Abstract
Homologs showing high degree of sequence similarity to the three subunits of the protochlorophyllide oxidoreductase enzyme complex (viz. BchL, BchN, and BchB), which carries out a central role in chlorophyll-bacteriochlorophyll (Bchl) biosynthesis, are uniquely found in photosynthetic organisms. The results of BLAST searches and homology modeling presented here show that proteins exhibiting a high degree of sequence and structural similarity to the BchB and BchN proteins are also present in organisms from the high G+C Gram-positive phylum of Actinobacteria, specifically in members of the genus Rubrobacter (R. x ylanophilus and R. r adiotolerans). The results presented exclude the possibility that the observed BLAST hits are for subunits of the nitrogenase complex or the chlorin reductase complex. The branching in phylogenetic trees and the sequence characteristics of the Rubrobacter BchB/BchN homologs indicate that these homologs are distinct from those found in other photosynthetic bacteria and that they may represent ancestral forms of the BchB/BchN proteins. Although a homolog showing high degree of sequence similarity to the BchL protein was not detected in Rubrobacter, another protein, belonging to the ParA/Soj/MinD family, present in these bacteria, exhibits high degree of structural similarity to the BchL. In addition to the BchB/BchN homologs, Rubrobacter species also contain homologs showing high degree of sequence similarity to different subunits of magnesium chelatase (BchD, BchH, and BchI) as well as proteins showing significant similarity to the BchP and BchG proteins. Interestingly, no homologs corresponding to the BchX, BchY, and BchZ proteins were detected in the Rubrobacter species. These results provide the first suggestive evidence that some form of photosynthesis either exists or was anciently present within the phylum Actinobacteria (high G+C Gram-positive) in members of the genus Rubrobacter. The significance of these results concerning the origin of the Bchl-based photosynthesis is also discussed.
Similar content being viewed by others
References
Albuquerque L, Johnson MM, Schumann P, Rainey FA, da Costa MS (2014) Description of two new thermophilic species of the genus Rubrobacter, Rubrobacter calidifluminis sp. nov. and Rubrobacter naiadicus sp. nov., and emended description of the genus Rubrobacter and the species Rubrobacter bracarensis. Syst Appl Microbiol 37:235–243
Altschul SF, Madden TL, Schaffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein databases search programs. Nucleic Acids Res 25:3389–3402
Beale SI (1999) Enzyme of chlorophyll biosynthesis. Photosynth Res 60:43–73
Benkert P, Tosatto SC, Schomburg D (2008) QMEAN: a comprehensive scoring function for model quality assessment. Proteins 71:261–277
Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 33:91–111
Blankenship RE (2010) Early evolution of photosynthesis. Plant Physiol 154:434–438
Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23:94–97
Boyd ES, Peters JW (2013) New insights into the evolutionary history of biological nitrogen fixation. Front Microbiol 4:201
Brocker MJ, Schomburg S, Heinz DW, Jahn D, Schubert WD, Moser J (2010) Crystal structure of the nitrogenase-like dark operative protochlorophyllide oxidoreductase catalytic complex (ChlN/ChlB)2. J Biol Chem 285:27336–27345
Bryant DA, Costas AM, Maresca JA et al (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317:523–526
Bryant DA, Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496
Burke DH, Hearst JE, Sidow A (1993) Early evolution of photosynthesis: clues from nitrogenase and chlrophyll iron proteins. Proc Natl Acad Sci USA 90:7134–7138
Carreto L, Moore E, Nobre MF et al (1996) Rubrobacter xylanophilus sp. nov., a new thermophilic species isolated from a thermally polluted effluent. Int J Syst Bacteriol 46:460–465
Chen MY, Wu SH, Lin GH et al (2004) Rubrobacter taiwanensis sp. nov., a novel thermophilic, radiation-resistant species isolated from hot springs. Int J Syst Evol Microbiol 54:1849–1855
Chew AG, Bryant DA (2007) Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. Annu Rev Microbiol 61:113–129
Colovos C, Yeates TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2:1511–1519
Cordell SC, Lowe J (2001) Crystal structure of the bacterial cell division regulator MinD. FEBS Lett 492:160–165
Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, DasGupta J, Tyryshkin A (2001) The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci USA 98:2170–2175
Egas C, Barroso C, Froufe HJ, Pacheco J, Albuquerque L, da Costa MS (2014) Complete genome sequence of the radiation–resistant bacterium Rubrobacter radiotolerans RSPS-4. Stand Genomic Sci 9:1062–1075
Eisenberg D, Luthy R, Bowie JU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277:396–404
Fiser A, Sali A (2003) Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol 374:461–491
Gao B, Gupta RS (2012) Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol Mol Biol Rev 76:66–112
Gest H, Favinger J (1983) Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a “new” form of bacteriochlorophyll. Arch Microbiol 136:11–16
Goodfellow M, Kampfer P, Busse HJ, Trujillo ME, Suzuki K, Ludwig W, Whitman W (2011) The Actinobacteria. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology. Springer, New York
Granick S (1965) Evolution of heme and chlorophyll. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 67–88
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
Gupta RS (2003) Evolutionary relationships among photosynthetic bacteria. Photosynth Res 76:173–183
Gupta RS (2009) Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int J Syst Evol Microbiol 59:2510–2526
Gupta RS (2010) Molecular signatures for the main phyla of photosynthetic bacteria and their subgroups. Photosynth Res 104:357–372
Gupta RS (2012) Origin and spread of photosynthesis based upon conserved sequence features in key bacteriochlorophyll biosynthesis proteins. Mol Biol Evol 29:3397–3412
Gupta RS (2013) Moelcular markers for photosynthetic bacteria and insights into the origin and spread of photosynthesis. Adv Bot Res 66:37–66
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
Hester CM, Lutkenhaus J (2007) Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci USA 104:20326–20331
Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62:515–548
Howard-Azzeh M, Shamseer L, Schellhorn HE, Gupta RS (2014) Phylogenetic analysis and molecular signatures defining a monophyletic clade of heterocystous cyanobacteria and identifying its closest relatives. Photosynth Res 122:171–185
Huang YJ, Mao B, Aramini JM, Montelione GT (2014) Assessment of template-based protein structure predictions in CASP10. Proteins 82(Suppl 2):43–56
Igarashi N, Harada J, Nagashima S, Matsuura K, Shimada K, Nagashima KVP (2001) Horizontal transfer of the photosynthesis gene cluster and operon rearrangement in purple bacteria. J Mol Evol 52:333–341
Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal x. Trends Biochem Sci 23:403–405
Jurado V, Miller AZ, Alias-Villegas C, Laiz L, Saiz-Jimenez C (2012) Rubrobacter bracarensis sp. nov., a novel member of the genus Rubrobacter isolated from a biodeteriorated monument. Syst Appl Microbiol 35:306–309
Kampfer P, Glaeser SP, Busse HJ, Abdelmohsen UR, Hentschel U (2014) Rubrobacter aplysinae sp. nov., isolated from the marine sponge Aplysina aerophoba. Int J Syst Evol Microbiol 64:705–709
Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858
Leonard TA, Butler PJ, Lowe J (2005) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer—a conserved biological switch. EMBO J 24:270–282
Lovell SC, Davis IW, Arendall WB III et al (2003) Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 50:437–450
Luthy R, Bowie JU, Eisenberg D (1992) Assessment of protein models with three-dimensional profiles. Nature 356:83–85
Lutkenhaus J (2012) The ParA/MinD family puts things in their place. Trends Microbiol 20:411–418
Margulis L (1993) Symbiosis in cell evolution. W.H. Freeman and Company, New York
Mariani V, Kiefer F, Schmidt T, Haas J, Schwede T (2011) Assessment of template based protein structure predictions in CASP9. Proteins 79(Suppl 10):37–58
Meng EC, Pettersen EF, Couch GS, Huang CC, Ferrin TE (2006) Tools for integrated sequence-structure analysis with UCSF Chimera. BMC Bioinform 7:339
Morden CW, Delwiche CF, Kuhsel M, Palmer JD (1992) Gene phylogenies and the endosymbiotic origin of plastids. Biosystems 28:75–90
Mulkidjanian AY, Koonin EV, Makarova KS et al (2006) The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci USA 103:13126–13131
Muraki N, Nomata J, Ebata K et al (2010) X-ray crystal structure of the light-independent protochlorophyllide reductase. Nature 465:110–114
Olson JM, Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80:373–386
Olson JM, Pierson BK (1987) Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol 108:209–248
Raymond J (2008) Coloring in the tree of life. Trends Microbiol 16:41–43
Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554
Raymond J, Zhaxybayeva O, Gogarten JP, Blankenship RE (2003) Evolution of photosynthetic prokaryotes: a maximum-likelihood mapping approach. Philos Trans R Soc Lond [Biol] 358:223–230
Raymond J, Zhaxybayeva O, Gogarten JP, Gerdes SY, Blankenship RE (2002) Whole-genome analysis of photosynthetic prokaryotes. Science 298:1616–1620
Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277
Rose PW, Prlic A, Bi C et al (2015) The RCSB Protein Data Bank: views of structural biology for basic and applied research and education. Nucleic Acids Res 43:D345–D356
Sakai N, Yao M, Itou H et al (2001) The three-dimensional structure of septum site-determining protein MinD from Pyrococcus horikoshii OT3 in complex with Mg-ADP. Structure 9:817–826
Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779–815
Sarma R, Barney BM, Hamilton TL, Jones A, Seefeldt LC, Peters JW (2008) Crystal structure of the L protein of Rhodobacter sphaeroides light-independent protochlorophyllide reductase with MgADP bound: a homologue of the nitrogenase Fe protein. Biochemistry 47:13004–13015
Sawana A, Adeolu M, Gupta RS (2014) Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 5:429
Shen MY, Sali A (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci 15:2507–2524
Shi T, Falkowski PG (2008) Genome evolution in cyanobacteria: the stable core and the variable shell. Proc Natl Acad Sci USA 105:2510–2515
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
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
Tank M, Bryant DA (2015) Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium. Int J Syst Evol Microbiol 65:1426–1430
Tank M, Bryant DA (2015) Nutrient requirements and growth physiology of the photoheterotrophic Acidobacterium, Chloracidobacterium thermophilum. Front Microbiol 6:226
Thakur S, Bothra AK, Sen A (2013) Functional divergence outlines the evolution of novel protein function in NifH/BchL protein family. J Biosci 38:733–740
Vermaas WFJ (1994) Evolution of heliobacteria: implications for photosynthetic reaction center complexes. Photosynth Res 41:285–294
Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699
Xiong J, Bauer CE (2002) Complex evolution of photosynthesis. Annu Rev Plant Biol 53:503–521
Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724–1730
Xiong J, Inoue K, Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterizaton of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95:14851–14856
Xu D, Zhang Y (2011) Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophys J 101:2525–2534
Yang J, Zhang Y (2015) I-TASSER server: new development for protein structure and function predictions. Nucleic Acids Res
Yarza P, Richter M, Peplies J et al (2008) The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31:241–250
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 USA 111:7795–7800
Zeng Y, Selyanin V, Lukes M, et al (2015) Characterization of microaerophilic bacteriochlorophyll a—containing bacterium Gemmatimonas phototrophica sp. nov. Int J Syst Evol Microbiol
Zhu K, Pincus DL, Zhao S, Friesner RA (2006) Long loop prediction using the protein local optimization program. Proteins 65:438–452
Zsebo KM, Hearst JE (1984) Genetic-physical mapping of a photosynthetic gene cluster from R. c apsulata. Cell 37:937–947
Acknowledgments
This work was supported by a research Grant (No. 249924) from the Natural Science and Engineering Research Council of Canada. We thank two anonymous reviewers for helpful comments.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gupta, R.S., Khadka, B. 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. Photosynth Res 127, 201–218 (2016). https://doi.org/10.1007/s11120-015-0177-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-015-0177-y