Fottea 12(2): 315-326, 2012 | DOI: 10.5507/fot.2012.022

Identification and characterization of a new  Halomicronema species (Cyanobacteria) isolated from the Mediterranean marine sponge Petrosia ficiformis (Porifera).

Carmela Caroppo*,1, Patrizia Albertano2, Laura Bruno2, Mariarosa Montinari3, Marco Rizzi4, Giovanni Vigliotta5, Patrizia Pagliara3
1 Institute for Coastal Marine Environment, Unit of Taranto, National Research Council, Via Roma, 3 - 74100, Taranto, Italy
2 Laboratory of Biology of Algae, Department of Biology, University of Rome "Tor Vergata", Italy
3 DiSTeBA, Department of Biological and Environmental Sciences and Technologies, University of Salento, Lecce, Italy
4 Azienda Ospedaliera Policlinico di Bari, Italy
5 Department of Chemistry, University of Salerno, Fisciano (Salerno), Italy

A filamentous cyanobacterium (strain ITAC101) isolated from a Mediterranean sponge (Petrosia ficiformis) was characterized by a combined phenotypic and genetic approach. Morphological and ultrastructural observations were performed along with growth measurements and pigment characterization. The molecular phylogenetic analyses were based on the sequencing of the 16S rRNA gene. In culture conditions, strain ITAC101 is moderately halophilic and grew in the range 0.3-7.6% (w/v) salinity with the optimum at 3.6%. Cell dimensions, thylakoid arrangement and pigment composition of this cyanobacterium fit the Halomicronema genus description, and phylogenetic analyses evidenced 99.9% similarity with another strain endolithic in tropical corals. The new Halomicronema metazoicum species was established including the two cyanobacteria associated to marine animals.

Keywords: cyanobacteria, Leptolyngbya, marine sponge, Mediterranean Sea, polyphasic approach,16S rRNA

Received: July 17, 2011; Accepted: September 11, 2011; Published: September 1, 2012  Show citation

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Caroppo, C., Albertano, P., Bruno, L., Montinari, M., Rizzi, M., Vigliotta, G., & Pagliara, P. (2012). Identification and characterization of a new  Halomicronema species (Cyanobacteria) isolated from the Mediterranean marine sponge Petrosia ficiformis (Porifera). Fottea, 12(2), 315-326. doi: 10.5507/fot.2012.022
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    References

    1. Aakermann, T.; Skulberg, O.M. & Liaaen-Jensen, S. (1992): A comparison of the carotenoids of strains of Oscillatoria and Spirulina (Cyanobacteria). - Biochem. Syst. Ecol. 20: 761-769. Go to original source...
    2. Abed, R.M.M.; Al-Thukair, A. & de Beer, D. (2006): Bacterial diversity of a cyanobacterial mat degrading petroleum compounds at elevated salinities and temperatures. - FEMS Microbiol. Ecol. 57: 290- 301. Go to original source...
    3. Abed, R.M.M.; Garcia-Pichel, F. & Hernández-Mariné, M. (2002a): Polyphasic characterization of benthic, moderately halophilic, moderately thermophilic cyanobacteria with very thin trichomes and the proposal of Halomicronema excentricum gen. nov., sp. nov. - Arch. Microbiol. 177: 361-370. Go to original source...
    4. Abed, R.M.M. & Golubic, S. (2009): Selection of oil- tolerant cyanobacteria on oil polluted sediments. - Algological Studies 130: 69-79. Go to original source...
    5. Abed, R.M.M. & Köster, J. (2005): The direct role of aerobic heterotrophic bacteria associated with cyanobacteria in the degradation of oil compounds. - Int. Biodet. Biodegr. 55: 29-37. Go to original source...
    6. Abed, R.M.M.; Safi, N.M.D.; Köster, J.; de Beer, D.; El- Nahhal, Y.; Rullkötter, J. & Garcia-Pichel, F. (2002b): Microbial diversity of a heavily polluted microbial mat and its community changes following degradation of petroleum compounds. - Appl. Environ. Microbiol. 68: 1674-1683. Go to original source...
    7. Airs, R.L.; Atkinson, J.E. & Keely, B.J. (2001): Development and application of a high resolution liquid chromatographic method for the analysis of complex pigment distributions. - J. Chromatog. A 917: 167-177. Go to original source...
    8. Anagnostidis, K. & Komárek, J. (1988): Modern approach to the classification system of cyanophytes. 5. Oscillatoriales. - Arch. Hydrobiol./ Algological Studies 80: 327-472.
    9. Bennett, A. & Bogorad, L. (1972): Properties of subunits and aggregates of blue-green algal biliproteins. - Biochemistry 10: 3625-3634. Go to original source...
    10. Bruno, L.; Billi, D.; Bellezza, S. & Albertano, P. (2009): Cytomorphological and genetic characterization of troglobitic Leptolyngbya strains isolated from Roman hypogea. - Appl. Environ. Microbiol. 75: 608-617. Go to original source...
    11. Carpenter, E.J. (2002): Marine cyanobacterial symbioses. Biology and environment. - P. Roy. Irish Acad. B 102: 15-18. Go to original source...
    12. Casamatta, D.A., Johansen, J.R., Vis, M.L. & Broadwater, S.T. (2005): Molecular and morphological characterization of ten polar and near polar strains within the Oscillatoriales (Cyanobacteria). - J. Phycol. 41: 421-438. Go to original source...
    13. Castenholz, R.W. (1988): Culturing methods for cyanobacteria. - In: Abelson, J. (ed.): Methods in Enzymology: Cyanobacteria 167. - pp. 68-93, Academic Press San Diego, CA, USA. Go to original source...
    14. Castenholz, R.W. & Waterbury, J.B. (1989): Taxa of the cyanobacteria. - In: Staley, J.T., Bryant, M.P.N. & Pfennig, J.G. (eds): Bergey's Manual of Systematic Bacteriology 3. - pp. 1727-1728, William & Wilkins, Baltimore.
    15. Comte, K.; Sabacka, M.; Carre-Mlouka, A.; Elster, J. & Komárek, J. (2007): Relationships between the Arctic and the Antarctic cyanobacteria; three Phomidium- like strains evaluated by a polyphasic approach. - FEMS Microbiol. Ecol. 59: 366-376. Go to original source...
    16. Diaz, M.C.; Thacker, R.W.; Rützler, K. & Piantoni, C. (2007): Two new haplosclerid sponges from Caribbean Panama with symbiotic filamentous cyanobacteria, and an overview of sponge cyanobacteria associations. - In: Custodio, M.R.; Lôbo-Hajdu, G.; Hajdu, E. & Muricy, G. (eds): Porifera Research: Biodiversity, Innovation and Sustainability. - pp. 31-39, Museu Nacional, Série Livros 28, Museu, Rio de Janeiro.
    17. Evangelista, V.; Frassanito, A.M.; Passatelli, V.; Barsanti, L. & Gualtieri, P. (2006): Microspectroscopy of the photosynthetic compartment of algae. - Photochem. Photobiol. 82: 1039-1046. Go to original source...
    18. Feldmann, J. (1933): Sur quelques cyanophycées vivant dans le tissu des éponges de banyules. - Arch. Zool. Exp. Gén. 5: 331-404.
    19. Fenical, W. (1997): New pharmaceuticals from marine organisms. - Mar. Biotechnol. 15: 339-341. Go to original source...
    20. Fiore, M.F.; Moon, D.H.; Tsai, S.M.; Lee, H. & Trevors, J.T. (2000): Miniprep DNA isolation from unicellular and filamentous Cyanobacteria. - J. Microbiol. Meth. 39: 159-169. Go to original source...
    21. Fourçans, A.; García de Oteyza, T.; Wieland, A.; Solé, A.; Diestra, E.; van Bleijswijk, J.; Grimalt, J.O.; Kühl, M.; Esteve, I.; Muyzer, G.; Caumette, P. & Duran, R. (2004): Characterization of functional bacterial groups in a hypersaline microbial mat community (Salins-de-Giraud, Camargue, France). - FEMS Microbiol. Ecol. 51: 55-70. Go to original source...
    22. Garcia-Pichel, F.; Nübel, U., & Muyzer, G. (1998): The phylogeny of unicellular, extremely halotolerant cyanobacteria. - Arch. Microbiol. 169: 469-482. Go to original source...
    23. Geitler, L. (1932): Cyanophyceae. In: Rabenhorst, L. (ed): Kryptogamen - Flora von Deutschland, Österreich und der Schweiz 14. - pp. 673-1056, Akademische Verlagsgesellschaft, Leipzig.
    24. Gerçe, B.; Schwartz, T.; Voigt, M.; Rühle, S.; Kirchen, S.; Putz, A.; Proksch P.; Obst, U.; Syldatk, C. & Hausmann, R. (2009): Morphological, bacterial, and secondary metabolite changes of Aplysina aerophoba upon long-term maintenance under artificial conditions. -Microb. Ecol. 58: 865-878. Go to original source...
    25. Giovannoni, S.J.; Turner, S.; Olsen, G.J.; Barns, S.; Lane, D.J. & Pace, N.R. (1988): Evolutionary relationships among cyanobacteria and green chloroplasts. - J. Bacteriol. 170: 3584-3592. Go to original source...
    26. Gkelis, S.; Rajaniemi, P.; Vardaka, E.; Moustaka-Gouni, M.; Lakaras, T. & Sivonen, K. (2005): Limnothrix redekei (Van Goor) Meffert (Cyanobacteria) strains from Lake Kastoria, Greece form a separate phylogenetic group. - Microb. Ecol. 49: 176-182. Go to original source...
    27. Haygood, M.G.; Schmidt, E.W.; Davidson, S.K. & Faulkner, D.J. (2000): Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. - In: Bartlett, D.H. (ed): Molecular Marine Microbiology 1. - pp. 61-84, Horizon Scientific Press, California.
    28. Hentschel, U.; Hopke, J.; Horn, M.; Friedrich, A.B.; Wagner, M. & Moore, B.S. (2002): Molecular evidence for a uniform microbial community in sponges from different oceans. - Appl. Environ. Microbiol. 68: 4431-4440. Go to original source...
    29. Hentschel, U.; Schmid, M.; Wagner, M.; Fieseler, L.; Gernert, C. & Hacker, J. (2001): Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. - FEMS Microbiol. Ecol. 35: 305-312. Go to original source...
    30. Hentschel, U.; Usher, K.M. & Taylor, M.W. (2006): Marine sponges as microbial fermenters. - FEMS Microbiol. Ecol. 55: 167-177. Go to original source...
    31. Hertzberg, S.; Liaaen-Jensen, S. & Siegelman, H.W. (1971): Carotenoids of blue-green algae 7. The carotenoids of further blue-green algae-a chemosystematic contribution. - Phytochemistry 10: 3121-3127. Go to original source...
    32. Kana, T.M. & Glibert, P.M.G. (1987): Effect of irradiances up to 2000 µE m-2 s-1 on marine Synechococcus WH7803-I. Growth, pigmentation and cell composition. - Deep-Sea Res. 34: 479-495. Go to original source...
    33. Komárek, J. (2005): The modern classification of Cyanoprokaryotes (Cyanobacteria). - Oceanol. Hydrobiol. Studies 34: 5-17.
    34. Küpper, H.; Seibert, S. & Parameswaran, A. (2007): Fast sensitive, and inexpensive alternative to analytical pigment HPLC: quantification of chlorophylls and carotenoids in crude extracts by fitting with Gauss peak spectra. - Anal. Chem. 79: 7611-7627. Go to original source...
    35. Lafi, F.F.; Garson, M.J. & Fuerst, J.A. (2005): Culturable Bacterial Symbionts Isolated from Two Distinct Sponge Species (Pseudoceratina clavata and Rhabdastrella globostellata) from the Great Barrier Reef Display Similar Phylogenetic Diversity. - Microb. Ecol. 50: 213-220. Go to original source...
    36. Lane, D.J.; Pace, B.; Olsen, G.J.; Stahl, D.A.; Sogin, M.L. & Pace, N.R. (1985): Rapid determination of 16s rRNA sequences for phylogenetic analyses. - P. Natl. Acad. Sci. USA 82: 6955-6959. Go to original source...
    37. Larkum, A.W.D. (1999): The cyanobacteria of coral reefs. - In: Charpy, L. & Larkum, A.W.D. (eds): Marine Cyanobacteria, Bulletin de I'Institut Oceanographique Monaco, Numero special 19. - pp. 149-167, Musee Oceanographique, Monaco.
    38. Larkum, A.W.D.; Cox, G.C. & Dibbayawan, T.P. (1988): Prokaryotic algal symbionts of coral reef sponges. - In: Choat, J.H.; Barnes, D.; Borowitzka, M.A.; Coll, J.C.; Davies, P.J.; Flood, P.; Hatcher, B.G.; Hopley, D.; Hutchings, P.A.; Kinsey, D.; Orme, G.R.; Pichon, M.; Sale, P.F.; Sammarco, P.; Wallace, C.C.; Wilkinson, C.; Wolanski, E. & Bellwood, O. (eds): Proceedings of the 6th International Coral Reef Symposium Contributed Papers 3. - pp. 163-169, Townsville, Australia.
    39. Lotti, F.; Giovannetti, L.; Margheri, M.C.; Ventura, S. & Materassi, R. (1996): Diversity of DNA methylation pattern and total DNA restriction pattern in symbiotic Nostoc. - World J. Microbiol. Biotechnol. 12: 38- 42. Go to original source...
    40. Maniatis, T.; Fritsch, E.F. & Sambrook, J. (1982): Molecular Cloning, A Laboratory Manual. - 545 pp., Cold Spring Harbor, New York.
    41. Marquardt, J. & Palinska, K.A. (2007): Genotypic and phenotypic diversity of cyanobacteria assigned to the genus Phormidium (Oscillatoriales) from different habitats and geographical sites. - Arch. Microbiol. 187: 397-413. Go to original source...
    42. Meeks, J.C. & Castenholz, R.W. (1971): Growth and photosynthesis in an extreme thermophile Synechococcus lividus (Cyanophyta). - Arch. Mikrobiol. 78: 25-41. Go to original source...
    43. Moore, R.E.; Patterson, G.M.L. &. Carmichael, W.W. (1988): New Pharmaceuticals From Cultured Blue- Green Algae. - In: Fautin, D.G. (ed.): Biomedical Importance of Marine Organisms 13. - pp. 143-150, Memoirs of the Californian Academy of Science, Californian Academy of Science, San Francisco, CA.
    44. Nübel, U.; Garcia-Pichel, F.; Clavero, E. & Muyzer, G. (2000): Matching molecular diversity and ecophysiology of benthic cyanobacteria and diatoms in communities along a salinity gradient. - Environ. Microbiol. 2: 217-226. Go to original source...
    45. Pagliara, P. & Caroppo, C. (2010): A Leptolyngbya species isolated from the sponge Petrosia ficiformis as potential source of novel compounds. - Rapp. Comm. Int. Mer Médit. 39: 392.
    46. Pagliara, P. & Caroppo, C. (2011): Cytotoxic and antimitotic assessment of aqueous extracts from eight cyanobacterial strains isolated from the marine sponge Petrosia ficiformis. - Toxicon 57: 889-896. Go to original source...
    47. Parmar, A.; Singh, N.K.; Kaushal, A.; Sonawala, S. & Madamwar, D. (2011): Purification, characterization and comparison of phycoerythrins from three different marine cyanobacterial cultures. - Bioresour. Technol. 102: 1795-1802. Go to original source...
    48. Posada, D. (2008): jModelTest: Phylogenetic Model Averaging. - Mol. Biol. Evol. 25: 1253-1256. Go to original source...
    49. Ralph, P.J.; Larkum, A.W.D. & Kühl, M. (2007): Photobiology of endolithic microorganisms in living coral skeletons: 1. Pigmentation, spectral reflectance and variable chlorophyll fluorescence analysis of endoliths in the massive corals Cyphastrea serailia, Porites lutea and Goniastrea australensis. - Mar. Biol. 152: 395-404. Go to original source...
    50. Rippka, R.; Deruelles, J.; Waterbury, J.B.; Herdman, M. & Stanier, R.Y. (1979): Generic assignments, strain histories and properties of pure cultures of cyanobateria. - J. Gen. Microbiol. 111: 1-61. Go to original source...
    51. Ronquist, F. & Huelsenbeck, J.P. (2003): MrBayes 3: Bayesian phylogenetic inference under mixed models. - Bioinformatics 19: 1572-1574. Go to original source...
    52. Rützler, K. (1990): Associations between Caribbean sponges and photosynthetic organisms. In: Rützler, K. (ed.): New Perspectives in Sponge Biology. - pp. 455-466, Smithsonian Institute Press, Washington, D.C.
    53. Sambrook, J. & Russel, D.W. (2001): Molecular Cloning: A Laboratory Manual, 3rd edn. - pp. 631-632, Cold Spring Harbour Laboratory Press, Cold Spring Harbour, New York.
    54. Sivonen, K. & Börner, T. (2008): Bioactive compounds produced by cyanobacteria. In: Herraro, A. & Flores, E. (eds): The cyanobacteria: Molecular Biology, Genomics and Evolution. - pp. 159-197, Caister Academic Press, Norfolk.
    55. Stackebrandt, E. & Ebers, J. (2006): Taxonomic parameters revisited: tarnished gold standards. - Microbiol. Today 33: 152-155.
    56. Steindler, L.; Huchon, D.; Avni, A. & Ilan, M. (2005): 16S rRNA phylogeny of sponge-associated cyanobacteria. - Appl. Environ. Microbiol. 17: 385-396. Go to original source...
    57. Swofford, D.L. (2001): PAUP_Phylogenetic Analysis Using Parsimony (and Other Methods). Version 4. Sinauer Associates, Sunderland, MA.
    58. Takaichi, S., & Mirauro, M. (1998): Distribution and geometric isomerism of neoxanthin in oxygenic phototrophs: 9'-Cis, a sole molecular form. - Plant Cell. Physiol. 39: 968-977. Go to original source...
    59. Taylor, M.W.; Thacker, R.W. & Hentschel, U. (2007): Genetics: evolutionary insights from sponges. - Science 316: 1854-1855. Go to original source...
    60. Thacker, R.W. & Starnes, S. (2003): Host specificity of the symbiotic cyanobacterium Oscillatoria spongeliae in marine sponges, Dysidea spp. - Mar. Biol. 142: 643-648. Go to original source...
    61. Usher, K.M. (2008): The ecology and phylogeny of cyanobacterial symbionts in sponges. - Mar. Ecol. 29: 178-192. Go to original source...
    62. Usher, K.M.; Fromont, J.; Sutton, D.C. & Toze, S. (2004): The biogeography and phylogeny of unicellular cyanobacterial symbionts in selected sponges from Australia and the Mediterranean. - Microb. Ecol. 48: 167-177. Go to original source...
    63. Webb, V.L. & Maas, E.W. (2002): Sequence analysis of 16S rRNA of cyanobacteria associated with the marine sponge Mycale (Carmia) hentscheli. - FEMS Microbiol. Lett. 207: 43-47. Go to original source...
    64. Wilhelm, C.; Volkmar, C.; Lohmann, C.; Becker, A. & Meyer, M. (1995): The HPLC-aided pigment analysis of phytoplankton cells as a powerful tool in water quality control. - J. Water SRT-Aqua 44: 132-141.
    65. Wilkinson, C.R. (1992): Symbiotic interactions between marine sponges and algae. - In: Reisser, W. (ed.): Algae and Symbiosis: Plants, Animals, Fungi, Viruses. Interactions explored. - pp. 112-151, Biopress, England.
    66. Wilmotte, A. (1994): Molecular evolution and taxonomy of the cyanobacteria. In: Bryant D.A. (ed): The Molecular Biology of the Cyanobacteria. - pp. 1-25, Kluwer, Dordrecht. Go to original source...
    67. Yamazaki, S.S.; Nakamura, T. & Yamasaki, H. (2006): Cyanobacterium Halomicronema sp. colonized within the skeleton of the reef-building coral Goniastrea aspera. - Plant Cell. Physiol. Suppl. 47: 581-581.
    68. Yamazaki, S.S.; Nakamura, T.; Yuen, Y.S. & Yamasaki, H. (2008a): Reef-building coral Goniastrea aspera harbour a novel filamentous cyanobacterium in their skeleton. Proceedings of the 11th International Coral Reef Symposium. - pp. 265-268, Ft. Lauderdale, Florida.
    69. Yamazaki, S.S.; Nakamura, T. & Yamasaki, H. (2008b): Photoprotective role of endolithic algae colonized in coral skeleton for the host photosynthesis. - In: Allen, J.F.; Gantt, E.; Golbeck, J.H. & Osmond, B. (eds): Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis. - pp. 1391-1395, Springer, Netherlands. Go to original source...
    70. Zhu, P.; Li, Q. & Wang, G. (2008): Unique microbial signatures of the alien Hawaiian marine sponge Suberites zeteki. - Microb. Ecol. 55: 406-414. Go to original source...

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