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
2020-04-06
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. Bioinformatics21:2104–2105 [CrossRef][PubMed]
    [Google Scholar]
  2. Allen M. M.. 1968; Simple conditions for growth of unicellular blue-green algae on plates. J Phycol4:1–4 [CrossRef][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. Extremophiles18:61–74 [CrossRef][PubMed]
    [Google Scholar]
  4. Baudoux A. C., Brussaard C. P.. 2005; Characterization of different viruses infecting the marine harmful algal bloom species Phaeocystis globosa . Virology341:80–90 [CrossRef][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. Geobiology8:1–23 [CrossRef][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 J8:2530–2542 [CrossRef][PubMed]
    [Google Scholar]
  7. Bonner J. T.. 1998; The origins of multicellularity. Integr Biol1:27–36 [CrossRef]
    [Google Scholar]
  8. Brown I. I., Mummey D., Cooksey K. E.. 2005; A novel cyanobacterium exhibiting an elevated tolerance for iron. FEMS Microbiol Ecol52:307–314 [CrossRef][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 Genomics15:977 [CrossRef][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 Biology35:387–399 [CrossRef]
    [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 Microbiol6:1070 [CrossRef][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 Microbiol12:115–124 [CrossRef][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 Evol5:31–44 [CrossRef][PubMed]
    [Google Scholar]
  14. Ewing B., Green P.. 1998; Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res8:186–194 [CrossRef][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 Res8:175–185[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 Evol23:82–90 [CrossRef][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 Virol86:236–245 [CrossRef][PubMed]
    [Google Scholar]
  18. Gordon D., Abajian C., Green P.. 1998; Consed: a graphical tool for sequence finishing. Genome Res8:195–202 [CrossRef][PubMed]
    [Google Scholar]
  19. Grosberg R. K., Strathmann R. R.. 2007; The evolution of eulticellularity: a minor major transition?. Annu Rev Ecol Evol Syst38:621–654 [CrossRef]
    [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 Ecol84:355–372 [CrossRef][PubMed]
    [Google Scholar]
  21. Herdman M., Janvier M., Rippka R., Stanier R. Y.. 1979; Genome Size of Cyanobacteria. J Gen Microbiol111:73–85 [CrossRef]
    [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 Evol48:723–739 [CrossRef][PubMed]
    [Google Scholar]
  23. Karnovsky M. J. A.. 1965; Formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol27:137
    [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 Microbiol64:346–351 [CrossRef][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 Evol16:111–120 [CrossRef][PubMed]
    [Google Scholar]
  26. Komárek J., Anagnostidis K.. 1998; Cyanoprokaryota, 1. Teil: Chroococcales. In Süsswasserflora Von Mitteleuropa19 , 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. Preslia86:295–335
    [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 Res22:850–859 [CrossRef][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). Preslia83:145–166
    [Google Scholar]
  30. Larsson J., Nylander J. A., Bergman B.. 2011; Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. BMC Evol Biol11:187 [CrossRef][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 Microbiol79:1655–1669 [CrossRef][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 Res25:955–964 [CrossRef][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 Ecol61:509–521 [CrossRef][PubMed]
    [Google Scholar]
  34. Mori T., Johnson C. H.. 2001; Independence of circadian timing from cell division in cyanobacteria. J Bacteriol183:2439–2444 [CrossRef][PubMed]
    [Google Scholar]
  35. Posada D., Crandall K. A.. 1998; Modeltest: testing the model of DNA substitution. Bioinformatics14:817–818 [CrossRef][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 Phycol45:394–403 [CrossRef]
    [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 Announc3:e00384 [CrossRef][PubMed]
    [Google Scholar]
  38. Rippka R.. 1988; Recognition and identification of cyanobacteria. Meth Enzymol167:28–76[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 Microbiol51:861–871 [CrossRef][PubMed]
    [Google Scholar]
  40. Ronquist F., Huelsenbeck J. P.. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics19:1572–1574 [CrossRef][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 Biol262:23–34 [CrossRef][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. Geobiology3:145–165 [CrossRef]
    [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 Res33:W686–W689 [CrossRef][PubMed]
    [Google Scholar]
  44. Schirrmeister B. E., Antonelli A., Bagheri H. C.. 2011; The origin of multicellularity in cyanobacteria. BMC Evol Biol11:45 [CrossRef][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. Palaeontology58:769–785 [CrossRef][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 A110:1053–1058 [CrossRef][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 Biol7:539 [CrossRef][PubMed]
    [Google Scholar]
  48. Spurr A. R.. 1969; A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res26:31–43 [CrossRef][PubMed]
    [Google Scholar]
  49. Stamatakis A.. 2014; RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics30:1312–1313 [CrossRef][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 Evol30:2725–2729 [CrossRef][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 Microbiol69:5157–5169 [CrossRef][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 Res22:4673–4690 [CrossRef][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 A103:5442–5447 [CrossRef][PubMed]
    [Google Scholar]
  54. Waterbury J. B.. 1989; Subsection II Order Pleurocapsales. In Bergeys Manual of Systematic BacteriologyVol. 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 Biol9:R151 [CrossRef][PubMed]
    [Google Scholar]
  56. Zuker M.. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res31:3406–3415 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/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

Most cited this month

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