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.
Similar content being viewed by others
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
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
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
Brock TD (1967) Life at high temperatures. Science 158(3804):1012–1019
Castenholz RW (1969) Thermophilic blue-green algae and the thermal environment. Bacteriol Rev 33(4):476–504
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
Castenholz RW (2008) Le rôle des cyanobactéries et autres phototrophes dans les écosystèmes des sources chaudes. Press Therm Climat 145:129–134
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552
Cavalier-Smith T (2002) Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 12(2):R62–R64
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
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
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
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
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
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797
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
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
Garcia-Pichel F, Nubel U, Muyzer G (1998) The phylogeny of unicellular, extremely halotolerant cyanobacteria. Arch Microbiol 169(6):469–482
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
Herrero A, Flores E (eds) (2008) The Cyanobacteria: molecular biology, genomics and evolution. Caister Academic, Wymondham, Norfolk
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
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
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
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
Kedaid FZ (2007) Database on the geothermal resources of Algeria. Geothermics 36(3):265–275. doi:10.1016/j.geothermics.2007.02.002
Komárek J, Anagnostidis K (1989) Modern approach to the classification system of cyano-bacteria 4. Nostocales. Arch Hydrobiol Algol Stud 56:247–345
Komárek J, Anagnostidis K (1999) Cyanoprokaryota: Chroococcales. Gustav Fischer Verlag, Jena
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
Masson IL (1939) Studies on the fauna of an Algerian hot spring. J Exp Biol 16(4):487–498
Mehta MP, Baross JA (2006) Nitrogen fixation at 92 degrees C by a hydrothermal vent archaeon. Science 314(5806):1783–1786
Miller SR, Castenholz RW (2000) Evolution of thermotolerance in hot spring cyanobacteria of the genus Synechococcus. Appl Environ Microbiol 66(10):4222–4229
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
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
Nubel U, GarciaPichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63(8):3327–3332
Papke RT, Ramsing NB, Bateson MM, Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5(8):650–659
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
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
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
Saibi H (2009) Geothermal resources in Algeria. Renew Sustain Energy Rev 13(9):2544–2552. doi:10.1016/j.rser.2009.06.019
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
Shannon CE, Weaver W (1963) The mathematical theory of communication. University of Illionois Press, Urbana
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
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
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Oren.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-014-0680-7