Skip to main content
SpringerLink
Log in

Phylogenetic analysis and molecular signatures defining a monophyletic clade of heterocystous cyanobacteria and identifying its closest relatives

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Detailed phylogenetic and comparative genomic analyses are reported on 140 genome sequenced cyanobacteria with the main focus on the heterocyst-differentiating cyanobacteria. In a phylogenetic tree for cyanobacteria based upon concatenated sequences for 32 conserved proteins, the available cyanobacteria formed 8–9 strongly supported clades at the highest level, which may correspond to the higher taxonomic clades of this phylum. One of these clades contained all heterocystous cyanobacteria; within this clade, the members exhibiting either true (Nostocales) or false (Stigonematales) branching of filaments were intermixed indicating that the division of the heterocysts-forming cyanobacteria into these two groups is not supported by phylogenetic considerations. However, in both the protein tree as well as in the 16S rRNA gene tree, the akinete-forming heterocystous cyanobacteria formed a distinct clade. Within this clade, the members which differentiate into hormogonia or those which lack this ability were also separated into distinct groups. A novel molecular signature identified in this work that is uniquely shared by the akinete-forming heterocystous cyanobacteria provides further evidence that the members of this group are specifically related and they shared a common ancestor exclusive of the other cyanobacteria. Detailed comparative analyses on protein sequences from the genomes of heterocystous cyanobacteria reported here have also identified eight conserved signature indels (CSIs) in proteins involved in a broad range of functions, and three conserved signature proteins, that are either uniquely or mainly found in all heterocysts-forming cyanobacteria, but generally not found in other cyanobacteria. These molecular markers provide novel means for the identification of heterocystous cyanobacteria, and they provide evidence of their monophyletic origin. Additionally, this work has also identified seven CSIs in other proteins which in addition to the heterocystous cyanobacteria are uniquely shared by two smaller clades of cyanobacteria, which form the successive outgroups of the clade comprising of the heterocystous cyanobacteria in the protein trees. Based upon their close relationship to the heterocystous cyanobacteria, the members of these clades are indicated to be the closest relatives of the heterocysts-forming cyanobacteria.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adeolu M, Gupta RS (2013) Phylogenomics and molecular signatures for the order Neisseriales: proposal for division of the order Neisseriales into the emended family Neisseriaceae and Chromobacteriaceae fam. nov. Antonie Van Leeuwenhoek 104:1–24

    Article  PubMed  Google Scholar 

  • Baldauf SL, Palmer JD (1993) Animals and fungi are each other’s closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci USA 90:11558–11562

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bhandari V, Gupta RS (2014) Molecular signatures for the phylum (class) Thermotogae and a proposal for its division into three orders (Thermotogales, Kosmotogales ord. nov. and Petrotogales ord. nov.) containing four families (Thermotogaceae, Fervidobacteriaceae fam. nov., Kosmotogaceae fam. nov. and Petrotogaceae fam. nov.) and a new genus Pseudothermotoga gen. nov. with five new combinations. Antonie Van Leeuwenhoek 105:143–168

  • Castenholz RW (2001) Phylum BX cyanobacteria oxygenic photosynthetic bacteria. In Bergey’s manual of systematic bacteriology. Springer, New York, pp 474–487

    Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2002) The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol 52:7–76

    PubMed  CAS  Google Scholar 

  • Ciccarelli FD, Doerks T, Von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287

    Article  PubMed  CAS  Google Scholar 

  • De Vos P, Truper HG (2000) Judicial Commission of the International Committee on Systematic Bacteriology; IXth International (IUMS) Congress of Bacteriology and Applied Microbiology. Int J Syst Evol Microbiol 50:2239–2244

    Article  Google Scholar 

  • Delwiche CF, Kuhsel M, Palmer JD (1995) Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Mol Phylogenet Evol 4:110–128

    Article  PubMed  CAS  Google Scholar 

  • Desikachary TV (1959) Cyanophyta, Indian Council of Agricultural Research, monographs on Algae. New Delhi, India

  • Fang G, Rocha E, Danchin A (2005) How essential are nonessential genes? Mol Biol Evol 22:2147–2156

    Article  PubMed  CAS  Google Scholar 

  • Gao B, Mohan R, Gupta RS (2009) Phylogenomics and protein signatures elucidating the evolutionary relationships among the Gammaproteobacteria. Int J Syst Evol Microbiol 59:234–247

    Article  PubMed  CAS  Google Scholar 

  • Geitler L (1932) Cyanophycea. Rabenhorst’s Kryptogamen-Flora von Deutschland, Österreich und der Schweiz, Reprint 1985:14

    Google Scholar 

  • Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ, Pace NR (1988) Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170:3584–3592

    PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS (1998) Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62:1435–1491

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gupta RS (2000) The phylogeny of proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol Rev 24:367–402

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS (2003) Evolutionary relationships among photosynthetic bacteria. Photosynth Res 76:173–183

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS (2009) Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int J Syst Evol Microbiol 59:2510–2526

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS (2010) Molecular signatures for the main phyla of photosynthetic bacteria and their subgroups. Photosynth Res 104:357–372

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS (2013) Molecular markers for photosynthetic bacteria and insights into the origin and spread of photosynthesis. Adv Bot Res 66:37–66

    Article  CAS  Google Scholar 

  • Gupta RS, Lali R (2013) Molecular signatures for the phylum Aquificae and its different clades: proposal for division of the phylum Aquificae into the emended order Aquificales, containing the families Aquificaceae and Hydrogenothermaceae, and a new order Desulfurobacteriales ord. nov., containing the family Desulfurobacteriaceae. Antonie Van Leeuwenhoek 104:349–368

    Article  PubMed  Google Scholar 

  • Gupta RS, Mathews DW (2010) Signature proteins for the major clades of Cyanobacteria. BMC Evol Biol 10:24

    Article  PubMed  PubMed Central  Google Scholar 

  • Gupta RS, Pereira M, Chandrasekera C, Johari V (2003) Molecular signatures in protein sequences that are characteristic of cyanobacteria and plastid homologues. Int J Syst Evol Microbiol 53:1833–1842

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS, Chander P, George S (2013) Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexi class. nov. into the suborder Chloroflexineae subord. nov., consisting of the emended family Oscillochloridaceae and the family Chloroflexaceae fam. nov., and the suborder Roseiflexineae subord. nov., containing the family Roseiflexaceae fam. nov. Antonie Van Leeuwenhoek 103:99–119

    Article  PubMed  Google Scholar 

  • Harris JK, Kelley ST, Spiegelman GB, Pace NR (2003) The genetic core of the universal ancestor. Genome Res 13:407–412

    Article  PubMed  CAS  PubMed Central  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 

  • Hoffmann L (2005) Nomenclature of Cyanophyta/Cyanobacteria: roundtable on the unification of the nomenclature under the Botanical and Bacteriological Codes. Algol Stud 117:13–29

    Article  Google Scholar 

  • Hoffmann L, Komarek J, Kastovsky J (2005) System of cyanoprokaryotes (cyanobacteria) state in 2004. Algol Stud 117:95–115

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comp Appl Biosci CABIOS 8:275–282

    CAS  Google Scholar 

  • Komárek J (2002) Problems in cyanobacterial taxonomy: implication for most common toxin producing species. Rapporti Istisan 9:6–43

  • Labeda DP (2000) International committee on systematic bacteriology; IXth international (IUMS) congress of bacteriology and applied microbiology. Int J Syst Evol Microbiol 50:2245–2247

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Naushad HS, Lee B, Gupta RS (2014) Conserved signature indels and signature proteins as novel tools for understanding microbial phylogeny and systematics: identification of molecular signatures that are specific for the phytopathogenic genera Dickeya, Pectobacterium and Brenneria. Int J Syst Evol Microbiol 64:366–383

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, USA

    Google Scholar 

  • Oren A (2004) A proposal for further integration of the cyanobacteria under the Bacteriological Code. Int J Syst Evol Microbiol 54:1895–1902

    Article  PubMed  Google Scholar 

  • Oren A, Garrity GM (2014) Proposal to change general consideration 5 and principle 2 of the International Code of Nomenclature of Prokaryotes. Int J Syst Evol Microbiol 64:309–310

    Article  PubMed  Google Scholar 

  • Oren A, Komarek J, Hoffmann L (2009) Nomenclature of the Cyanophyta/Cyanobacteria/Cyanoprokaryotes: What has happened since IAC Luxembourg? Algol Stud 130:17–26

    Article  Google Scholar 

  • Parte AC (2014) LPSN-list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42:D613–D616

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rajaniemi P, Hrouzek P, Kastovska K, Willame R, Rantala A, Hoffmann L, Komarek 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, 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 

  • Rokas A, Holland PW (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459

    Article  PubMed  Google Scholar 

  • Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804

    Article  PubMed  CAS  Google Scholar 

  • Saatcioglu FAHR, Perry DJ, Pasco DS, Fagan JB (1990) Multiple DNA-binding factors interact with overlapping specificities at the aryl hydrocarbon response element of the cytochrome P450IA1 gene. Mol Cell Biol 10:6408–6416

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sanchez-Baracaldo P, Hayes PK, Blank CE (2005) Morphological and habitat evolution in the Cyanobacteria using a compartmentalization approach. Geobiology 3:145–165

    Article  CAS  Google Scholar 

  • Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Federhen S (2010) Database resources of the national center for biotechnology information. Nucleic Acids Res 38:D5–D16

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schoeffler AJ, May AP, Berger JM (2010) A domain insertion in Escherichia coli GyrB adopts a novel fold that plays a critical role in gyrase function. Nucleic Acids Res 38:7830–7844

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shi T, Falkowski PG (2008) Genome evolution in cyanobacteria: the stable core and the variable shell. Proc Natl Acad Sci 105:2510–2515

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, Talla E, Calteau A, Cai F, de Marsac NT, Rippka R (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci 110:1053–1058

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Singh B, Gupta RS (2009) Conserved inserts in the Hsp60 (GroEL) and Hsp70 (DnaK) proteins are essential for cellular growth. Mol Genet Genomics 281:361–373

    Article  PubMed  CAS  Google Scholar 

  • Singh P, Singh SS, Elster J, Mishra AK (2013) Molecular phylogeny, population genetics, and evolution of heterocystous cyanobacteria using nifH gene sequences. Protoplasma 250:751–764

    Article  PubMed  Google Scholar 

  • Stanier RY, Sistrom WR, Hansen TA, Whitton BA, Castenholz RW, Pfennig N, Gorlenko VN, Kondratieva EN, Eimhjellen KE, Whittenbury R (1978) Proposal to place the nomenclature of the cyanobacteria (blue-green algae) under the rules of the International Code of Nomenclature of Bacteria. Int J Syst Bacteriol 28:335–336

    Article  Google Scholar 

  • Swingley WD, Blankenship RE, Raymond J (2008) Integrating Markov clustering and molecular phylogenetics to reconstruct the cyanobacterial species tree from conserved protein families. Mol Biol Evol 25:643–654

    Article  PubMed  CAS  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  PubMed Central  Google Scholar 

  • Turner SE, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis 1. J Eukaryot Microbiol 46:327–338

    Article  PubMed  CAS  Google Scholar 

  • Wilmotte A, Herdman M (2001) Phylogenetic relationships among the cyanobacteria based on 16S rRNA sequences. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology. Springer, New York, pp 487–493

    Google Scholar 

  • Woese CR (1992) Prokaryote systematics: the evolution of a science. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer, New York, pp 3–18

    Google Scholar 

  • Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462:1056–1060

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yarza P, Ludwig W, Euzeby J, Amann R, Schleifer KH, Glockner FO, Rossello-Mora R (2010) Update of the All-Species Living Tree Project based on 16S and 23S rRNA sequence analyses. Syst Appl Microbiol 33:291–299

    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. Microbiology 143:1443–1450

    Article  PubMed  CAS  Google Scholar 

  • Zhaxybayeva O, Gogarten JP, Charlebois RL, Doolittle WF, Papke RT (2006) Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res 16:1099–1108

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by an MRI-ORF Water Round research grant. We thank Mobolaji Adeolu for helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. Department of Biology, McMaster University, Hamilton, L8N 3Z5, Canada

    Mohammad Howard-Azzeh & Herb E. Schellhorn

  2. Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, L8N 3Z5, Canada

    Mohammad Howard-Azzeh, Larissa Shamseer & Radhey S. Gupta

Authors
  1. Mohammad Howard-Azzeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Larissa Shamseer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Herb E. Schellhorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Radhey S. Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Radhey S. Gupta.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 4297 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Howard-Azzeh, M., Shamseer, L., Schellhorn, H.E. et al. Phylogenetic analysis and molecular signatures defining a monophyletic clade of heterocystous cyanobacteria and identifying its closest relatives. Photosynth Res 122, 171–185 (2014). https://doi.org/10.1007/s11120-014-0020-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-014-0020-x

Keywords

Search

Navigation