Novel insights into the origin and diversification of photosynthesis based on analyses of conserved indels in the core reaction center proteins
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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.
KeywordsEvolution of photosynthesis Reaction center core proteins Conserved indels Ancestral sequence reconstruction Structural alignments
This work was supported by a research grant from the Natural Sciences and Engineering Research Council of Canada to Radhey S. Gupta.
- Bains W, Schulze-Makuch D (2016) The cosmic zoo: the (near) inevitability of the evolution of complex. Macrosc Life. Life (Basel) 6:25Google 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 207–230Google 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 153–182Google 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-VCH295-324Google 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–D482CrossRefPubMedGoogle 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 1837:366–374CrossRefPubMedGoogle 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 462:1056–1060CrossRefPubMedPubMedCentralGoogle Scholar