1887

Abstract

The cyanobacterial genus is an important contributor to carbon and nitrogen bioavailability in terrestrial ecosystems and a frequent partner in symbiotic relationships with non-diazotrophic organisms. However, since this currently is a polyphyletic genus, the diversity of -like cyanobacteria is considerably underestimated at this moment. While reviewing the phylogenetic placement of previously isolated -like cyanobacteria originating from Brazilian Amazon, Caatinga and Atlantic forest samples, we detected 17 strains isolated from soil, freshwater, rock and tree surfaces presenting patterns that diverged significantly from related strains when ecological, morphological, molecular and genomic traits were also considered. These observations led to the identification of the evaluated strains as representative of three novel nostocacean genera and species: gen. nov., sp. nov.; gen. nov., sp. nov.; and gen. nov., sp. nov., which are herein described according to the rules of the International Code of Nomenclature for algae, fungi and plants. This finding highlights the great importance of tropical and equatorial South American ecosystems for harbouring an unknown microbial diversity in the face of the anthropogenic threats with which they increasingly struggle.

Funding
This study was supported by the:
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (Award 306851/2017-2)
    • Principle Award Recipient: LuisHenrique Zanini Branco
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (Award 302599/2016-9)
    • Principle Award Recipient: Alessandrode Mello Varani
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR) (Award 306803/2018-6)
    • Principle Award Recipient: MarliFátima Fiore
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (Award 2009/15402-1)
    • Principle Award Recipient: AnaPaula Dini Andreote
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (Award 2011/08092-6)
    • Principle Award Recipient: DanilloOliveira Alvarenga
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (Award 2013/50425-8)
    • Principle Award Recipient: MarliFátima Fiore
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004811
2021-05-25
2024-12-06
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/71/5/ijsem004811.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004811&mimeType=html&fmt=ahah

References

  1. Komárek J, Anagnostidis K. Modern approach to the classification system of Cyanophytes 4 – Nostocales. Alg Stud 1989; 56:247–345
    [Google Scholar]
  2. Komárek J. Modern taxonomic revision of planktic nostocacean cyanobacteria: a short review of genera. Hydrobiologia 2010; 639:231–243 [View Article]
    [Google Scholar]
  3. Komárek J. Cyanoprokaryota - 3. Teil/ Part 3: Heterocytous genera. In Büdel B, Gärtner G, Krienitz L, Schagerl M. (editors) Süsswasserflora von Mitteleuropa 19/3 Heidelberg: Springer/Spektrum; 2013
    [Google Scholar]
  4. 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]
  5. Rajaniemi P, Hrouzek P, Kaštovská K, Willame R, Rantala A et al. Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int J Syst Evol Microbiol 2005; 55:11–26 [View Article][PubMed]
    [Google Scholar]
  6. Linnaeus CA. Species Plantarum. Holmiae: Salvius 1753
    [Google Scholar]
  7. Oren A, Ventura S. The current status of cyanobacterial nomenclature under the "prokaryotic" and the "botanical" code. Antonie van Leeuwenhoek 2017; 110:1257–1269 [View Article][PubMed]
    [Google Scholar]
  8. Elenkin AA. Monografia Algarum Cyanophycearum Aquidulcium and Terrestrial in Finibus URSS Inventarum Pars Generalis. Moscow/Leningrad: Sumptibus Academiae Scientiarum URSS; 1936
    [Google Scholar]
  9. Řeháková K, Johansen JR, Casamatta DA, Xuesong L, Vincent J. Morphological and molecular characterization of selected desert soil cyanobacteria: three species new to science including Mojavia pulchra gen. et sp. nov. Phycologia 2007; 46:481–502 [View Article]
    [Google Scholar]
  10. Hrouzek P, Lukešová A, Mares J, Ventura S, Mareš VS. Description of the cyanobacterial genus Desmonostoc gen. nov. including D. muscorum comb. nov. as a distinct, phylogenetically coherent taxon related to the genus Nostoc . Fottea 2013; 13:201–213 [View Article]
    [Google Scholar]
  11. Genuário DB, Vaz MGMV, Hentschke GS, Sant'Anna CL, Fiore MF. Halotia gen. nov., a phylogenetically and physiologically coherent cyanobacterial genus isolated from marine coastal environments. Int J Syst Evol Microbiol 2015; 65:663–675 [View Article][PubMed]
    [Google Scholar]
  12. Bagchi SN, Dubey N, Singh P. Phylogenetically distant clade of Nostoc-like taxa with the description of Aliinostoc gen. nov. and Aliinostoc morphoplasticum sp. nov. Int J Syst Evol Microbiol 2017; 67:3329–3338 [View Article][PubMed]
    [Google Scholar]
  13. Scotta Hentschke G, Johansen JR, Pietrasiak N, Rigonato J, Fiore MF et al. Komarekiella atlantica gen. et sp. nov. (Nostocaceae, Cyanobacteria): a new subaerial taxon from the Atlantic Rainforest and Kauai, Hawaii. Fottea 2017; 17:178–190 [View Article]
    [Google Scholar]
  14. Saraf AG, Dawda HG, Singh P. Desikacharya gen. nov., a phylogenetically distinct genus of Cyanobacteria along with the description of two new species, Desikacharya nostocoides sp. nov. and Desikacharya soli sp. nov., and reclassification of Nostoc thermotolerans to Desikacharya thermotolerans comb. nov. Int J Syst Evol Microbiol 2019; 69:307–315 [View Article][PubMed]
    [Google Scholar]
  15. Cai F, Li X, Geng R, Peng X, Li R. Phylogenetically distant clade of Nostoc-like taxa with the description of Minunostoc gen. nov. and Minunostoc cylindricum sp. nov. Fottea 2019; 19:13–24 [View Article]
    [Google Scholar]
  16. Rikkinen J. Cyanobacteria in terrestrial symbiotic systems. In Hallenbeck P. editor Modern Topics in the Phototrophic Prokaryotes Cham: Springer International Publishing; 2017 pp 243–294
    [Google Scholar]
  17. Nabout JC, da Silva Rocha B, Carneiro FM, Sant’Anna CL. How many species of Cyanobacteria are there? Using a discovery curve to predict the species number. Biodivers Conserv 2013; 22:2907–2918 [View Article]
    [Google Scholar]
  18. Rigonato J, Alvarenga DO, Fiore MF. Tropical cyanobacteria and their biotechnological applications. In Azevedo JL, Quecine MC. (editors) Diversity and Benefits of Microorganisms from the Tropics Cham: Springer; 2017 pp 139–167
    [Google Scholar]
  19. Allen MM. Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 1968; 4:1–4 [View Article][PubMed]
    [Google Scholar]
  20. 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 [View Article][PubMed]
    [Google Scholar]
  21. 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 [View Article][PubMed]
    [Google Scholar]
  22. Nübel U, Garcia-Pichel F, Muyzer G. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 1997; 63:3327–3332 [View Article][PubMed]
    [Google Scholar]
  23. Lane DJ. 16S/23S rRNA sequencing. In Stackebrandt E, Goodfellow M. (editors) Nucleic Acid Techniques in Bacterial Systematics Chichester: Wiley; 1991 pp 115–175
    [Google Scholar]
  24. Ewing B, Green P. Base-calling of automated sequencer traces using Phred: II. error probabilities. Genome Res 1998; 8:186–194
    [Google Scholar]
  25. 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
    [Google Scholar]
  26. Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res 1998; 8:195–202 [View Article][PubMed]
    [Google Scholar]
  27. Sayers EW, Agarwala R, Bolton EE, Brister JR, Canese K et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 2019; 47:D23–D28 [View Article][PubMed]
    [Google Scholar]
  28. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article][PubMed]
    [Google Scholar]
  29. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9:772 [View Article][PubMed]
    [Google Scholar]
  30. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  31. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012; 61:539–542 [View Article][PubMed]
    [Google Scholar]
  32. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31:3406–3415 [View Article][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 [View Article][PubMed]
    [Google Scholar]
  34. 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. Microbiol 2000; 146:1275–1286
    [Google Scholar]
  35. Lin S, Wu Z, Yu G, Zhu M, Yu B et al. Genetic diversity and molecular phylogeny of Planktothrix (Oscillatoriales, cyanobacteria) strains from China. Harmful Algae 2010; 9:87–97 [View Article]
    [Google Scholar]
  36. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
    [Google Scholar]
  37. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  38. Kajitani R, Toshimoto K, Noguchi H, Toyoda A, Ogura Y et al. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res 2014; 24:1384–1395 [View Article][PubMed]
    [Google Scholar]
  39. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46 [View Article][PubMed]
    [Google Scholar]
  40. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article][PubMed]
    [Google Scholar]
  41. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N et al. AntiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 2019; 47:W81–W87 [View Article][PubMed]
    [Google Scholar]
  42. O'Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 2016; 44:D733–D745 [View Article][PubMed]
    [Google Scholar]
  43. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article][PubMed]
    [Google Scholar]
  44. Edgar RC. Search and clustering orders of magnitude faster than blast . Bioinformatics 2010; 26:2460–2461 [View Article][PubMed]
    [Google Scholar]
  45. Wang Z, Wu M. A phylum-level bacterial phylogenetic marker database. Mol Biol Evol 2013; 30:1258–1262 [View Article][PubMed]
    [Google Scholar]
  46. Bengtsson J, Eriksson KM, Hartmann M, Wang Z, Shenoy BD et al. Metaxa: a software tool for automated detection and discrimination among ribosomal small subunit (12S/16S/18S) sequences of archaea, bacteria, eukaryotes, mitochondria, and chloroplasts in metagenomes and environmental sequencing datasets. Antonie van Leeuwenhoek 2011; 100:471–475 [View Article][PubMed]
    [Google Scholar]
  47. de Area Leão Pereira EJ, Silveira Ferreira PJ, de Santana Ribeiro LC, Sabadini Carvalho T, de Barros Pereira HB. Policy in Brazil (2016–2019) threaten conservation of the Amazon rainforest. Environ Sci Policy 2019; 100:8–12 [View Article]
    [Google Scholar]
  48. Lovejoy TE, Nobre C. Amazon tipping point: last chance for action. Sci Adv 2019; 5:eaba2949 [View Article][PubMed]
    [Google Scholar]
  49. Rezende CL, Scarano FR, Assad ED, Joly CA, Metzger JP. From hotspost to hopespot: an opportunity for the Brazilian Atlantic forest. Perspect Ecol Conserv 2018; 16:208–214
    [Google Scholar]
  50. Overbeck GE, Vélez-Martin E, Scarano FR, Lewinsohn TM, Fonseca CR et al. Conservation in Brazil needs to include non-forest ecosystems. Diversity Distrib 2015; 21:1455–1460 [View Article]
    [Google Scholar]
  51. Svenning MM, Eriksson T, Rasmussen U. Phylogeny of symbiotic cyanobacteria within the genus Nostoc based on 16S rDNA sequence analyses. Arch Microbiol 2005; 183:19–26 [View Article][PubMed]
    [Google Scholar]
  52. 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 [View Article][PubMed]
    [Google Scholar]
  53. Alvarenga DO, Fiore MF, Varani AM, Alessandro AM. A metagenomic approach to cyanobacterial genomics. Front Microbiol 2017; 8:809 [View Article][PubMed]
    [Google Scholar]
  54. Bohunická M, Pietrasiak N, Johansen JR, Gómez EB, Hauer T et al. Roholtiella, gen. nov. (Nostocales, Cyanobacteria)—a tapering and branching cyanobacteria of the family Nostocaceae. Phytotaxa 2015; 197:84–103 [View Article]
    [Google Scholar]
  55. Shih PM, Wu D, Latifi A, Axen SD, Fewer DP et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci U S A 2013; 110:1053–1058 [View Article][PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.004811
Loading
/content/journal/ijsem/10.1099/ijsem.0.004811
Loading

Data & Media loading...

Supplements

Supplementary material 1

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