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Morphological and phylogenetic diversity of thermophilic cyanobacteria in Algerian hot springs

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Abstract

Geothermal springs in Algeria have been known since the Roman Empire. They mainly locate in Eastern Algeria and are inhabited by thermophilic organisms, which include cyanobacteria forming mats and concretions. In this work, we have investigated the cyanobacterial diversity of these springs. Cyanobacteria were collected from water, concretions and mats in nine hot springs with water temperatures ranging from 39 to 93 °C. Samples were collected for isolation in culture, microscopic morphological examination, and molecular diversity analysis based on 16S rRNA gene sequences. Nineteen different cyanobacterial morphotypes were identified, the most abundant of which were three species of Leptolyngbya, accompanied by members of the genera Gloeocapsa, Gloeocapsopsis, Stigonema, Fischerella, Synechocystis, Microcoleus, Cyanobacterium, Chroococcus and Geitlerinema. Molecular diversity analyses were in good general agreement with classical identification and allowed the detection of additional species in three springs with temperatures higher than 50 °C. They corresponded to a Synechococcus clade and to relatives of the intracellularly calcifying Candidatus Gloeomargarita lithophora. The hottest springs were dominated by members of Leptolyngbya, Synechococcus-like cyanobacteria and Gloeomargarita, whereas Oscillatoriales other than Leptolyngbya, Chroococcales and Stigonematales dominated lower temperature springs. The isolation of some of these strains sets the ground for future studies on the biology of thermophilic cyanobacteria.

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References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bhaya D, Grossman AR, Steunou AS, Khuri N, Cohan FM, Hamamura N, Melendrez MC, Bateson MM, Ward DM, Heidelberg JF (2007) Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J 1(8):703–713. doi:10.1038/ismej.2007.46

    Article  PubMed  CAS  Google Scholar 

  • Bouanane-Darenfed A, Fardeau M-L, Gregoire P, Joseph M, Kebbouche-Gana S, Benayad T, Hacene H, Cayol J-L, Ollivier B (2011) Caldicoprobacter algeriensis sp nov a new thermophilic anaerobic, xylanolytic bacterium isolated from an Algerian hot spring. Curr Microbiol 62(3):826–832. doi:10.1007/s00284-010-9789-9

    Article  PubMed  CAS  Google Scholar 

  • Brock TD (1967) Life at high temperatures. Science 158(3804):1012–1019

    Article  PubMed  CAS  Google Scholar 

  • Castenholz RW (1969) Thermophilic blue-green algae and the thermal environment. Bacteriol Rev 33(4):476–504

    PubMed  CAS  PubMed Central  Google Scholar 

  • Castenholz RW (2001) Phylum BX. Cyanobacteria: oxygenic photosynthetic bacteria. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. Springer, New York, pp 473–599

    Chapter  Google Scholar 

  • Castenholz RW (2008) Le rôle des cyanobactéries et autres phototrophes dans les écosystèmes des sources chaudes. Press Therm Climat 145:129–134

    Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2002) Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 12(2):R62–R64

    Article  PubMed  CAS  Google Scholar 

  • Coman C, Druga B, Hegedus A, Sicora C, Dragos N (2013) Archaeal and bacterial diversity in two hot spring microbial mats from a geothermal region in Romania. Extremophiles 17(3):523–534

    Article  PubMed  Google Scholar 

  • Couradeau E, Benzerara K, Moreira D, Gerard E, Kazmierczak J, Tavera R, Lopez-Garcia P (2011) Prokaryotic and eukaryotic community structure in field and cultured microbialites from the alkaline Lake Alchichica (Mexico). PLoS One 6(12):e28767. doi:10.1371/journal.pone.0028767

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Couradeau E, Benzerara K, Gerard E, Moreira D, Bernard S, Brown GE Jr, Lopez-Garcia P (2012) An early-branching microbialite cyanobacterium forms intracellular carbonates. Science 336(6080):459–462. doi:10.1126/science.1216171

    Article  PubMed  CAS  Google Scholar 

  • Dadheech PK, Glockner G, Casper P, Kotut K, Mazzoni CJ, Mbedi S, Krienitz L (2013) Cyanobacterial diversity in the hot spring, pelagic and benthic habitats of a tropical soda lake. FEMS Microbiol Ecol 85(2):389–401

    Article  PubMed  CAS  Google Scholar 

  • Dib H (1985) Le thermalisme de l’Est Algérien. Thèse de doctorat 3ème cycle, University of Science and Technology Houari Boumedienne, Algiers

  • Dyer DL, Gafford RD (1961) Some characteristics of a thermophilic blue-green alga. Science 134(3479):616–617. doi:10.1126/science.134.3479.616

    Article  PubMed  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ferris MJ, Nold SC, Revsbech NP, Ward DM (1997) Population structure and physiological changes within a hot spring microbial mat community following disturbance. Appl Environ Microbiol 63(4):1367–1374

    PubMed  CAS  PubMed Central  Google Scholar 

  • Fouke BW, Farmer JD, Des Marais DJ, Pratt L, Sturchio NC, Burns PC, Discipulo MK (2000) Depositional facies and aqueous-solid geochemistry of travertine-depositing hot springs (Angel Terrace, Mammoth Hot Springs, Yellowstone National Park, USA). J Sediment Res 70(3):565–585. doi:10.1306/2dc40929-0e47-11d7-8643000102c1865d

    Article  CAS  Google Scholar 

  • Garcia-Pichel F, Nubel U, Muyzer G (1998) The phylogeny of unicellular, extremely halotolerant cyanobacteria. Arch Microbiol 169(6):469–482

    Article  PubMed  CAS  Google Scholar 

  • Gorbushina AA, Broughton WJ (2009) Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annu Rev Microbiol 63:431–450

    Article  PubMed  CAS  Google Scholar 

  • Herrero A, Flores E (eds) (2008) The Cyanobacteria: molecular biology, genomics and evolution. Caister Academic, Wymondham, Norfolk

    Google Scholar 

  • Hopkinson BM, Morel FM (2009) The role of siderophores in iron acquisition by photosynthetic marine microorganisms. Biometals 22(4):659–669. doi:10.1007/s10534-009-9235-2

    Article  PubMed  CAS  Google Scholar 

  • Ionescu D, Hindiyeh M, Malkawi H, Oren A (2010) Biogeography of thermophilic cyanobacteria: insights from the Zerka Ma’in hot springs (Jordan). FEMS Microbiol Ecol 72(1):103–113. doi:10.1111/j.1574-6941.2010.00835.x

    Article  PubMed  CAS  Google Scholar 

  • Issaadi A (1992) Le thermalisme dans son cadre géostructural, apports à la connaissance de la structure profonde de l’Algérie et de ses ressources géothermales. Thèse de doctorat d’état, University of Science and Technology Houari Boumedienne, Algiers

  • Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4(1):18

    Article  PubMed  PubMed Central  Google Scholar 

  • Kecha M, Benallaoua S, Touzel JP, Bonaly R, Duchiron F (2007) Biochemical and phylogenetic characterization of a novel terrestrial hyperthermophilic archaeon pertaining to the genus Pyrococcus from an Algerian hydrothermal hot spring. Extremophiles 11(1):65–73. doi:10.1007/s00792-006-0010-9

    Article  PubMed  CAS  Google Scholar 

  • Kedaid FZ (2007) Database on the geothermal resources of Algeria. Geothermics 36(3):265–275. doi:10.1016/j.geothermics.2007.02.002

    Article  Google Scholar 

  • Komárek J, Anagnostidis K (1989) Modern approach to the classification system of cyano-bacteria 4. Nostocales. Arch Hydrobiol Algol Stud 56:247–345

    Google Scholar 

  • Komárek J, Anagnostidis K (1999) Cyanoprokaryota: Chroococcales. Gustav Fischer Verlag, Jena

    Google Scholar 

  • Mackenzie R, Pedros-Alio C, Diez B (2013) Bacterial composition of microbial mats in hot springs in Northern Patagonia: variations with seasons and temperature. Extremophiles 17(1):123–136

    Article  PubMed  Google Scholar 

  • Masson IL (1939) Studies on the fauna of an Algerian hot spring. J Exp Biol 16(4):487–498

    Google Scholar 

  • Mehta MP, Baross JA (2006) Nitrogen fixation at 92 degrees C by a hydrothermal vent archaeon. Science 314(5806):1783–1786

    Article  PubMed  CAS  Google Scholar 

  • Miller SR, Castenholz RW (2000) Evolution of thermotolerance in hot spring cyanobacteria of the genus Synechococcus. Appl Environ Microbiol 66(10):4222–4229

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nelissen B, Van de Peer Y, Wilmotte A, De Wachter R (1995) An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences. Mol Biol Evol 12(6):1166–1173

    PubMed  CAS  Google Scholar 

  • Norris TB, Wraith JM, Castenholz RW, McDermott TR (2002) Soil microbial community structure across a thermal gradient following a geothermal heating event. Appl Environ Microbiol 68(12):6300–6309

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nubel U, GarciaPichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63(8):3327–3332

    PubMed  CAS  PubMed Central  Google Scholar 

  • Papke RT, Ramsing NB, Bateson MM, Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5(8):650–659

    Article  PubMed  CAS  Google Scholar 

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ragon M, Restoux G, Moreira D, Moller AP, Lopez-Garcia P (2011) Sunlight-exposed biofilm microbial communities are naturally resistant to Chernobyl ionizing-radiation levels. PLoS One 6(7):e21764. doi:10.1371/journal.pone.0021764

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Robertson BR, Tezuka N, Watanabe MM (2001) Phylogenetic analyses of Synechococcus strains (cyanobacteria) using sequences of 16S rDNA and part of the phycocyanin operon reveal multiple evolutionary lines and reflect phycobilin content. Int J Syst Evol Microbiol 51(Pt 3):861–871

    Article  PubMed  CAS  Google Scholar 

  • Saibi H (2009) Geothermal resources in Algeria. Renew Sustain Energy Rev 13(9):2544–2552. doi:10.1016/j.rser.2009.06.019

    Article  Google Scholar 

  • Sen S, Peters JW (2006) The thermal adaptation of the nitrogenase Fe protein from thermophilic Methanobacter thermoautotrophicus. Proteins 62(2):450–460. doi:10.1002/prot.20765

    Article  PubMed  CAS  Google Scholar 

  • Shannon CE, Weaver W (1963) The mathematical theory of communication. University of Illionois Press, Urbana

    Google Scholar 

  • Verdeil P (1982) Algerian thermalism in its geostructural setting—how hydrogeology has helped in the elucidation of Algeria deep-seated structure. J Hydrol 56(1–2):107–117. doi:10.1016/0022-1694(82)90060-9

    Article  CAS  Google Scholar 

  • Ward DM, Ferris MJ, Nold SC, Bateson MM (1998) A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol Mol Biol Rev 62(4):1353–1370

    PubMed  CAS  PubMed Central  Google Scholar 

  • Warren-Rhodes KA, Rhodes KL, Pointing SB, Ewing SA, Lacap DC, Gomez-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(3):389–398

    Article  PubMed  Google Scholar 

  • Wierzchos J, Ascaso C, McKay CP (2006) Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama Desert. Astrobiology 6(3):415–422

    Article  PubMed  Google Scholar 

  • Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L, Vaulot D, Not F, Massana R, Ulloa O, Scanlan DJ (2008) Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10(1):147–161

    PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Moulla Adnane-Soufi and Ouarezki Sid-Ali for their help during field sampling. This work was financed by the Centre de Recherche Nucléaire d’Alger and by the program INTERRVIE from the French Centre National de la Recherche Scientifique, CNRS.

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Correspondence to Purificación López-García.

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Communicated by A. Oren.

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Amarouche-Yala, S., Benouadah, A., El Ouahab Bentabet, A. et al. Morphological and phylogenetic diversity of thermophilic cyanobacteria in Algerian hot springs. Extremophiles 18, 1035–1047 (2014). https://doi.org/10.1007/s00792-014-0680-7

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