Advertisement

Protoplasma

, Volume 252, Issue 2, pp 519–535 | Cite as

Decoding cyanobacterial phylogeny and molecular evolution using an evonumeric approach

  • Prashant Singh
  • Satya Shila Singh
  • Marina Aboal
  • Arun Kumar Mishra
Original Article

Abstract

Forty-one heterocystous cyanobacteria strains representing 12 cyanobacterial genera collected from all across India were assessed in phylogenetic and evolutionary perspectives. The structural gene 16S ribosomal RNA (rRNA) and the functional genes nifD and psbA were selected as molecular chronometers in this study. The phylogenetic analyses demonstrated the monophyly of heterocystous cyanobacteria with significant intermixing, along with establishing the polyphyly of Stigonematales, strongly supporting the need for re-amendments in cyanobacterial taxonomy and systematics. Molecular trends obtained did not clearly reflect the phenotypic affiliations, thus advocating for genetic characterizations using more molecular markers. Large-scale evonumeric extrapolations of gene sequence data of all the three molecular markers was performed to assess the evolutionary pace of heterocystous cyanobacteria on the basis of nucleotide diversity, recombination frequencies, and the DNA divergence between the sampled taxa. The obtained results tilted the evolutionary pace in favor of the less complex Nostocales thus indicating that possibly the simple non-branched forms are more flexible and adaptive for evolutionary diversifications as compared to the more complex and branched ones. This study hence represents a unique blend of molecular phylogeny with evogenomic sequence analyses for understanding the genetic diversity, phylogeny, and evolutionary pace within the heterocystous cyanobacteria.

Keywords

Phylogeny Heterocystous cyanobacteria Evolutionary pace Evonumeric approach Evonumeric simulation 

Notes

Acknowledgments

We are thankful to the CSIR, DST, and UGC, New Delhi, for providing financial support in the form of project. Prashant Singh is also thankful to CSIR, New Delhi, for their financial support in the form of SRF. The Head, Department of Botany, Banaras Hindu University, Varanasi, India, is gratefully acknowledged for providing laboratory facilities.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Berrendero E, Perona E, Mateo P (2008) Genetic and morphological characterization of Rivularia and Calothrix (Nostocales, Cyanobacteria) from running water. Int J Syst Evol Microbiol 58:447–460CrossRefPubMedGoogle Scholar
  2. Desikachary TV (1959) Cyanophyta, part I and II. Indian Council of Agricultural Research, New DelhiGoogle Scholar
  3. Didelot X, Martin CJ (2010) Maiden impact of recombination on bacterial evolution. Trends Microbiol 18:315–322CrossRefPubMedCentralPubMedGoogle Scholar
  4. Dopazo J (1994) Estimating errors and confidence intervals for branch lengths in phylogenetic trees by a bootstrap approach. J Mol Evol 38:300–304CrossRefPubMedGoogle Scholar
  5. Druga B, Weker M, Sesarman A, Hegedus A, Coma C, Sicora C, Dragos N (2013) Molecular characterization of microcystin-producing cyanobacteria from Romanian fresh waters. Eur J Phycol 48:287–294Google Scholar
  6. Fearnhead P, Smith NG, Barrigas M, Fox A, French N (2005) Analysis of recombination in Campylobacter jejuni from MLST population data. J Mol Evol 61:333–340CrossRefPubMedGoogle Scholar
  7. Fewer D, Friedl T, Büdel B (2002) Chroococcidiopsis and heterocyst-differentiating cyanobacteria are each other’s closest living relatives. Mol Phylogenet Evol 23:82–90CrossRefPubMedGoogle Scholar
  8. Fox GE, Wisotzkey JD, Jurtshuk P (1992) How close is close: 16S ribosomal-RNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42:166–170CrossRefPubMedGoogle Scholar
  9. Gascuel O, Steel M (2006) Neighbor-joining revealed. Mol Biol Evol 23:1997–2000CrossRefPubMedGoogle Scholar
  10. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224CrossRefPubMedGoogle Scholar
  11. Gugger M, Hoffmann L (2004) Polyphyly of the true branching cyanobacteria (Stigonematales). Int J Syst Evol Microbiol 54:349–357CrossRefPubMedGoogle Scholar
  12. Hanage WP, Fraser C, Spratt BG (2006) The impact of homologous recombination on the generation of diversity in bacteria. J Theor Biol 239:210–219CrossRefPubMedGoogle Scholar
  13. Henson BJ, Watson LE, Barnum SR (2002) Molecular differentiation of the heterocystous cyanobacteria, Nostoc and Anabaena, based on complete NifD sequences. Curr Microbiol 45:161–164CrossRefPubMedGoogle Scholar
  14. Henson BJ, Hesselbrock SM, Watson LE, Barnum SR (2004) Molecular phylogeny of the heterocystous cyanobacteria (subsections IV and V) based on nifD. Int J Syst Evol Microbiol 54:493–497CrossRefPubMedGoogle Scholar
  15. Hoffmann L, Komárek J, Kástovský J (2005) System of cyanoprokaryotes (cyanobacteria) - state. Algol Stud 117:95–115CrossRefGoogle Scholar
  16. Jolley KA, Wilson DJ, Kriz P, McVean G, Maiden MC (2005) The influence of mutation, recombination, population history, and selection on patterns of genetic diversity in Neisseria meningitidis. Mol Biol Evol 22:562–569CrossRefPubMedGoogle Scholar
  17. Junier P, Witzel KP, Hadas O (2007) Genetic diversity of cyanobacterial communities in Lake Kinneret (Israel) using 16S rRNA gene, psbA and ntcA sequence analyses. Aquat Microb Ecol 49:233–241CrossRefGoogle Scholar
  18. Kenyon CK (2003) Phylogenetic analysis of the heterocystous cyanobacteria as assessed by 16S and 23S rRNA. Thesis submitted to the Miami University, Oxford. pp 1–51Google Scholar
  19. Komárek J, Anagnostidis K (1989) Modern approach to the classification system of cyanophytes for Nostocales. Arch Hydrobiol Suppl 82:247–345Google Scholar
  20. Kulick S, Moccia C, Didelot X, Falush D, Kraft C, Suerbaum S (2008) Mosaic DNA imports with interspersions of recipient sequence after natural transformation of Helicobacter pylori. PLoS ONE 3(11):e0003797CrossRefGoogle Scholar
  21. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. J Bioinform 23:2947–2948CrossRefGoogle Scholar
  22. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  23. Litvaitis MK (2002) A molecular test of cyanobacterial phylogeny: inferences from constraint analyses. Hydrobiologia 468:135–145Google Scholar
  24. Mansai SP, Kado T, Innan H (2011) The rate and tract length of gene conversion between duplicated genes. Genes 2:313–331CrossRefPubMedCentralPubMedGoogle Scholar
  25. Maynard-Smith J, Dowson CG, Spratt BG (1991) Localized sex in bacteria. Nature 349:29–31CrossRefGoogle Scholar
  26. Mishra AK, Shukla E, Singh SS (2013) Phylogenetic comparison among the heterocystous cyanobacteria based on a polyphasic approach. Protoplasma 250:77–94CrossRefPubMedGoogle Scholar
  27. Mollenhauer D (1988) Nostoc species in the field. Arch Hydrobiol Suppl 80:315–326Google Scholar
  28. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New YorkGoogle Scholar
  29. Pardia F, Guillemota S, Gascuela O (2010) Robustness of phylogenetic inference based on minimum evolution. Bull Math Biol 72:1820–1839CrossRefGoogle Scholar
  30. Rajaniemi P, Hrouzek P, Kastovska K, Willame R, Rantala A, Hoffmann L, Komárek J, Sivonen K (2005) Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int J Syst Evol Microbiol 55:11–26CrossRefPubMedGoogle Scholar
  31. Rippka R (1988) Recognition and identification of cyanobacteria. Methods Enzymol 167:28–67CrossRefGoogle Scholar
  32. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61CrossRefGoogle Scholar
  33. Roeselers G, Norris TB, Castenholz RW, Rysqaard S, Glud RN, Kuhl M, Muyzer G (2007) Diversity of phototrophic bacteria in microbial mats from Arctic hot springs (Greenland). Environ Microbiol 9:26–38CrossRefPubMedGoogle Scholar
  34. Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum evolution trees. Mol Biol Evol 9:945–967Google Scholar
  35. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  36. Schulz ME, Scherer S (1999) UV protection in cyanobacteria. Eur J Phycol 34:329–338CrossRefGoogle Scholar
  37. Singh P, Singh SS, Elster J, Mishra AK (2013) Molecular phylogeny, population genetics and evolution of heterocystous cyanobacteria using nifH gene sequences. Protoplasma 250:751–764CrossRefPubMedGoogle Scholar
  38. Singh P, Fatma A, Mishra AK (2014a) Molecular phylogeny and evogenomics of heterocystous cyanobacteria using rbcl gene sequence data. Ann Microbiol. doi: 10.1007/s13213-014-0920-1 Google Scholar
  39. Singh P, Kaushik MS, Srivastava M, Mishra AK (2014b) Phylogenetic analysis of heterocystous cyanobacteria (subsections IV and V) using highly iterated palindromes as molecular markers. Physiol Mol Biol Plants 20:331–342CrossRefPubMedGoogle Scholar
  40. Stuken A, Rucker J, Endrulat T, Preussel K, Hemm M, Nixdorf B, Karsten U, Wiedner C (2006) Distribution of three alien cyanobacterial species (Nostocales) in northeast Germany Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 45:696–703CrossRefGoogle Scholar
  41. Tamas I, Svircev Z, Andersson SGE (2000) Determinative value of a portion of the nifH sequence for the genera Nostoc and Anabaena (Cyanobacteria). Curr Microbiol 41:197–200PubMedGoogle Scholar
  42. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedCentralPubMedGoogle Scholar
  43. Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266CrossRefPubMedGoogle Scholar
  44. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S et al (2009) Organised genome dynamics in the Escherichia coli Species results in highly diverse adaptive paths. PLoS Genet 5(1):e1000344CrossRefPubMedCentralPubMedGoogle Scholar
  45. Wall JD (2004) Estimating recombination rates using three site likelihoods. Genet 167:1461–1473CrossRefGoogle Scholar
  46. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703PubMedCentralPubMedGoogle Scholar
  47. Wilmotte A (1994) Molecular evolution and taxonomy of the cyanobacteria. In: Bryant DA (ed) The molecular biology of cyanobacteria, vol 1. Kluwer Academic Publishers, Springer Netherlands, pp 1–25CrossRefGoogle Scholar
  48. Woese CR (1987) Bacterial evolution. Microbial Rev 51:221–271Google Scholar
  49. Yang S, Yuan Y, Wang L, Li J, Wang W, Liu H, Chen JQ, Hurst LD, Tiana D (2012) Great majority of recombination events in Arabidopsis are gene conversion events. PNAS. doi: 10.1073/pnas.1211827110 Google Scholar
  50. Yannarell AC, Steppe TF, Paerl HW (2006) Genetic variance in the composition of two functional groups (diazotrophs and cyanobacteria) from a hypersaline microbial mat. Appl Environ Microbiol 72:1207–1217CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Prashant Singh
    • 1
    • 2
  • Satya Shila Singh
    • 1
    • 3
  • Marina Aboal
    • 4
  • Arun Kumar Mishra
    • 1
  1. 1.Laboratory of Microbial Genetics, Department of BotanyBanaras Hindu UniversityVaranasiIndia
  2. 2.Microbial Culture Collection (MCC)National Centre for Cell Science (NCCS)PuneIndia
  3. 3.Department of Botany, Guru Ghasidas VishwavidyalayaBilaspurIndia
  4. 4.Laboratory of Algae, Department of Vegetal BiologyUniversity of MurciaMurciaSpain

Personalised recommendations