Skip to main content
SpringerLink
Log in

Molecular phylogeny, population genetics, and evolution of heterocystous cyanobacteria using nifH gene sequences

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

In order to assess phylogeny, population genetics, and approximation of future course of cyanobacterial evolution based on nifH gene sequences, 41 heterocystous cyanobacterial strains collected from all over India have been used in the present study. NifH gene sequence analysis data confirm that the heterocystous cyanobacteria are monophyletic while the stigonematales show polyphyletic origin with grave intermixing. Further, analysis of nifH gene sequence data using intricate mathematical extrapolations revealed that the nucleotide diversity and recombination frequency is much greater in Nostocales than the Stigonematales. Similarly, DNA divergence studies showed significant values of divergence with greater gene conversion tracts in the unbranched (Nostocales) than the branched (Stigonematales) strains. Our data strongly support the origin of true branching cyanobacterial strains from the unbranched strains.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Castenholz RW (2001) Phylum BX. Cyanobacteria, oxygenic photosynthetic bacteria. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, vol 1. Springer, New York, p 721

    Google Scholar 

  • Desikachary TV (1959) Cyanophyta, part I and II. Indian council of agricultural research, New Delhi

    Google Scholar 

  • Dopazo J (1994) Estimating errors and confidence intervals for branch lengths in phylogenetic trees by a bootstrap approach. J Mol Evol 38:300–304

    Article  PubMed  CAS  Google Scholar 

  • Gugger M, Hoffmann L (2004) Polyphyly of the true branching cyanobacteria (Stigonematales). Int J Syst Evol Microbiol 54:349–357

    Article  PubMed  CAS  Google Scholar 

  • Gugger M, Lyra C, Henrikson P, Coute A, Humbert JF, Sihvonen K (2002) Phylogenetic comparison of the cyanobacterial genera Anabaena and Aphanizomenon. Int J Syst Evol Microbiol 52:1867–1880

    Article  PubMed  CAS  Google Scholar 

  • Gugger M, Molica R, Berre BL, Dufour P, Bernard C, Humbert JF (2005) Genetic diversity of Cylindrospermopsis Strains (Cyanobacteria) isolated from four continents. Appl Environ Microbiol 71:1097–1100

    Article  PubMed  CAS  Google Scholar 

  • Henson BJ, Watson LE, Barnum SR (2002) Molecular differentiation of the heterocystous cyanobacteria, Nostoc and Anabaena, based on complete NifD sequences. Curr Microbiol 45:161–164

    Article  PubMed  CAS  Google Scholar 

  • 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 54:493–497

    Article  PubMed  CAS  Google Scholar 

  • Iteman I, Rippka R, Tandeau de Marsac N, Herdman M (2002) rDNA analyses of planktonic heterocystous cyanobacteria, including members of the genera Anabaenopsis and Cyanospira. Microbiol 148:481–496

    CAS  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, pp 21–132

    Google Scholar 

  • Komárek J, Anagnostidis K (1989) Modern approach to the classification system of cyanophytes 4 Nostocales. Arch Hydrobiol Suppl 82:247–345

    Google Scholar 

  • Lammers P, Haselkorn R (1984) Sequence of the nifD gene coding for the α subunit from the cyanobacterium Anabaena. Cell 44:905–911

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Mevarech M, Rice D, Haselkorn R (1980) Nucleotide sequence of a cyanobacterial nifH gene coding for nitrogenase reductase. Proc Natl Acad Sci USA 77:6476–6480

    Article  PubMed  CAS  Google Scholar 

  • Mishra AK, Shukla E, Singh SS (2012) Phylogenetic comparison among the heterocystous cyanobacteria based on a polyphasic approach. Protoplasma. doi:10.1007/s00709-012-0375-9

  • Mollenhauer D (1988) Nostoc species in the field. Arch Hydrobiol Suppl 80(315):326

    Google Scholar 

  • Neilan BA, Jacobs D, Goodman AE (1995) Genetic diversity and phylogeny of toxic cyanobacteria determined by DNA polymorphisms within the phycocyanin locus. Appl Environ Microbiol 61:875–3883

    Google Scholar 

  • Postgate JR (1982) The fundamentals of nitrogen fixation. Cambridge University Press, Cambridge

    Google Scholar 

  • 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 55:11–26

    Article  PubMed  CAS  Google Scholar 

  • Rippka R (1988) Recognition and identification of cyanobacteria. Methods Enzymol 167:28–67

    Article  Google Scholar 

  • Rippka R, Herdman M (1992) Pasteur culture collection of cyanobacterial strains in axenic culture, catalogue and taxonomic handbook. Institut Pasteur, Paris

    Google Scholar 

  • 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 111:1–61

    Article  Google Scholar 

  • Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum evolution trees. Mol Biol Evol 9:945–967

    CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour joining method—a new method for reconstructing phylogenetic tree. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sihvonen LM, Lyra C, Fewer DP, Rajaniemi-Wacklin P, Lehtimáki JM, Wahlsten M, Sivonen K (2007) Strains of the cyanobacterial genera Calothrix and Rivularia isolated from the Baltic Sea display cryptic diversity and are distantly related to Gloeotrichia and Tolypothrix. FEMS Microbiol Ecol 61:74–84

    Article  PubMed  CAS  Google Scholar 

  • 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 45:696–703

    Article  Google Scholar 

  • 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 41:97–200

    Google Scholar 

  • 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 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • 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 72:1207–1217

    Article  PubMed  CAS  Google Scholar 

  • Zehr JP, Mellon MT, Hiorns WD (1997) Phylogeny of cyanobacterial nifH genes: evolutionary implications and potential applications to natural assemblages. Microbiol 143:1443–1450

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are thankful to the Department of Science and Technology, Ministry of Science and Technology, for providing financial support in the form of a project. One of us (PS) 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.

Author information

Authors and Affiliations

  1. Laboratory of Microbial Genetics, Department of Botany, Banaras Hindu University, Varanasi, 221005, India

    Prashant Singh & Arun Kumar Mishra

  2. Department of Botany, Guru Ghasidas Vishwavidyalaya, Bilaspur, Chhattisgarh, India

    Satya Shila Singh

  3. Centre for Polar Ecology, Faculty of Science, University of South Bohemia, České Budĕjovice, Czech Republic

    Josef Elster

  4. Centre for Phycology, Institute of Botany, Academy of Sciences CR, Třeboň, Czech Republic

    Josef Elster

Authors
  1. Prashant Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Satya Shila Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Josef Elster
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arun Kumar Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arun Kumar Mishra.

Additional information

Handling Editor: Peter Nick

Rights and permissions

Reprints and permissions

About this article

Cite this article

Singh, P., Singh, S.S., Elster, J. et al. Molecular phylogeny, population genetics, and evolution of heterocystous cyanobacteria using nifH gene sequences. Protoplasma 250, 751–764 (2013). https://doi.org/10.1007/s00709-012-0460-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-012-0460-0

Keywords

Search

Navigation