Skip to main content
SpringerLink
Log in

Novel insights into the origin and diversification of photosynthesis based on analyses of conserved indels in the core reaction center proteins

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The evolution and diversification of different types of photosynthetic reaction centers (RCs) remains an important unresolved problem. We report here novel sequence features of the core proteins from Type I RCs (RC-I) and Type II RCs (RC-II) whose analyses provide important insights into the evolution of the RCs. The sequence alignments of the RC-I core proteins contain two conserved inserts or deletions (indels), a 3 amino acid (aa) indel that is uniquely found in all RC-I homologs from Cyanobacteria (both PsaA and PsaB) and a 1 aa indel that is specifically shared by the Chlorobi and Acidobacteria homologs. Ancestral sequence reconstruction provides evidence that the RC-I core protein from Heliobacteriaceae (PshA), lacking these indels, is most closely related to the ancestral RC-I protein. Thus, the identified 3 aa and 1 aa indels in the RC-I protein sequences must have been deletions, which occurred, respectively, in an ancestor of the modern Cyanobacteria containing a homodimeric form of RC-I and in a common ancestor of the RC-I core protein from Chlorobi and Acidobacteria. We also report a conserved 1 aa indel in the RC-II protein sequences that is commonly shared by all homologs from Cyanobacteria but not found in the homologs from Chloroflexi, Proteobacteria and Gemmatimonadetes. Ancestral sequence reconstruction provides evidence that the RC-II subunits lacking this indel are more similar to the ancestral RC-II protein. The results of flexible structural alignments of the indel-containing region of the RC-II protein with the homologous region in the RC-I core protein, which shares structural similarity with the RC-II homologs, support the view that the 1 aa indel present in the RC-II homologs from Cyanobacteria is a deletion, which was not present in the ancestral form of the RC-II protein. Our analyses of the conserved indels found in the RC-I and RC-II proteins, thus, support the view that the earliest photosynthetic lineages with living descendants likely contained only a single RC (RC-I or RC-II), and the presence of both RC-I and RC-II in a linked state, as found in the modern Cyanobacteria, is a derivation from these earlier phototrophs.

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
Fig. 6

Similar content being viewed by others

References

  • Adachi J, Hasegawa M (1996) Model of amino acid substitution in proteins encoded by mitochondrial DNA. J Mol Evol 42:459–468

    Article  CAS  PubMed  Google Scholar 

  • Adachi J, Waddell PJ, Martin W, Hasegawa M (2000) Plastid genome phylogeny and a model of amino acid substitution for proteins encoded by chloroplast DNA. J Mol Evol 50:348–358

    Article  CAS  PubMed  Google Scholar 

  • Akiva E, Itzhaki Z, Margalit H (2008) Built-in loops allow versatility in domain-domain interactions: lessons from self-interacting domains. Proc Natl Acad Sci U S A 105:13292–13297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen JF (2005) A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Lett 579:963–968

    Article  CAS  PubMed  Google Scholar 

  • Ashkenazy H, Penn O, Doron-Faigenboim A, Cohen O, Cannarozzi G, Zomer O, Pupko T (2012) FastML: a web server for probabilistic reconstruction of ancestral sequences. Nucleic Acids Res 40:W580–W584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bains W, Schulze-Makuch D (2016) The cosmic zoo: the (near) inevitability of the evolution of complex. Macrosc Life. Life (Basel) 6:25

    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 U S A 90:11558–11562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baymann F, Brugna M, Muhlenhoff U, Nitschke W (2001) Daddy, where did (PS)I come from? Biochim Biophys Acta 1507:291–310

    Article  CAS  PubMed  Google Scholar 

  • Bjorn LO, Govindjee (2015) The evolution of photosynthesis and its environmental impact. In: Bjorn LO (ed) Photobiology: the science of light and life. Springer, New York, pp 207–230

    Google Scholar 

  • Bjorn LO, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: Why chlorophyll a? Photosyn Res 99:85–98

    Article  PubMed  Google Scholar 

  • Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosyn Res 33:91–111

    Article  CAS  Google Scholar 

  • Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23:94–97

    Article  CAS  PubMed  Google Scholar 

  • Bryant DA, Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496

    Article  CAS  PubMed  Google Scholar 

  • Bryant DA, Costas AM, Maresca JA, Chew AG, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF, Ward DM (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317:523–526

    Article  CAS  PubMed  Google Scholar 

  • Camara-Artigas A, Brune D, Allen JP (2002) Interactions between lipids and bacterial reaction centers determined by protein crystallography. Proc Natl Acad Sci U S A 99:11055–11060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardona T (2014) A fresh look at the evolution and diversification of photochemical reaction centers. Photosyn Res 126:111–134

    Article  PubMed  PubMed Central  Google Scholar 

  • Chevenet F, Brun C, Banuls AL, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7:439

    Article  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Fromme P, Jordan P, Krauss N (2001) Structure of photosystem I. Biochim Biophys Acta 1507:5–31

    Article  CAS  PubMed  Google Scholar 

  • Golbeck JH (1993) Shared thematic elements in photochemical reaction centers. Proc Natl Acad Sci U S A 90:1642–1646

    Article  CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta RS (2001) The branching order and phylogenetic placement of species from completed bacterial genomes, based on conserved indels found in various proteins. Int Microbiol 4:187–202

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gupta RS (2012) Origin and spread of photosynthesis based upon conserved sequence features in key bacteriochlorophyll biosynthesis proteins. Mol Biol Evol 29:3397–3412

    Article  CAS  PubMed  Google Scholar 

  • Gupta RS (2013) Moelcular 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 (2014) Identification of conserved indels that are useful for classification and evolutionary studies. In: Goodfellow M, Sutcliffe IC, Chun J (eds) Bacterial taxonomy, methods in microbiology, vol 41. Elsevier, London, pp 153–182

    Google Scholar 

  • Gupta RS (2016a) Impact of genomics on the understanding of microbial evolution and classification: the importance of Darwin’s views on classification. FEMS Microbiol Rev 40:520–553

    Article  PubMed  Google Scholar 

  • Gupta RS (2016b) Molecular signatures that are distinctive characteristics of the vertebrates and chordates and supporting a grouping of vertebrates with the tunicates. Mol Phylogenet Evol 94:383–391

    Article  CAS  PubMed  Google Scholar 

  • Gupta RS, Khadka B (2015) Evidence for the presence of key chlorophyll-biosynthesis-related proteins in the genus Rubrobacter (Phylum Actinobacteria) and its implications for the evolution and origin of photosynthesis. Photosyn Res 127:201–218

    Article  PubMed  Google Scholar 

  • Hartman H (1998) Photosynthesis and the origin of life. Orig Life Evol Biosph 28:515–521

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto K, Panchenko AR (2010) Mechanisms of protein oligomerization, the critical role of insertions and deletions in maintaining different oligomeric states. Proc Natl Acad Sci U S A 107:20352–20357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinnickel M, Golbeck JH (2007) Heliobacterial photosynthesis. Photosyn Res 92:35–53

    Article  CAS  PubMed  Google Scholar 

  • Hohmann-Marriott MF, Blankenship RE (2008) Anoxygenic type-I photosystems and evolution of photosynthetic reaction centers. Photosynthetic Protein Complexes, ed P fromme, Weinheim, Ger : Wiley-VCH295-324

  • Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62:515–548

    Article  CAS  PubMed  Google Scholar 

  • Hou HJ, Allakhverdiev SI, Najafpour MM, Govindjee (2014) Current challenges in photosynthesis: from natural to artificial. Front Plant Sci 5:232

    PubMed  PubMed Central  Google Scholar 

  • Janecka JE, Miller W, Pringle TH, Wiens F, Zitzmann A, Helgen KM, Springer MS, Murphy WJ (2007) Molecular and genomic data identify the closest living relative of primates. Science 318:792–794

    Article  CAS  PubMed  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411:909–917

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kondo T, Matsuoka M, Azai C, Itoh S, Oh-Oka H (2016) Orientations of iron-sulfur clusters FA and FB in the homodimeric Type-I photosynthetic reaction center of Heliobacterium modesticaldum. J Phys Chem B 120:4204–4212

    Article  CAS  PubMed  Google Scholar 

  • Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320

    Article  CAS  PubMed  Google Scholar 

  • Lockhart PJ, Steel MA, Larkum AW (1996) Gene duplication and the evolution of photosynthetic reaction center proteins. FEBS Lett 385:193–196

    Article  CAS  PubMed  Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 a resolution structure of photosystem II. Nature 438:1040–1044

    Article  CAS  PubMed  Google Scholar 

  • Mathis P (1990) Compared structure of plant and bacterial photosynthetic reaction centers-evolutionary implications. Biochim Biophys Acta 1018:163–167

    Article  CAS  Google Scholar 

  • Mulkidjanian AY, Koonin EV, Makarova KS, Mekhedov SL, Sorokin A, Wolf YI, Dufresne A, Partensky F, Burd H, Kaznadzey D, Haselkorn R, Galperin MY (2006) The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci U S A 103:13126–13131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nitschke W, Rutherford AW (1991) Photosynthetic reaction centres: variations on a common structural theme? Trends Biochem Sci 16:241–245

    Article  CAS  PubMed  Google Scholar 

  • Oh-Oka H (2007) Type 1 reaction center of photosynthetic heliobacteria. Photochem Photobiol 83:177–186

    Article  CAS  PubMed  Google Scholar 

  • Olson JM (2001) Evolution of photosynthesis’ (1970), re-examined thirty years later. Photosyn Res 68:95–112

    Article  CAS  PubMed  Google Scholar 

  • Olson JM, Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosyn Res 80:373–386

    Article  CAS  PubMed  Google Scholar 

  • Olson JM, Pierson BK (1987a) Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol 108:209–248

    Article  CAS  PubMed  Google Scholar 

  • Olson JM, Pierson BK (1987b) Origin and evolution of photosynthetic reaction centers. Orig Life Evol Biosph 17:419–430

    Article  CAS  Google Scholar 

  • Raymond J, Zhaxybayeva O, Gogarten JP, Gerdes SY, Blankenship RE (2002) Whole-genome analysis of photosynthetic prokaryotes. Science 298:1616–1620

    Article  CAS  PubMed  Google Scholar 

  • Rivera MC, Lake JA (1992) Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257:74–76

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rose PW, Bi C, Bluhm WF, Christie CH, Dimitropoulos D, Dutta S, Green RK, Goodsell DS, Prlic A, Quesada M, Quinn GB, Ramos AG, Westbrook JD, Young J, Zardecki C, Berman HM, Bourne PE (2013) The RCSB Protein Data Bank: new resources for research and education. Nucleic Acids Res 41:D475–D482

    Article  CAS  PubMed  Google Scholar 

  • Sadekar S, Raymond J, Blankenship RE (2006) Conservation of distantly related membrane proteins: photosynthetic reaction centers share a common structural core. Mol Biol Evol 23:2001–2007

    Article  CAS  PubMed  Google Scholar 

  • Sadowski MI, Taylor WR (2012) Evolutionary inaccuracy of pairwise structural alignments. Bioinformatics 28:1209–1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saer RG, Pan J, Hardjasa A, Lin S, Rosell F, Mauk AG, Woodbury NW, Murphy ME, Beatty JT (2014) Structural and kinetic properties of Rhodobacter sphaeroides photosynthetic reaction centers containing exclusively Zn-coordinated bacteriochlorophyll as bacteriochlorin cofactors. Biochim Biophys Acta 1837:366–374

    Article  CAS  PubMed  Google Scholar 

  • Schliep KP (2011) phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593

    Article  CAS  PubMed  Google Scholar 

  • Schubert WD, Klukas O, Saenger W, Witt HT, Fromme P, Krauss N (1998) A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. J Mol Biol 280:297–314

    Article  CAS  PubMed  Google Scholar 

  • Segata N, Bornigen D, Morgan XC, Huttenhower C (2013) PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 4:2304

    Article  PubMed  PubMed Central  Google Scholar 

  • Sela I, Ashkenazy H, Katoh K, Pupko T (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res 43:W7–W14

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Sousa FL, Shavit-Grievink L, Allen JF, Martin WF (2013) Chlorophyll biosynthesis gene evolution indicates photosystem gene duplication, not photosystem merger, at the origin of oxygenic photosynthesis. Genome Biol Evol 5:200–216

    Article  PubMed  Google Scholar 

  • Springer MS, Stanhope MJ, Madsen O, de Jong WW (2004) Molecules consolidate the placental mammal tree. Trends Ecol Evol 19:430–438

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valas RE, Bourne PE (2009) Structural analysis of polarizing indels: an emerging consensus on the root of the tree of life. Biol Direct 4:30

    Article  PubMed  PubMed Central  Google Scholar 

  • Vermaas WF (1994) Evolution of heliobacteria: implications for photosynthetic reaction center complexes. Photosyn Res 41:285–294

    Article  CAS  Google Scholar 

  • Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D’haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M, Copeland A, Han C, Chen F, Cheng JF, Lucas S, Kerfeld C, Lang E, Gronow S, Chain P, Bruce D, Rubin EM, Kyrpides NC, Klenk HP, Eisen JA (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462:1056–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong J, Bauer CE (2002) Complex evolution of photosynthesis. Annu Rev Plant Biol 53:503–521

    Article  CAS  PubMed  Google Scholar 

  • Ye Y, Godzik A (2003) Flexible structure alignment by chaining aligned fragment pairs allowing twists. Bioinformatics 19(Suppl 2):ii246–ii255

    Article  PubMed  Google Scholar 

  • Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glockner FO (2014) The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res 42:D643–D648

    Article  CAS  PubMed  Google Scholar 

  • Zeng Y, Feng F, Medova H, Dean J, Koblizek M (2014) Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci U S A 111:7795–7800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Chen M, Zhou BB, Jermiin LS, Larkum AW (2007) Evolution of the inner light-harvesting antenna protein family of cyanobacteria, algae, and plants. J Mol Evol 64:321–331

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a research grant from the Natural Sciences and Engineering Research Council of Canada to Radhey S. Gupta.

Author information

Authors and Affiliations

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

    Bijendra Khadka, Mobolaji Adeolu & Radhey S. Gupta

  2. Department of Biology and Department of Chemistry, Washington University in St. Louis, St. Louis, MO, 63130, USA

    Robert E. Blankenship

Authors
  1. Bijendra Khadka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mobolaji Adeolu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert E. Blankenship
    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 23,393 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khadka, B., Adeolu, M., Blankenship, R.E. et al. Novel insights into the origin and diversification of photosynthesis based on analyses of conserved indels in the core reaction center proteins. Photosynth Res 131, 159–171 (2017). https://doi.org/10.1007/s11120-016-0307-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-016-0307-1

Keywords

Search

Navigation