Article  CAS  PubMed  Google Scholar 

  • Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G (2006) Insights on the evolution of trehalose biosynthesis. BMC Evol Biol 6:109

    Article  PubMed Central  PubMed  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 

  • Azua-Bustos A, González-Silva C, Mancilla RA, Salas L, Gómez-Silva B, McKay CP, Vicuña R (2011) Hypolithic cyanobacteria supported mainly by fog in the Coastal Range of the Atacama Desert. Microb Ecol 61:568–581

    Article  PubMed  Google Scholar 

  • Azua-Bustos A, González-Silva C, Arenas-Fajardo C, Vicuña R (2012a) Extreme environments as drivers of convergent evolution: the Atacama Desert Coastal Range as a relevant model. Front Microbiol. doi:10.3389/fmicb.2012.00426

    PubMed Central  PubMed  Google Scholar 

  • Azua-Bustos A, Urrejola C, Vicuña R (2012b) Life at the dry edge: microorganisms of the Atacama Desert. FEBS Lett 586:2939–2945

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424

    Article  CAS  PubMed  Google Scholar 

  • Billi D (2009) Subcellular integrities in Chroococcidiopsis sp. CCMEE 029 survivors after prolonged desiccation revealed by molecular probes and genome stability assays. Extremophiles 13:49–57

    Article  CAS  PubMed  Google Scholar 

  • Billi D, Grilli Caiola M, Paolozzi L, Ghelardini P (1998) A method for DNA extraction from the desert cyanobacterium Chroococcidiopsis and its application to identification of ftsZ. Appl Environ Microbiol 64:4053–4056

    CAS  PubMed Central  PubMed  Google Scholar 

  • Billi D, Friedmann EI, Helm RF, Potts M (2001) Gene transfer to the desiccation-tolerant cyanobacterium Chroococcidiopsis. J Bacteriol 183:2298–2305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Billi D, Viaggiu E, Cockell CS, Rabbow E, Horneck G, Onofri S (2011) Damage escape and repair in dried Chroococcidiopsis spp. from hot and cold deserts exposed to simulated space and Martian conditions. Astrobiology 11:65–73

    Article  CAS  PubMed  Google Scholar 

  • Bruno L, Billi D, Albertano P (2005) Optimization of molecular techniques applied to the taxonomy of epilithic Leptolyngbya strains. Arch Hydrobiol Suppl Algol Stud 117:197–207

    Google Scholar 

  • Buitink J, Leprince O (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48:215–228

    Article  CAS  PubMed  Google Scholar 

  • Bukhov NG, Carpentier R (2004) Effects of water stress on the photosynthetic efficiency of plants. In Advances in: Papageorgiou GC, Govindjee (eds) Photosynthesis and Respiration, Springer, Netherlands, 19: 623–635

  • Caiola MG, Ocampo-Friedmann R, Friedmann EI (1993) Cytology of long-term desiccation in the desert cyanobacterium Chroococcidiopsis (Chroococcales). Phycologia 32:315–322

    Article  CAS  PubMed  Google Scholar 

  • Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to public health significance, monitoring and management. E&FN Spon, London

    Book  Google Scholar 

  • Costerton JW, Stoodley P (2003) Microbial biofilms: protective niches in ancient and modern microbiology. In: Krumbein WE, Paterson DM, Zavarzin GA (eds) Fossil and recent biofilms: a natural history of life on earth. Kluwer, Dordrecht

    Google Scholar 

  • Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328:307–317

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • de Los Ríos A, Valea S, Ascaso C, Davila A, Kastovsky J, McKay CP, Gómez-Silva B, Wierzchos J (2010) Comparative analysis of the microbial communities inhabiting halite evaporates of the Atacama Desert. Int Microbiol 13:79–89

    Google Scholar 

  • 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  CAS  PubMed Central  PubMed  Google Scholar 

  • Edwards HGM, Moody CD, Villar SE, Wynn-Williams D (2005) Raman spectroscopic detection of key biomarkers of cyanobacteria and lichen symbiosis in extreme Antarctic habitats: evaluation for Mars Lander missions. Icarus 174:560–571

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hagemann M, Marin K (1999) Salt-induced Sucrose accumulation is mediated by sucrose-phosphate-synthase in cyanobacteria. J Plant Physiol 155:424–430

    Article  CAS  Google Scholar 

  • Harel Y, Ohad I, Kaplan A (2004) Activation of photosynthesis and resistance to photo inhibition in cyanobacteria within biological desert crust. Plant Physiol 136:3070–3079

    Article  CAS  PubMed Central  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 London 162:421–424

    Article  Google Scholar 

  • Hershkovitz N, Oren A, Cohen Y (1991) Accumulation of trehalose and sucrose in cyanobacteria exposed to matric water stress. Appl Environ Microbiol 57:645–648

    CAS  PubMed Central  PubMed  Google Scholar 

  • Higo A, Katoh H, Ohmori K, Ikeuchi M, Ohmori M (2006) The role of a gene cluster for trehalose metabolism in dehydration tolerance of the filamentous cyanobacterium Anabaena sp. PCC 7120. Microbiology 152:979–987

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Hirai M, Yamakawa R, Nishio J, Yamaji T, Kashino Y, Koike H, Satoh K (2004) Deactivation of photosynthetic activities is triggered by loss of a small amount of water in a desiccation-tolerant cyanobacterium, Nostoc commune. Plant Cell Physiol 45:872–878

    Article  CAS  PubMed  Google Scholar 

  • Janse I, Meima M, Kardinaal WE, Zwart G (2003) High-resolution differentiation of cyanobacteria by using rRNA-internal transcribed spacer denaturing gradient gel electrophoresis. Appl Environ Microbiol 69:6634–6643

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klähn S, Hagemann M (2011) Compatible solute biosynthesis in cyanobacteria. Environ Microbiol 13:551–562

    Article  PubMed  Google Scholar 

  • Komárek J (1993) Validation of the genera Gloeocapsopsis and Asterocapsa (Cyanoprokaryota) with regard to species from Japan, Mexico and Himalayas. B Natl Sci Museum Ser. B (Botany) 19:19–37

    Google Scholar 

  • Komárek J (2003) Coccoid and colonial cyanobacteria. In: Wehr JD, Sheath RG (eds) Freshwater algae of North America. Ecology and classification. Academic Press, San Diego

    Google Scholar 

  • Komárek J, Anagnostidis K (1998) Cyanoprokaryota 1. Teil: Chroococcales. In: Ettl H, Gartner G, Heynig H, Mollenhauer D (eds) Süsswasserflora von Mitteleuropa. Gustav Fischer Verlag, Jena

    Google Scholar 

  • Lacap DC, Warren-Rhodes KA, McKay CP, Pointing SB (2011) Cyanobacteria and chloroflexi-dominated hypolithic colonization of quartz at the hyper-arid core of the Atacama Desert, Chile. Extremophiles 15:31–38

    Article  PubMed Central  PubMed  Google Scholar 

  • Lunn JE (2002) Evolution of sucrose synthesis. Plant Physiol 128:1490–1500

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lunn JE, Ashton AR, Hatch MD, Heldt HW (2000) Purification, molecular cloning, and sequence analysis of sucrose-6F-phosphate phosphohydrolase from plants. Proc Natl Acad Sci USA 97:12914–12919

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marin K, Huckauf J, Fulda S, Hagemann M (2002) Salt-dependent expression of glucosylglycerol-phosphate synthase, involved in osmolyte synthesis in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 184:2870–2877

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mathlouthi M, Luu DV (1980) Laser-Raman spectra of d-glucose and sucrose in aqueous solution. Carbohyd Res 81:203–212

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

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

    PubMed Central  PubMed  Google Scholar 

  • Page-Sharp M, Behm CA, Smith GD (1999) Involvement of the compatible solutes trehalose and sucrose in the response to salt stress of a cyanobacterial Scytonema species isolated from desert soils. Biochim Biophys Acta 1472:519–528

    Article  CAS  PubMed  Google Scholar 

  • Parro V, de Diego-Castilla G, Moreno-Paz M, Blanco Y, Cruz-Gil P, Rodríguez-Manfredi JA, Fernández-Remolar D, Gómez F, Gómez MJ, Rivas LA, Demergasso C, Echeverría A, Urtuvia VN, Ruiz-Bermejo M, García-Villadangos M, Postigo M, Sánchez-Román M, Chong-Díaz G, Gómez-Elvira J (2011) A microbial oasis in the hypersaline Atacama subsurface discovered by a life detector chip: implications for the search for life on Mars. Astrobiology 11:969–996

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Potts M (1999) Mechanisms of desiccation tolerance in cyanobacteria. Eur J Phycol 34:319–328

    Article  Google Scholar 

  • Ramos V, Seabra R, Brito A, Santos A, Santos CL, Lopo M, Moradas-Ferreira P, Vasconcelos VM, Tamagnini P (2010) Characterization of an intertidal cyanobacterium that constitutes a separate clade together with thermophilic strains. Eur J Phycol 45:394–403

    Article  CAS  Google Scholar 

  • Reed RH, Stewart WDP (1983) Physiological responses of Rivularia atra to salinity: osmotic adjustment in hyposaline media. New Phytol 95:595–603

    Article  CAS  Google Scholar 

  • Reed RH, Borowitzka LJ, Mackay MA, Chudek JA, Foster R, Warr SRC, Moore DJ, Stewart WDP (1986) Organic solute accumulation in osmotically stressed cyanobacteria. FEMS Microbiol Rev 39:51–56

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of Cyanobacteria. J Gen Microbiol 111:1–61

    Article  Google Scholar 

  • Sakamoto T, Yoshida T, Arima H, Hatanaka Y, Takani Y, Tamaru Y (2009) Accumulation of trehalose in response to desiccation and salt stress in the terrestrial cyanobacterium Nostoc commune. Phyc Res 57:66–73

    Article  CAS  Google Scholar 

  • Sakamoto T, Kumihashi K, Kunita S, Masaura T, Inoue-Sakamoto K, Yamaguchi M (2011) The extracellular-matrix-retaining cyanobacterium Nostoc verrucosum accumulates trehalose, but is sensitive to desiccation. FEMS Microbiol Ecol 77:385–394

    Article  CAS  PubMed  Google Scholar 

  • Salerno GL, Curatti L (2003) Origin of sucrose metabolism in higher plants: when, how and why? Trends Plant Sci 8:63–69

    Article  CAS  PubMed  Google Scholar 

  • Shirkey B, McMaster NJ, Smith SC, Wright DJ, Rodriguez H, Jaruga P, Birincioglu M, Helm RF, Potts M (2003) Genomic DNA of Nostoc commune (Cyanobacteria) becomes covalently modified during long-term (decades) desiccation but is protected from oxidative damage and degradation. Nucleic Acids Res 31:2995–3005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tweddle JC, Dickie JB, Baskin CC, Baskin JM (2003) Ecological aspects of seed desiccation sensitivity. J Ecol 91:294–304

    Article  Google Scholar 

  • Warr SRC, Reed RH, Stewart WDP (1987) Low-molecular-weight carbohydrate biosynthesis and the distribution of cyanobacteria (blue-green-algae) in marine environments. Br Phycol J 22:175–180

    Article  Google Scholar 

  • 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 

  • Yoshida T, Sakamoto T (2009) Water-stress induced trehalose accumulation and control of trehalase in the cyanobacterium Nostoc punctiforme IAM M-15. J Gen Appl Microbiol 55:135–145

    Article  CAS  PubMed  Google Scholar 

  • Zeng XQ, Hou YJ, Yang ZC, Pèli E, Peng Cl, Nie L (2013) Opportunistic growth and desiccation tolerance: the ecological success of poikilohydrous autotrophs. Nova Hedwigia 96:511–524

    Article  Google Scholar 

Download references

Acknowledgments

Work on this thesis would not have been possible without the Scholarship for Graduate Studies received from CONICYT Chile by AAB, the financial support from FONDECYT project no 1110597, the Millennium Institute for Fundamental and Applied Biology (MIFAB), Chile and from the AngelicvM Foundation, Chile. We also thank Fabio Rodrigues for his help with Raman analysis.

Author information

Authors and Affiliations

  1. Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Alameda 340, Santiago, Chile

    Armando Azua-Bustos, Jorge Zúñiga, Cristián Arenas-Fajardo, Loreto Salas & Vicuña Rafael

  2. Departamento de Ingeniería Química y Bioprocesos, Facultad de Ingeniería, Pontificia Universidad Católica de Chile, Santiago, Chile

    Marcelo Orellana

Authors
  1. Armando Azua-Bustos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Zúñiga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cristián Arenas-Fajardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcelo Orellana
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Loreto Salas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vicuña Rafael
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Armando Azua-Bustos.

Additional information

Communicated by A. Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

792_2013_592_MOESM1_ESM.jpg

Supplementary Table 1 Microbial biodiversity of the quartz hypolithic biofilm. Note: “Chroococcales cyanobacterium LEGE 06123” was later classified as Gloeocapsopsis crepidinum LEGE 06123. (JPEG 653 kb)

792_2013_592_MOESM2_ESM.jpg

Supplementary Table 2- GC content (%) of 16S rRNA-ITS-23S rRNA operon sequences. The right column shows the percentage difference in GC content in relation to the sequence of Gloeocapsopsis AAB1. (JPEG 35 kb)

Supplementary Figure 1- Bright field micrograph of Gloeocapsopsis AAB1 cells in culture. (JPEG 394 kb)

792_2013_592_MOESM4_ESM.jpg

Supplementary Figure 2- DGGE gel of DNA samples obtained by amplification of the ITS gene sequences. Lane 1, hypolithic biofilms; 1.1: Calothrix sp. HA4236-MV1; 1.2: Leptolyngbya sp. Kovacik; 1.3: Nostoc commune NC5 clone 11; 1.4: Gloeocapsopsis AAB1. Lanes 2 – 5, samples obtained from the culture at various times. 2.1, 3.1, 4.1 and 5.1, Gloeocapsopsis AAB1. (JPEG 234 kb)

792_2013_592_MOESM5_ESM.jpg

Supplementary Figure 3- Desiccation chamber. A, chamber assembly. The green color represents the cell sample on top of a microscope slide, whereas the blue marbles are the hygroscopic agent. The arrow points to the internal RH sensor attached to the Petri dish lid. B: temporal profile of  % RH inside the chamber with different desiccating agents. No D.A.: no desiccating agent. 1: Silica gel, 1 g. 2: Silica gel, 2 g. 3: Silica gel, 5 g. 4: NaCl, 1 g. 5: NaCl, 2 g. 6: NaCl, 5 g. 7: CaCl, 1 g. 8: CaCl, 2 g. 9: CaCl, 5 g. (JPEG 189 kb)

792_2013_592_MOESM6_ESM.jpg

Supplementary Figure 4 - Absence of DNA and RNA fragmentation of Gloeocapsopsis AAB1 cells desiccated for 13 days at 0.4 aw. Lanes 1 and 3 correspond to the non desiccated control. (JPEG 58 kb)

792_2013_592_MOESM7_ESM.jpg

Supplementary Figure 5- Maximum likelihood phylogenetic trees obtained with the aligned sucrose 6-phosphate synthase (A) and sucrose 6-phosphate phosphatase (B) Gloeocapsopsis gene sequences using BOSQUE. The numbers on the nodes represent bootstrap values with 1000 replicates. Gray pentagons besides names denote species from which sequences were obtained from their genomes. (JPEG 221 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Azua-Bustos, A., Zúñiga, J., Arenas-Fajardo, C. et al. Gloeocapsopsis AAB1, an extremely desiccation-tolerant cyanobacterium isolated from the Atacama Desert. Extremophiles 18, 61–74 (2014). https://doi.org/10.1007/s00792-013-0592-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-013-0592-y

Keywords

Search

Navigation