Cytomorphological and genetic characterization of troglobitic leptolyngbya strains isolated from roman hypogea

Applied and Environmental Microbiology

Volumn 75, Issue 3, 2009, Pages 608-617

  Bruno, Laura ^a   Billi, Daniela ^a   Bellezza, Simona ^a   Albertano, Patrizia ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENES; GENETIC CHARACTERIZATIONS; INTRASPECIFIC VARIATIONS; OPERATIONAL TAXONOMIC UNITS; PHYCOCYANIN; PHYLOTYPES; SEQUENCE IDENTITIES; TRANSCRIBED SPACERS; TROGLOBITIC;

INTELLIGENT VEHICLE HIGHWAY SYSTEMS;

STRAIN;

CYANOBACTERIUM; CYTOLOGY; GENETIC ANALYSIS; GEOTHERMAL GRADIENT; MORPHOLOGY; POLYMORPHISM; RELATEDNESS; TAXONOMY;

CLUSTER ANALYSIS; CYANOBACTERIA; DNA, BACTERIAL; DNA, RIBOSOMAL; DNA, RIBOSOMAL SPACER; GENES, RRNA; MICROSCOPY; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; PHYLOGENY; PIGMENTS, BIOLOGICAL; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; RNA, TRANSFER, ALA; RNA, TRANSFER, ILE; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SOIL MICROBIOLOGY;

LEPTOLYNGBYA; OTUS; ROMAN HYPOGEA;

EID: 59649114763     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01183-08     Document Type: Article

References (59)

1. Albertano, P. 1991. Effects of monochromatic lights on four species of Leptolyngbya. Arch. Hydrobiol. Algolog. Studies 64:199-214.
2. Albertano, P. 1993. Epilithic algal communities in hypogean monument environment. Giorn. Bot. Ital. 127:385-392.
3. Albertano, P. 2003. Methodological approaches to the study of stone alteration caused by cyanobacterial biofilms in hypogean environments, p. 302-315. In R. J. Koestler, V. R. Koestler, A. E. Charola and F. E. Nieto- Fernandez (ed.), Art, biology, and conservation: biodeterioration of works of art. Metropolitan Museum of Art, New York, NY.
4. Albertano, P., L. Barsanti, L. Passatelli, and P. Gualtieri. 2000. A complex photoreceptive structure in the cyanobacterium Leptolyngbya sp. Micron 31:27-34.
5. Albertano, P., and S. Bellezza. 2001. Cytochemistry of cyanobacterial exopolymers in biofilms from Roman hypogea. Nova Hedwigia 123:501-518.
6. Albertano, P., and M. Grilli Caiola. 1988. Structural and ultrastructural characters of a red biodeteriorating Lyngbya sp. in culture. Arch. Hydrobiol. Algolog. Studies 50:55-57.
7. Albertano, P., and L. Kováčik. 1994. Is the genus Leptolyngbya an homogeneous taxon? Arch. Hydrobiol. Algolog. Studies 75:37-51.
8. Albertano, P., L. Kováčik, and M. Grilli Caiola. 1994. Preliminary investigations on epilithic cyanophytes from a Roman necropolis. Arch. Hydrobiol. Algolog. Studies 75:71-74.
9. Albertano, P., L. Kovacik, P. Marvan, and M. Grilli Caiola. 1995. A terrestrial epilithic diatom from Roman catacombs, p. 11-21. In D. Marino and M. Montresor (ed.), Proceedings of the Thirteenth International Diatom Symposium. Biopress Limited, Bristol, United Kingdom.
10. Albertano, P., and C. Urzì. 1999. Structural interactions among epilithic cyanobacteria and heterotrophic microorganisms in Roman hypogea. Mi- crob. Ecol. 38:244-252.
11. Anagnostidis, K., and J. Komàrek. 1988. Modern approach to classification system of cyanophytes. 3. Oscillatoriales. Arch. Hydrobiol. Algolog. Studies 53:327-472.
12. Baurain, D., L. Renquin, S. Grubisic, and P. Scheldeman. 2002. Remarkable conservation of internally transcribed spacer sequences of Arthospira ((Spir- ulina') (Cyanophyceae, Cyanobacteria) strains from four continents and of recent and 30-year-old dried samples from Africa. J. Phycol. 38:384-393.
13. Bellezza, S., R. De Philippis, G. Paradossi, and P. Albertano. 2003. Leptolyngbya sp. strains from Roman hypogea: cytochemical and physico-chemical characterisation of exopolysaccharides. J. Appl. Phycol. 15:193-200.
14. Boyer, S. L., V. R. Flechtner, and J. R. Johansen. 2001. Is the 16S-23S rRNA internal transcribed spacer (ITS) region a good tool for use in molecular systematic and population genetics? A case study in cyanobacteria. Mol. Biol. Evol. 18:1057-1069.
15. Bruno, L., D. Billi, and P. Albertano. 2005. Optimization of molecular techniques applied to the taxonomy of epilithic Leptolyngbya strains. Arch. Hydrobiol. Algolog. Studies 117:197-207.
16. Bruno, L., S. Piermarini, and P. Albertano. 2001. Characterisation of spectral emission by cyanobacterial biofilms in the Roman catacombs of Priscilla in Rome (Italy). Nova Hedwigia 123:229-236.
17. Bruno, L., C. Urzi', D. Billi, and P. Albertano. 2006. Genetic characterization of epilithic cyanobacteria and their associated bacteria. Geomicrobiol. J. 23:293-299.
18. Cadel-Six, S., C. Peyraud-Thomas, L. Brient, N. Tandeau de Marsac, R. Rippka, and A. Mèjean. 2007. Different genotypes of anatoxin-producing cyanobacteria coexist in the Tarn River, France. Appl. Environ. Microbiol. 73:7605-7614.
19. Casamatta, D. A., J. R. Johansen, M. L. Vis, and S. T. Broadwater. 2005. Molecular and morphological characterization of ten polar and near polar strains within the Oscillatoriales (Cyanobacteria). J. Phycol. 41:421-438.
20. Castenholz, R. W., and T. B. Norris. 2005. Revisionary concepts of species in the cyanobacteria and their applications. Arch. Hydrobiol. Algolog. Studies 117:53-69.
21. Ciferri, O. 1999. Microbial degradation of paintings. Appl. Environ. Micro-biol. 65:879-885.
22. Leu (UAA) intron: evolutionary patterns in a genetic marker. Mol. Biol. Evol. 19:850-857.
23. Ernst, A., S. Becker, U. I. A. Wollenzien, and C. Postius. 2003. Ecosystem- dependent adaptive radiations of picocyanobacteria inferred from 16S rRNA and ITS-1 sequence analysis. Microbiology 149:217-228.
24. Fox, G. E., J. D. Wisotzkey, and P. Jurtshuk. 1992. How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int. J. Syst. Bacteriol. 42:166-170.
25. Gugger, M., R. Molica, B. Le Berre, P. Dufour, C. Bernard, and J.-F Humbert. 2005. Genetic diversity of Cylindrospermopsis strains (Cyanobacteria) isolated from four continents. Appl. Environ. Microbiol. 71:1097-1100.
26. Hernandez-Mariné, M., E. Clavero, and M. Roldan. 2003. Why there is such luxurius growth in the hypogean environments? Arch. Hydrobiol. Algologi. Studies 109:229-240.
27. Hoffmann, L. 2002. Caves and other low-light environments: aerophytic photoautotrophic microorganisms, p. 171-177. In G. Bitton (ed.), Encyclopedia of environmental microbiology. John Wiley & Sons, New York, NY.
28. Hoffmann, L., J. Komárek, and J. Kastošký. 2005. System of cyanopro karyotes (cyanobacteria). Arch. Hydrobiol. Algolog. Studies 117:95-115.
29. Humbert, J. F., D. Duris-Latour, B. Le Berre, H. Giraudet, and M. J. Salencon. 2005. Genetic diversity in Microcystis populations of a French storage reservoir assessed by sequencing of the 16S-23S rRNA intergenic spacer. Microb. Ecol. 49:308-314.
30. Ionescu, D., A. Oren, Y. Hindiyeh, and H. I. Malkawi. 2007. The thermophilic cyanobacteria of the Zerka Ma'in thermal springs in Jordan, p. 413-424. In J. Seckbach (ed.), Algae and cyanobacteria in extreme environments. Springer, Dordrecht, The Netherlands.
31. Ishida, T., M. M. Watanabe, J. Sugiyama, and A. Yokota. 2001. Evidence for polyphyletic origin of the members of the orders of Oscillatoriales and Pleurocapsales as determined by 16S rDNA analysis. FEMS Microbiol. Lett. 201:79-82.
32. Iteman, I., R. Rippka, N. Tandeau de Marsac, and M. Herdman. 2000. Comparison of conserved structural and regulatory domains within divergent 16S rRNA-23S rRNA spacer sequences of cyanobacteria. Microbiology 146: 1275-1286.
33. Iteman, I., R. Rippka, N. Tandeau de Marsac, and M. Herdman. 2002. rDNA analyses of planktonic heterocystous cyanobacteria, including members of the genera Anabaenopsis and Cyanospira. Microbiology 148:481-196.
34. Komárek, J. 2003. Problem of the taxonomic category 'species' in cyanobacteria. Arch. Hydrobiol. Algolog. Studies 109:281-297.
35. Komárek, J., and K. Anagnostidis. 2005. Cyanoprokaryota. Part 2. Oscilla toriales, p. 1-759. In B. Büdel, G. Gärtner, L. Krienitz, and M. Schagerl (ed.) Süusswasserflora von Mitteleuropa Band, 19/2. Gustav Fischer, Jena, Germany.
36. Komárek, J., and J. Kaštovsky. 2003. Coincidences of structural and molecular characters in evolutionary lines of cyanobacteria. Arch. Hydrobiol. Algolog. Studies 109:305-325.
37. Laloui, W., K. A. Palinska, R. Rippka, F. Partensky, N. Tandeau de Marsac, M. Herdman, and I. Iteman. 2002. Genotyping of axenic and non-axenic isolates of the genus Prochlorococcus and the OMF-Synechococcus clade by size sequence analysis or RFLP of the internal transcribed spacer of the ribosomal operon. Microbiology 148:453-465.
38. Marquardt, J., and K. A. Palinska. 2007. Genotypic and phenotypic diversity of cyanobacteria assigned to the genus Phormidium (Oscillatoriales) from different habitats and geographical sites. Arch. Microbiol. 187:397-413.
39. Nelissen, B., R. De Baere, A. Wilmotte, and R. De Wachter. 1996. Phylogenetic relationships of nonaxenic filamentous cyanobacterial strains based on 16S rRNA sequence analysis. J. Mol. Evol. 42:194-200.
40. Nelissen, B., A. Wilmotte, J.-M. Neefs, and R. De Wachter. 1994. Phylogenetic relationships among filamentous helical cyanobacteria investigated on the basis of 16S ribosomal RNA gene sequence analysis. Syst. Appl. Microbiol. 17:206-210.
41. Nubel, U., F. Garcia-Pichel, and G. Muyzer. 1997. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl. Environ. Microbiol. 63:3327-3333.
42. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
43. Premanandh, J., B. Priya, I. Teneva, B. Dzhambazov, D. Prabaharan, and L. Uma. 2006. Molecular characterization of marine cyanobacteria from the Indian subcontinent deduced from sequence analysis of the phycocyanin operon (cpcB-IGS-cpcA) and 16S-23S ITS region. J. Microbiol. 44:607-616.
44. Reynolds,C. S. 1963. The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J. Cell Biol. 17:208-212.
45. Rippka, R., J. Deruelles, B. Waterbury, M. Herdman, and R. Y. Stanier. 1979. Generic assignments, strains histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111:1-61.
46. Roeselers, G., T. B. Norris, R. W. Castenholz, S. Rysgaard, R. N. Glud, M. Kuhl, and G. Muyzer. 2007. Diversity of phototrophic bacteria in microbial mats from Arctic hot springs (Greenland). Environ. Microbiol. 9:26-38.
47. Saarela, M., H-L. Halakomi, M-L. Suihko, L. Maunuksela, L. Raaska, and T. Mattila-Sandholm. 2004. Heterotrophic microorganisms in air and bio- film samples from Roman catacombs, with special emphasis on actinobacteria and fungi. Int. Biodeterior. Biodegrad. 54:27-37.
48. Sànchez-Moral, S., J. C. Cañiaveras, L. Laiz, C. Saiz-Jimenez, J. Bedoya, and L. Luque. 2003. Biomediated precipitation of calcium carbonate metastable phases in hypogean environments. Geomicrob. J. 20:491-500.
49. Scheldeman, P., D. Baurain, R. Bouhy, M. Scott, M. Muhling, B. A. Whitton, A. Belay, and A. Wilmotte. 1999. Arthrospira (Spirulina) strains from four continents are resolved into only two clusters, based on amplified ribosomal DNA restriction analysis of the internally transcribed spacer. FEMS Microbiol. Lett. 172:213-222.
50. Stackebrandt, E., and B. M. Goebel. 1994. Taxonomical note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present definition in bacteriology. Int. J. Syst. Bacteriol. 44:846-849.
51. Swofford, D. L. 2001. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4. Sinauer Associates, Sunderland, MA.
52. Taton, A., S. Grubisic, D. Ertz, D. A. Hodgson, R. Piccardi, N. Biondi, M. R. Tredici, M. Mainini, D. Losi, F. Marinelli, and A. Wilmotte. 2006. Polyphasic study of antartic cyanobacterial strains. J. Phycol. 42:1257-1270.
53. Taton, A., S. Grubisic, E. Brambilla, R. de Wit, and A. Wilmotte. 2003. Cyanobacterial diversity in natural and artificial microbial mats of lake Fryxell (Dry Valleys, Antarctica): a morphological and molecular approach. Appl. Environ. Microbiol. 69:5157-5169.
54. Turner, S., K. M. Pryer, V. P. W. Miao, and J. D. Palmer. 1999. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J. Eukaryot. Microbiol. 46:327-338.
55. Urzì, C., P. Donato, C. Lo Passo, and P. Albertano. 2002. Occurrence and biodiversity of Streptomyces strains isolated from Roman hypogea, p. 269-272. In E. Galan and F. Zezza (ed.), Protection and conservation of the cultural heritage of the Mediterranean cities. Balkema Publishers, Lisse, The Netherlands.
56. Willame, R., C. Boutte, S. Grubisic, A. Wilmotte, J. Komaarek, and L. Hoffmann. 2006. Morphological and molecular characterization of planktonic cyanobacteria from Belgium and Luxembourg. J. Phycol. 42:1312-1332.
57. Wilmotte, A., and M. Herdman. 2001. Phylogenetic relationships among the cyanobacteria based on 16S rRNA sequences, p. 487-599. In G. M. Garrity, D. R. Boone, and R. W. Castenholz (ed.), Bergey's manual of systematic bacteriology. Springer-Verlag, New York, NY.
58. Wilmotte, A., J. M. Neefs, and R. De Wachter. 1994. Evolutionary affiliation of the marine nitrogen-fixing cyanobacterium Trichodesmium sp. strain NIBB 1067, derived by 16S ribosomal RNA sequence analysis. Microbiology 140:2159-2164.
59. Wilmotte, A., G. Van der Auwer, and R. De Wachter. 1993. Structure of the 16S ribosomal RNA of the thermophilic cyanobacterium Chlorogloeopsis HTF ('Mastigocladus laminosus HTF') strain PCC7518, and phylogenetic analysis. FEBS Lett. 317:96-100.