1887

Abstract

Cyanobacteria dwelling on the salt-excreting leaves of the mangrove tree were isolated and characterized by ecological, morphological and genetic approaches. Leaves were collected in a mangrove with a history of oil contamination on the coastline of São Paulo state, Brazil, and isolation was achieved by smearing leaves on the surface of solid media or by submerging leaves in liquid media. Twenty-nine isolated strains were shown to belong to five cyanobacterial orders (thirteen to , seven to , seven to , one to , and one to ) according to morphological and 16S rRNA gene sequence evaluations. More detailed investigations pointed six Rivulariacean and four Xenococcacean strains as novel taxa. These strains were classified as gen. nov. (type species sp. nov. with type strain CENA341) and gen. nov. (type species sp. nov. with type strain CENA333), according to the International Code of Nomenclature for Algae, Fungi, and Plants. This investigation shows some of the unique cyanobacteria inhabiting the phyllosphere of can be retrieved by culturing techniques, improving current taxonomy and providing new insights into the evolution, ecology, and biogeography of this phylum.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.000774
2016-02-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/66/2/689.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.000774&mimeType=html&fmt=ahah

References

  1. Allen M. M. 1968; Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 4:1–4 [View Article]
    [Google Scholar]
  2. Alvarenga D. O., Rigonato J., Branco L. H. Z, Fiore M. F. 2015; Cyanobacteria in mangrove ecosystems. Biodivers Conserv 24:799–817 [View Article]
    [Google Scholar]
  3. Belkin S., Qvit-Raz N., Seckbach J., Grube M. 2010; Life on a leaf: bacterial epiphytes of a salt-excreting desert tree. In Symbioses and Stress. Joint Ventures in Biology, Cellular Origin, Life in Extreme Habitats and Astrobiology vol. 17 pp 393–406 Dordrecht: Springer; [View Article]
    [Google Scholar]
  4. Bobbarala V., Vadlapudi V. R., Naidu K. C. 2009; Antimicrobial potentialities of mangrove plant Avicennia marina. J Pharm Res 2:1019–1021
    [Google Scholar]
  5. Castenholz R. W. 1988; Culturing methods for cyanobacteria. Methods Enzymol 167:68–93 [View Article]
    [Google Scholar]
  6. Darriba D., Taboada G. L., Doallo R., Posada D. 2012; jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772 [View Article][PubMed]
    [Google Scholar]
  7. Dias A. C. F, Taketani R. G., Andreote F. D., Luvizotto D. M., da Silva J. L., Nascimento R. S., de Melo I. S. 2012; Interspecific variation of the bacterial community structure in the phyllosphere of the three major plant components of mangrove forests. Braz J Microbiol 43:653–660 [View Article][PubMed]
    [Google Scholar]
  8. Drennan P., Pammenter N. W. 1982; Physiology of salt excretion in the mangrove Avicennia marina (Forsk.) Vierh. New Phytol 91:597–606 [View Article]
    [Google Scholar]
  9. Ewing B., Green P. 1998; Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194 [View Article][PubMed]
    [Google Scholar]
  10. Ewing B., Hillier L., Wendl M. C., Green P. 1998; Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185 [View Article][PubMed]
    [Google Scholar]
  11. Felsenstein J. 1981; Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376 [View Article][PubMed]
    [Google Scholar]
  12. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 [View Article]
    [Google Scholar]
  13. Finkel O. M., Burch A. Y., Lindow S. E., Post A. F., Belkin S. 2011; Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl Environ Microbiol 77:7647–7655 [View Article][PubMed]
    [Google Scholar]
  14. 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 Methods 39:159–169 [View Article][PubMed]
    [Google Scholar]
  15. Fitzgerald M. A., Orlovich D. A., Allaway W. G. 1992; Evidence that abaxial leaf glands are the sites of salt secretion in leaves of the mangrove Avicennia marina (Forsk.) Vierh. New Phytol 120:1–7 [View Article]
    [Google Scholar]
  16. Freiberg E. 1998; Microclimatic parameters influencing nitrogen fixation in the phyllosphere in a costa rican premontane rain forest. Oecologia 117:9–18 [View Article]
    [Google Scholar]
  17. Fürnkranz M., Wanek W., Richter A., Abell G., Rasche F., Sessitsch A. 2008; Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2:561–570 [View Article][PubMed]
    [Google Scholar]
  18. Furtado A. L. F. F., Calijuri M. C., Lorenzi A. S., Honda R. Y., Genuário D. B., Fiore M. F. 2009; Morphological and molecular characterization of cyanobacteria from a Brazilian facultative wastewater stabilization pond and evaluation of microcystin production. Hydrobiologia 627:195–209 [View Article]
    [Google Scholar]
  19. Gau A. E., Dietrich C., Kloppstech K. 2002; Non-invasive determination of plant-associated bacteria in the phyllosphere of plants. Environ Microbiol 4:744–752 [View Article][PubMed]
    [Google Scholar]
  20. Golubič S. 1980; Halophily and halotolerance in cyanophytes. Orig Life 10:169–183 [View Article]
    [Google Scholar]
  21. Gordon D., Abajian C., Green P. 1998; Consed: a graphical tool for sequence finishing. Genome Res 8:195–202 [View Article][PubMed]
    [Google Scholar]
  22. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
    [Google Scholar]
  23. Hirano S. S., Upper C. D. 2000; Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae – a pathogen, ice nucleus, and epiphyte. Microbiol Mol Biol Rev 64:624–653 [View Article][PubMed]
    [Google Scholar]
  24. Hoffmann L., Komárek J., Kaštovský J. 2005; System of cyanoprokaryotes (Cyanobacteria) – state in 2004. Algological Studies 117:95–115 [View Article]
    [Google Scholar]
  25. Humphrey P. T., Nguyen T. T., Villalobos M. M., Whiteman N. K. 2014; Diversity and abundance of phyllosphere bacteria are linked to insect herbivory. Mol Ecol 23:1497–1515 [View Article][PubMed]
    [Google Scholar]
  26. Ishida T., Watanabe M. M., Sugiyama J., Yokota A. 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 [View Article][PubMed]
    [Google Scholar]
  27. Johansen J. R., Kovacik L., Casamatta D. A., Fučiková K., Kaštovský J. 2011; Utility of 16S–23S ITS sequence and secondary structure for recognition of intrageneric and intergeneric limits within cyanobacterial taxa: Leptolyngbya corticola sp. nov. (Pseudanabaenaceae, Cyanobacteria). Nova Hedwigia 92:283–302 [View Article]
    [Google Scholar]
  28. Junker R. R., Tholl D. 2013; Volatile organic compound mediated interactions at the plant-microbe interface. J Chem Ecol 39:810–825 [View Article][PubMed]
    [Google Scholar]
  29. Karnovsky M. J. 1965; A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137
    [Google Scholar]
  30. Kinkel L. L., Andrews J. H., Berbee F. M., Nordheim E. V. 1987; Leaves as islands for microbes. Oecologia 71:405–408 [View Article]
    [Google Scholar]
  31. Knoll A. H. 2009; The coevolution of life and environments. Rend Fis Acc Lincei 20:301–306 [View Article]
    [Google Scholar]
  32. Komárek J. 2006; Cyanobacterial taxonomy: current problems and prospects for the integration of traditional and molecular approaches. Algae 21:349–375 [View Article]
    [Google Scholar]
  33. Komárek J. 2013 Cyanoprokaryota - 3. Teil/ Part 3: Heterocytous Genera (Süsswasserflora von Mitteleuropa Bd. 19/3) Series editors B. Büdel, G. Gärtner, L. Krienitz & M. Schagerl Heidelberg: Springer/Spektrum; [View Article]
    [Google Scholar]
  34. Komárek J., Anagnostidis K. 1998 Cyanoprokaryota - 1. Teil/ 1nd Part: Chroococcales (Süsswasserflora von Mitteleuropa Bd. 19/1) Series editors H. Ettl, G. Gärtner, H. Heynig & D. Mollenhauer Jena: Gustav Fischer;
    [Google Scholar]
  35. Komárek J., Anagnostidis K. 2005 Cyanoprokaryota - 2. Teil/ 2nd Part: Oscillatoriales (Süsswasserflora von Mitteleuropa Bd. 19/1) Series editors B. Büdel, L. Krienitz, G. Gärtner & M. Schagerl Heidelberg: Elsevier/Spektrum;
    [Google Scholar]
  36. Komárek J., Kaštovský J., Mareš J., Johansen J. R. 2014; Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86:295–335
    [Google Scholar]
  37. Leveau J. H. J, Lindow S. E. 2001; Appetite of an epiphyte: quantitative monitoring of bacterial sugar consumption in the phyllosphere. Proc Natl Acad Sci U S A 98:3446–3453 [View Article][PubMed]
    [Google Scholar]
  38. Lindow S. E., Brandl M. T. 2003; Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883 [View Article][PubMed]
    [Google Scholar]
  39. Lindow S. E., Leveau J. H. J. 2002; Phyllosphere microbiology. Curr Opin Biotechnol 13:238–243 [View Article][PubMed]
    [Google Scholar]
  40. Mahasneh I. A., Grainger S. L. J, Whitton B. A. 1990; Influence of salinity on hair formation and phosphatase activities of the blue-green alga (Cyanobacterium) Calothrix viguieri D253. Br Phycol J 25:25–32 [View Article]
    [Google Scholar]
  41. Mau B., Newton M. A., Larget B. 1999; Bayesian phylogenetic inference via Markov chain Monte Carlo methods. Biometrics 55:1–12 [View Article][PubMed]
    [Google Scholar]
  42. Miller W. G., Brandl M. T., Quiñones B., Lindow S. E. 2001; Biological sensor for sucrose availability: relative sensitivities of various reporter genes. Appl Environ Microbiol 67:1308–1317 [View Article][PubMed]
    [Google Scholar]
  43. Neilan B. A., Jacobs D., Del Dot T., Blackall L. L., Hawkins P. R., Cox P. T., Goodman A. E. 1997; rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. Int J Syst Bacteriol 47:693–697 [View Article][PubMed]
    [Google Scholar]
  44. Peñuelas J., Terradas J. 2014; The foliar microbiome. Trends Plant Sci 19:278–280 [View Article][PubMed]
    [Google Scholar]
  45. Qvit-Raz N., Jurkevitch E., Belkin S. 2008; Drop-size soda lakes: transient microbial habitats on a salt-secreting desert tree. Genetics 178:1615–1622 [View Article][PubMed]
    [Google Scholar]
  46. Qvit-Raz N., Finkel O. M., Al-Deeb T. M., Malkawi H. I., Hindiyeh M. Y., Jurkevitch E., Belkin S. 2012; Biogeographical diversity of leaf-associated microbial communities from salt-secreting Tamarix trees of the Dead Sea region. Res Microbiol 163:142–150 [View Article][PubMed]
    [Google Scholar]
  47. Rastogi G., Coaker G. L., Leveau J. H. J. 2013; New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett 348:1–10 [View Article][PubMed]
    [Google Scholar]
  48. Redford A. J., Bowers R. M., Knight R., Linhart Y., Fierer N. 2010; The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12:2885–2893 [View Article][PubMed]
    [Google Scholar]
  49. Rigonato J., Alvarenga D. O., Andreote F. D., Dias A. C. F, Melo I. S., Kent A., Fiore M. F. 2012; Cyanobacterial diversity in the phyllosphere of a mangrove forest. FEMS Microbiol Ecol 80:312–322 [View Article][PubMed]
    [Google Scholar]
  50. Ronquist F., Huelsenbeck J. P. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574 [View Article][PubMed]
    [Google Scholar]
  51. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  52. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467 [View Article][PubMed]
    [Google Scholar]
  53. Schreiber L., Krimm U., Knoll D. 2004; Interactions between epiphyllic microorganisms and leaf cuticles. In Plant Surface Microbiology pp 145–156Edited by Varma A., Abbott L., Werner D., Hampp R. Heidelberg: Springer; [View Article]
    [Google Scholar]
  54. Seehausen O. 2009; Ecology: Speciation affects ecosystems. Nature 458:1122–1123 [View Article][PubMed]
    [Google Scholar]
  55. Simberloff D. S. 1974; Equilibrium theory of island biogeography and ecology. Annu Rev Ecol Syst 5:161–182 [View Article]
    [Google Scholar]
  56. Simon R. D., Abeliovich A., Belkin S. 1994; A novel terrestrial halophilic environment: the phylloplane of Atripex halimus, a salt-excreting plant. FEMS Microbiol Ecol 14:99–109 [View Article]
    [Google Scholar]
  57. Spurr A. R. 1969; A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43 [View Article][PubMed]
    [Google Scholar]
  58. Stamatakis A., Ludwig T., Meier H. 2005; RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456–463 [View Article][PubMed]
    [Google Scholar]
  59. Stanier R. Y., Kunisawa R., Mandel M., Cohen-Bazire G. 1971; Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205
    [Google Scholar]
  60. Taton A., Grubsic S., Ertz D., Hodgson D. A., Piccardi R., Biondi N., Tredici M. R., Mainini M., Losi D., other authors. 2006; Polyphasic study of Antarctic cyanobacterial strains. J Phycol 42:1257–1270 [View Article]
    [Google Scholar]
  61. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  62. Vandamme P., Pot B., Gillis M., de Vos P., Kersters K., Swings J. 1996; Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60:407–438
    [Google Scholar]
  63. Vorholt J. A. 2012; Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840 [View Article][PubMed]
    [Google Scholar]
  64. Ward D. M., Ferris M. J., Nold S. C., Bateson M. M. 1998; A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol Mol Biol Rev 62:1353–1370
    [Google Scholar]
  65. Waterbury J. B., Dworkin M., Falkow S., Rosenberg E., Schleifer K. H., Stackebrandt E. 2006; The cyanobacteria – isolation, purification and identification. In The prokaryotes vol 4, 3rd edn. pp 1053–1073 New York: Springer; [View Article]
    [Google Scholar]
  66. Whipps J. M., Hand P., Pink D., Bending G. D. 2008; Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.000774
Loading
/content/journal/ijsem/10.1099/ijsem.0.000774
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error