1887

Abstract

Tropical ecosystems worldwide host very diverse microbial communities, but are increasingly threatened by deforestation and climate change. Thus, characterization of biodiversity in these environments, and especially of microbial communities that show unique adaptations to their habitats, is a very urgent matter. Information about representatives of the phylum in tropical environments is scarce, even though they are fundamental primary producers that help other microbes to thrive in nutrient-depleted habitats, including phyllospheres. In order to increase our knowledge of cyanobacterial diversity, a study was conducted to characterize isolates from and leaves collected at a mangrove and an Atlantic forest reserve located at the littoral of São Paulo state, south-east Brazil. The morphological, ultrastructural, phylogenetic, molecular and ecological features of the strains led to the recognition of the new genus , comprising two new species, gen. nov., sp. nov. and sp. nov., described here according to the International Code of Nomenclature for algae, fungi and plants. The new genus and species were classified in the nostocalean family . This finding advances knowledge on the microbial diversity of South American ecosystems and sheds further light on the systematics of cyanobacteria.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.002109
2017-09-01
2020-01-26
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/67/9/3301.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.002109&mimeType=html&fmt=ahah

References

  1. Lambais MR, Crowley DE, Cury JC, Büll RC, Rodrigues RR. Bacterial diversity in tree canopies of the Atlantic forest. Science 2006;312:1917 [CrossRef][PubMed]
    [Google Scholar]
  2. Vacher C, Hampe A, Porté AJ, Sauer U, Compant S et al. The phyllosphere: microbial jungle at the plant–climate interface. Annu Rev Ecol Evol Syst 2016;47:1–24 [CrossRef]
    [Google Scholar]
  3. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 2010;12:2885–2893 [CrossRef][PubMed]
    [Google Scholar]
  4. Vorholt JA. Microbial life in the phyllosphere. Nat Rev Microbiol 2012;10:828–840 [CrossRef][PubMed]
    [Google Scholar]
  5. Kembel SW, O'Connor TK, Arnold HK, Hubbell SP, Wright SJ et al. Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci USA 2014;111:13715–13720 [CrossRef][PubMed]
    [Google Scholar]
  6. Abril AB, Torres PA, Bucher EH. The importance of phyllosphere microbial populations in nitrogen cycling in the Chaco semi-arid woodland. J Trop Ecol 2005;21:103–107 [CrossRef]
    [Google Scholar]
  7. Freiberg E. Microclimatic parameters influencing nitrogen fixation in the phyllosphere in a costa rican premontane rain forest. Oecologia 1998;117:9–18 [CrossRef][PubMed]
    [Google Scholar]
  8. Fürnkranz M, Wanek W, Richter A, Abell G, Rasche F et al. Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2008;2:561–570 [CrossRef][PubMed]
    [Google Scholar]
  9. Ray K, Mukherjee C, Ghosh AN. A way to curb phosphorus toxicity in the environment: use of polyphosphate reservoir of cyanobacteria and microalga as a safe alternative phosphorus biofertilizer for Indian agriculture. Environ Sci Technol 2013;47:11378–11379 [CrossRef][PubMed]
    [Google Scholar]
  10. Sergeeva E, Liaimer A, Bergman B. Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 2002;215:229–238 [CrossRef][PubMed]
    [Google Scholar]
  11. Spaepen S, Vanderleyden J, Remans R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 2007;31:425–448 [CrossRef][PubMed]
    [Google Scholar]
  12. Rodríguez AA, Stella AM, Storni MM, Zulpa G, Zaccaro MC. Effects of cyanobacterial extracellular products and gibberellic acid on salinity tolerance in Oryza sativa L. Saline Syst 2006;2:7 [CrossRef][PubMed]
    [Google Scholar]
  13. Becher PG, Jüttner F. Insecticidal compounds of the biofilm-forming cyanobacterium Fischerella sp. (ATCC 43239). Environ Toxicol 2005;20:363–372 [CrossRef][PubMed]
    [Google Scholar]
  14. Singh NK, Dhar DW, Tabassum R. Role of cyanobacteria in crop protection. Proc Natl Acad Sci India Sect B: Biol Sci 2016;86:1–8 [CrossRef]
    [Google Scholar]
  15. Rigonato J, Gonçalves N, Andreote AP, Lambais MR, Fiore MF. Estimating genetic structure and diversity of cyanobacterial communities in Atlantic forest phyllosphere. Can J Microbiol 2016;62:953–960 [CrossRef][PubMed]
    [Google Scholar]
  16. Rigonato J, Alvarenga DO, Andreote FD, Dias AC, Melo IS et al. Cyanobacterial diversity in the phyllosphere of a mangrove forest. FEMS Microbiol Ecol 2012;80:312–322 [CrossRef][PubMed]
    [Google Scholar]
  17. Alvarenga DO, Rigonato J, Branco LH, Melo IS, Fiore MF. Phyllonema aviceniicola gen. et sp. nov. and Foliisarcina bertiogensis gen. et. sp. nov., novel epiphyllic cyanobacteria associated with Avicennia schaueriana leaves. Int J Syst Evol Microbiol 2015;66:689–700 [CrossRef][PubMed]
    [Google Scholar]
  18. Allen MM. Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 1968;4:1–4 [CrossRef][PubMed]
    [Google Scholar]
  19. Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 1971;35:171–205[PubMed]
    [Google Scholar]
  20. Karnovsky MJ. A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 1965;27:137
    [Google Scholar]
  21. Spurr AR. A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 1969;26:31–43 [CrossRef][PubMed]
    [Google Scholar]
  22. Fiore MF, Moon DH, Tsai SM, Lee H, Trevors JT. Miniprep DNA isolation from unicellular and filamentous cyanobacteria. J Microbiol Methods 2000;39:159–169 [CrossRef][PubMed]
    [Google Scholar]
  23. Taton A, Grubisic S, Brambilla E, de Wit R, Wilmotte A. Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl Environ Microbiol 2003;69:5157–5169 [CrossRef][PubMed]
    [Google Scholar]
  24. Nübel U, Garcia-Pichel F, Muyzer G. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 1997;63:3327–3332[PubMed]
    [Google Scholar]
  25. Lane DJ. 16S/23S rRNA sequencing. In Stackebrandt E, Goodfellow M. (editors) Nucleic Acid Techniques in Bacterial Systematics Chichester: John Wiley & Sons; 1991; pp.115–175
    [Google Scholar]
  26. Ewing B, Green P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 1998;8:186–194 [CrossRef][PubMed]
    [Google Scholar]
  27. Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 1998;8:175–185 [CrossRef][PubMed]
    [Google Scholar]
  28. Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res 1998;8:195–202 [CrossRef][PubMed]
    [Google Scholar]
  29. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011;7:539 [CrossRef][PubMed]
    [Google Scholar]
  30. Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol 2008;25:1253–1256 [CrossRef][PubMed]
    [Google Scholar]
  31. Iteman I, Rippka R, Tandeau de Marsac N, Herdman M. Comparison of conserved structural and regulatory domains within divergent 16S rRNA–23S rRNA spacer sequences of cyanobacteria. Microbiology 2000;146:1275–1286 [CrossRef][PubMed]
    [Google Scholar]
  32. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003;31:3406–3415 [CrossRef][PubMed]
    [Google Scholar]
  33. Byun Y, Han K. PseudoViewer: web application and web service for visualizing RNA pseudoknots and secondary structures. Nucleic Acids Res 2006;34:W416–W422 [CrossRef][PubMed]
    [Google Scholar]
  34. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003;19:1572–1574 [CrossRef][PubMed]
    [Google Scholar]
  35. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006;22:2688–2690 [CrossRef][PubMed]
    [Google Scholar]
  36. Komárek J, Kaštovský J, Mareš J, Johansen JR. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 2014;86:295–335
    [Google Scholar]
  37. de Marques AA, Schneider M, Peres CA. Human population and socioeconomic modulators of conservation performance in 788 Amazonian and Atlantic Forest reserves. PeerJ 2016;4:e2206 [CrossRef][PubMed]
    [Google Scholar]
  38. Richards DR, Friess DA. Rates and drivers of mangrove deforestation in Southeast Asia, 2000–2012. Proc Natl Acad Sci USA 2016;113:344–349 [CrossRef][PubMed]
    [Google Scholar]
  39. Lemes P, Melo AS, Loyola RD. Climate change threatens protected Areas of the Atlantic Forest. Biodivers Conserv 2014;23:357–368 [CrossRef]
    [Google Scholar]
  40. Alongi DM. The impact of climate change on Mangrove forests. Curr Clim Change Rep 2015;1:30–39 [CrossRef]
    [Google Scholar]
  41. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F. Impacts of climate change on the future of biodiversity. Ecol Lett 2012;15:365–377 [CrossRef][PubMed]
    [Google Scholar]
  42. Mantyka-Pringle CS, Martin TG, Rhodes JR. Interactions between climate and habitat loss effects on biodiversity: a systematic review and meta-analysis. Glob Chang Biol 2012;18:1239–1252 [CrossRef]
    [Google Scholar]
  43. Rybicki J, Hanski I. Species-area relationships and extinctions caused by habitat loss and fragmentation. Ecol Lett 2013;16:27–38 [CrossRef][PubMed]
    [Google Scholar]
  44. Philippot L, Spor A, Hénault C, Bru D, Bizouard F et al. Loss in microbial diversity affects nitrogen cycling in soil. ISME J 2013;7:1609–1619 [CrossRef][PubMed]
    [Google Scholar]
  45. Tardy V, Mathieu O, Lévêque J, Terrat S, Chabbi A et al. Stability of soil microbial structure and activity depends on microbial diversity. Environ Microbiol Rep 2014;6:173–183 [CrossRef][PubMed]
    [Google Scholar]
  46. Sharma NK. From natural to human-impacted ecosystems: rationale to investigate the impact of urbanization on cyanobacterial diversity in soils. Biodivers Conserv 2015;24:1007–1015 [CrossRef]
    [Google Scholar]
  47. Müller T, Ruppel S. Progress in cultivation-independent phyllosphere microbiology. FEMS Microbiol Ecol 2014;87:2–17 [CrossRef][PubMed]
    [Google Scholar]
  48. Rastogi G, Coaker GL, Leveau JH. New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett 2013;348:1–10 [CrossRef][PubMed]
    [Google Scholar]
  49. Komárek J, Genuário DB, Fiore MF, Elster J. Heterocytous cyanobacteria of the Ulu Peninsula, James Ross Island, Antarctica. Polar Biol 2015;38:475–492 [CrossRef]
    [Google Scholar]
  50. Casamatta DA, Vis ML, Sheath RG. Cryptic species in cyanobacterial systematics: a case study of phormidium retzii (Oscillatoriales) using RAPD molecular markers and 16S rDNA sequence data. Aquatic Botany 2003;77:295–309 [CrossRef]
    [Google Scholar]
  51. Lahr DJ, Laughinghouse HD, Oliverio AM, Gao F, Katz LA. How discordant morphological and molecular evolution among microorganisms can revise our notions of biodiversity on Earth. Bioessays 2014;36:950–959 [CrossRef][PubMed]
    [Google Scholar]
  52. Dvořák P, Poulíčková A, Hašler P, Belli M, Casamatta DA et al. Species concepts and speciation factors in cyanobacteria, with connection to the problems of diversity and classification. Biodivers Conserv 2015;24:739–757 [CrossRef]
    [Google Scholar]
  53. Rigonato J, Gama WA, Alvarenga DO, Branco LH, Brandini FP et al. Aliterella atlantica gen. nov., sp. nov., and Aliterella antarctica sp. nov., novel members of coccoid Cyanobacteria. Int J Syst Evol Microbiol 2016;66:2853–2861 [CrossRef][PubMed]
    [Google Scholar]
  54. Hasler P, Dvorak P, Poulickova A, Casamatta DA. A novel genus Ammassolinea gen. nov. (Cyanobacteria) isolated from sub-tropical epipelic habitats. Fottea 2014;14:241–248 [CrossRef]
    [Google Scholar]
  55. Martins MD, Rigonato J, Taboga SR, Branco LH. Proposal of Ancylothrix gen. nov., a new genus of Phormidiaceae (Cyanobacteria, Oscillatoriales) based on a polyphasic approach. Int J Syst Evol Microbiol 2016;66:2396–2405 [CrossRef][PubMed]
    [Google Scholar]
  56. Dvořák P, Jahodářová E, Hašler P, Gusev E, Poulíčková A. A new tropical Cyanobacterium Pinocchia polymorpha gen. et sp. nov. Fottea 2015;15:113–120[CrossRef]
    [Google Scholar]
  57. Martins MD, Branco LH. Potamolinea gen. nov. (Oscillatoriales, Cyanobacteria): a phylogenetically and ecologically coherent cyanobacterial genus. Int J Syst Evol Microbiol 2016;66:3632–3641 [CrossRef][PubMed]
    [Google Scholar]
  58. Casamatta D, Stani D, Gantar M, Richardson LL. Characterization of Roseofilum reptotaenium (Oscillatoriales, Cyanobacteria) gen. et sp. nov. isolated from Caribbean black band disease. Phycologia 2012;51:489–499 [CrossRef]
    [Google Scholar]
  59. Hauer T, Bohunická M, Johansen JR, Mareš J, Berrendero-Gomez E. Reassessment of the cyanobacterial family Microchaetaceae and establishment of new families Tolypothrichaceae and Godleyaceae. J Phycol 2014;50:1089–1100 [CrossRef][PubMed]
    [Google Scholar]
  60. Barth H. The biogeography of mangroves. In Sen DN, Rajpurohit KS. (editors) Tasks for Vegetation Science Hague: Dr W Junk Publishers; 1982; pp.35–60
    [Google Scholar]
  61. Saenger P. Mangrove vegetation: an evolutionary perspective. Mar Freshwater Res 1998;49:277–286 [CrossRef]
    [Google Scholar]
  62. Filgueiras T, Shirasuna RT. Rediscovery of presumably extinct species of Poaceae from flora of São Paulo, Brazil. Hoehnea 2009;36:507–509[CrossRef]
    [Google Scholar]
  63. Fitzgerald MA, Orlovich DA, Allaway WG. Evidence that abaxial leaf glands are the sites of salt secretion in leaves of the mangrove Avicennia marina (Forsk.) Vierh. New Phytol 1992;120:1–7 [CrossRef]
    [Google Scholar]
  64. Thatoi H, Samantaray D, Das SK. The genus Avicennia, a pioneer group of dominant mangrove plant species with potential medicinal values: a review. Front Life Sci 2016;9:267–291 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.002109
Loading
/content/journal/ijsem/10.1099/ijsem.0.002109
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited articles

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