1887

Abstract

Two isolated from South Atlantic Ocean continental shelf deep water and from a marine green algae inhabiting the Admiralty Bay, King George Island, Antarctica were investigated based on morphological and ultrastructural traits, phylogeny of 16S rRNA gene sequences, secondary structure of the 16S-23S internal transcribed spacer regions and phylogenomic analyses. The majority of these evaluations demonstrated that both strains differ from the genera of cyanobacteria with validly published names and, therefore, supported the description of the novel genus as gen. nov. The identity and phylogeny of 16S rRNA gene sequences, together with the secondary structure of D1D1′ and BoxB intergenic regions, further supported the two strains representing distinct species: gen. nov., sp. nov. (type SP469036, strain CENA595) and sp. nov. (type SP469035, strain CENA408). The phylogenomic analysis of sp. nov. CENA595, based on 21 protein sequences, revealed that this genus belongs to the cyanobacterial order . The isolation and cultivation of two geographically distant unicellular members of a novel cyanobacterial genus and the sequenced genome of the type strain bring new insights into the current classification of the coccoid group, and into the reconstruction of their evolutionary history.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.001066
2016-08-01
2024-10-06
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/66/8/2853.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.001066&mimeType=html&fmt=ahah

References

  1. Abascal F., Zardoya R., Posada D. 2005; ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105 [View Article][PubMed]
    [Google Scholar]
  2. Allen M. M. 1968; Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 4:1–4 [View Article][PubMed]
    [Google Scholar]
  3. Azua-Bustos A., Zúñiga J., Arenas-Fajardo C., Orellana M., Salas L., Rafael V. 2014; Gloeocapsopsis AAB1, an extremely desiccation-tolerant cyanobacterium isolated from the Atacama Desert. Extremophiles 18:61–74 [View Article][PubMed]
    [Google Scholar]
  4. Baudoux A. C., Brussaard C. P. 2005; Characterization of different viruses infecting the marine harmful algal bloom species Phaeocystis globosa . Virology 341:80–90 [View Article][PubMed]
    [Google Scholar]
  5. Blank C. E., Sánchez-Baracaldo P. 2010; Timing of morphological and ecological innovations in the cyanobacteria–a key to understanding the rise in atmospheric oxygen. Geobiology 8:1–23 [View Article][PubMed]
    [Google Scholar]
  6. Bombar D., Heller P., Sanchez-Baracaldo P., Carter B. J., Zehr J. P. 2014; Comparative genomics reveals surprising divergence of two closely related strains of uncultivated UCYN-A cyanobacteria. ISME J 8:2530–2542 [View Article][PubMed]
    [Google Scholar]
  7. Bonner J. T. 1998; The origins of multicellularity. Integr Biol 1:27–36 [View Article]
    [Google Scholar]
  8. Brown I. I., Mummey D., Cooksey K. E. 2005; A novel cyanobacterium exhibiting an elevated tolerance for iron. FEMS Microbiol Ecol 52:307–314 [View Article][PubMed]
    [Google Scholar]
  9. Calteau A., Fewer D. P., Latifi A., Coursin T., Laurent T., Jokela J., Kerfeld C. A., Sivonen K., Piel J., Gugger M. 2014; Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria. BMC Genomics 15:977 [View Article][PubMed]
    [Google Scholar]
  10. Chong C. W., Convey P., Pearce D. A., Tan I. K. P. 2012; Assessment of soil bacterial communities on Alexander Island (in the maritime and continental Antarctic transitional zone). Polar Biology 35:387–399 [View Article]
    [Google Scholar]
  11. Chrismas N. A., Anesio A. M., Sánchez-Baracaldo P. 2015; Multiple adaptations to polar and alpine environments within cyanobacteria: a phylogenomic and Bayesian approach. Front Microbiol 6:1070 [View Article][PubMed]
    [Google Scholar]
  12. Claessen D., Rozen D. E., Kuipers O. P., Søgaard-Andersen L., van Wezel G. P. 2014; Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol 12:115–124 [View Article][PubMed]
    [Google Scholar]
  13. Dagan T., Roettger M., Stucken K., Landan G., Koch R., Major P., Gould S. B., Goremykin V. V., Rippka R. et al. 2013; Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol Evol 5:31–44 [View Article][PubMed]
    [Google Scholar]
  14. 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]
  15. 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[PubMed] [CrossRef]
    [Google Scholar]
  16. Fewer D., Friedl T., Büdel B. 2002; Chroococcidiopsis and heterocyst-differentiating cyanobacteria are each other's closest living relatives. Mol Phylogenet Evol 23:82–90 [View Article][PubMed]
    [Google Scholar]
  17. Gao E. B., Gui J. F., Zhang Q. Y. 2012; A novel cyanophage with a cyanobacterial nonbleaching protein A gene in the genome. J Virol 86:236–245 [View Article][PubMed]
    [Google Scholar]
  18. Gordon D., Abajian C., Green P. 1998; Consed: a graphical tool for sequence finishing. Genome Res 8:195–202 [View Article][PubMed]
    [Google Scholar]
  19. Grosberg R. K., Strathmann R. R. 2007; The evolution of eulticellularity: a minor major transition?. Annu Rev Ecol Evol Syst 38:621–654 [View Article]
    [Google Scholar]
  20. Hallmann C., Stannek L., Fritzlar D., Hause-Reitner D., Friedl T., Hoppert M. 2013; Molecular diversity of phototrophic biofilms on building stone. FEMS Microbiol Ecol 84:355–372 [View Article][PubMed]
    [Google Scholar]
  21. Herdman M., Janvier M., Rippka R., Stanier R. Y. 1979; Genome Size of Cyanobacteria. J Gen Microbiol 111:73–85 [View Article]
    [Google Scholar]
  22. Honda D., Yokota A., Sugiyama J. 1999; Detection of seven major evolutionary lineages in cyanobacteria based on the 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J Mol Evol 48:723–739 [View Article][PubMed]
    [Google Scholar]
  23. Karnovsky M. J. A. 1965; Formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137
    [Google Scholar]
  24. Kim M., Oh H. S., Park S. C., Chun J. 2014; Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351 [View Article][PubMed]
    [Google Scholar]
  25. Kimura M. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 [View Article][PubMed]
    [Google Scholar]
  26. Komárek J., Anagnostidis K. 1998; Cyanoprokaryota, 1. Teil: Chroococcales. In Süsswasserflora Von Mitteleuropa 19 , pp. 1–548 Edited by Ettl H. Stuttgart: Gustave Fisher;
    [Google Scholar]
  27. Komárek J., Kaštovský J., Mareš J., Johansen J. R. 2014; Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) using a polyphasic approach. Preslia 86:295–335
    [Google Scholar]
  28. Kong H. H., Oh J., Deming C., Conlan S., Grice E. A., Beatson M. A., Nomicos E., Polley E. C., Komarow H. D. et al. 2012; Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–859 [View Article][PubMed]
    [Google Scholar]
  29. Kováčik L., Jezberová J., Komárková J., Kopecký J., Komárek J. 2011; Ecological characteristics and polyphasic taxonomic classification of stable pigment-types of the genus Chroococcus (Cyanobacteria). Preslia 83:145–166
    [Google Scholar]
  30. Larsson J., Nylander J. A., Bergman B. 2011; Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. BMC Evol Biol 11:187 [View Article][PubMed]
    [Google Scholar]
  31. Lehner J., Zhang Y., Berendt S., Rasse T. M., Forchhammer K., Maldener I. 2011; The morphogene AmiC2 is pivotal for multicellular development in the cyanobacterium Nostoc punctiforme . Mol Microbiol 79:1655–1669 [View Article][PubMed]
    [Google Scholar]
  32. Lowe T. M., Eddy S. R. 1997; tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964 [View Article][PubMed]
    [Google Scholar]
  33. Moissl C., Osman S., La Duc M. T., Dekas A., Brodie E., DeSantis T., Desantis T., Venkateswaran K. 2007; Molecular bacterial community analysis of clean rooms where spacecraft are assembled. FEMS Microbiol Ecol 61:509–521 [View Article][PubMed]
    [Google Scholar]
  34. Mori T., Johnson C. H. 2001; Independence of circadian timing from cell division in cyanobacteria. J Bacteriol 183:2439–2444 [View Article][PubMed]
    [Google Scholar]
  35. Posada D., Crandall K. A. 1998; Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818 [View Article][PubMed]
    [Google Scholar]
  36. Ramos V., Seabra R., Brito Ângela., Santos A., Santos C. L., Lopo M., Moradas-Ferreira P., Vasconcelos V. M., Tamagnini P. 2010; Characterization of an intertidal cyanobacterium that constitutes a separate clade together with thermophilic strains. Eur J Phycol 45:394–403 [View Article]
    [Google Scholar]
  37. Rigonato J., Alvarenga D. O., Branco L. H., Varani A. M., Brandini F. P., Fiore M. F. 2015; Draft genome sequence of a novel culturable marine chroococcalean cyanobacterium from the South atlantic ocean. Genome Announc 3:e00384 [View Article][PubMed]
    [Google Scholar]
  38. Rippka R. 1988; Recognition and identification of cyanobacteria. Meth Enzymol 167:28–76 [CrossRef]
    [Google Scholar]
  39. Robertson B. R., Tezuka N., Watanabe M. M. 2001; Phylogenetic analyses of Synechococcus strains (cyanobacteria) using sequences of 16S rDNA and part of the phycocyanin operon reveal multiple evolutionary lines and reflect phycobilin content. Int J Syst Evol Microbiol 51:861–871 [View Article][PubMed]
    [Google Scholar]
  40. Ronquist F., Huelsenbeck J. P. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574 [View Article][PubMed]
    [Google Scholar]
  41. Rossetti V., Schirrmeister B. E., Bernasconi M. V., Bagheri H. C. 2010; The evolutionary path to terminal differentiation and division of labor in cyanobacteria. J Theor Biol 262:23–34 [View Article][PubMed]
    [Google Scholar]
  42. Sanchez-baracaldo P., Hayes P. K., Blank C. E. 2005; Morphological and habitat evolution in the Cyanobacteria using a compartmentalization approach. Geobiology 3:145–165 [View Article]
    [Google Scholar]
  43. Schattner P., Brooks A. N., Lowe T. M. 2005; The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689 [View Article][PubMed]
    [Google Scholar]
  44. Schirrmeister B. E., Antonelli A., Bagheri H. C. 2011; The origin of multicellularity in cyanobacteria. BMC Evol Biol 11:45 [View Article][PubMed]
    [Google Scholar]
  45. Schirrmeister B. E., Gugger M., Philip C. J., Donoghue P. C. J. 2015; Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils. Palaeontology 58:769–785 [View Article][PubMed]
    [Google Scholar]
  46. Shih P. M., Wu D., Latifi A., Axen S. D., Fewer D. P., Talla E., Calteau A., Cai F., Tandeau de Marsac N. et al. 2013; Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci U S A 110:1053–1058 [View Article][PubMed]
    [Google Scholar]
  47. Sievers F., Wilm A., Dineen D., Gibson T. J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M. et al. 2011; Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539 [View Article][PubMed]
    [Google Scholar]
  48. 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]
  49. Stamatakis A. 2014; RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  50. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  51. Taton A., Grubisic S., Brambilla E., De Wit R., Wilmotte A. 2003; Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl Environ Microbiol 69:5157–5169 [View Article][PubMed]
    [Google Scholar]
  52. 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 22:4673–4690 [View Article][PubMed]
    [Google Scholar]
  53. Tomitani A., Knoll A. H., Cavanaugh C. M., Ohno T. 2006; The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proc Natl Acad Sci U S A 103:5442–5447 [View Article][PubMed]
    [Google Scholar]
  54. Waterbury J. B. 1989; Subsection II Order Pleurocapsales. In Bergeys Manual of Systematic Bacteriology Vol. 3 , pp. 1746–1770 Edited by Buchanan R. E., Gibbons N. E. Baltimore: Williams & Wilkins;
    [Google Scholar]
  55. Wu M., Eisen J. A. 2008; A simple, fast, and accurate method of phylogenomic inference. Genome Biol 9:R151 [View Article][PubMed]
    [Google Scholar]
  56. Zuker M. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415 [View Article][PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.001066
Loading
/content/journal/ijsem/10.1099/ijsem.0.001066
Loading

Data & Media loading...

Supplements

Supplementary File 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