Phylogenetic Analyses of the Core Antenna Domain: Investigatingthe Origin of Photosystem I Article Received: 30 December 2003 Accepted: 29 July 2004 DOI:
Cite this article as: Mix, L.J., Haig, D. & Cavanaugh, C.M. J Mol Evol (2005) 60: 153. doi:10.1007/s00239-003-0181-2 Abstract
Phototrophy, the conversion of light to biochemical energy, occurs throughout the Bacteria and plants, however, debate continues over how different phototrophic mechanisms and the bacteria that contain them are related. There are two types of phototrophic mechanisms in the Bacteria: reaction center type 1 (RC1) has core and core antenna domains that are parts of a single polypeptide, whereas reaction center type 2 (RC2) is composed of short core proteins without antenna domains. In cyanobacteria, RC2 is associated with separate core antenna proteins that are homologous to the core antenna domains of RC1. We reconstructed evolutionary relationships among phototrophic mechanisms based on a phylogeny of core antenna domains/proteins. Core antenna domains of 46 polypeptides were aligned, including the RC1 core proteins of heliobacteria, green sulfur bacteria, and photosystem I (PSI) of cyanobacteria and plastids, plus core antenna proteins of photosystem II (PSII) from cyanobacteria and plastids. Maximum likelihood, parsimony, and neighbor joining methods all supported a single phylogeny in which PSII core antenna proteins (PsbC, PsbB) arose within the cyanobacteria from duplications of the RC1-associated core antenna domains and accessory antenna proteins (IsiA, PcbA, PcbC) arose from duplications of PsbB. The data indicate an evolutionary history of RC1 in which an initially homodimeric reaction center was vertically transmitted to green sulfur bacteria, heliobacteria, and an ancestor of cyanobacteria. A heterodimeric RC1 (=PSI) then arose within the cyanobacterial lineage. In this scenario, the current diversity of core antenna domains/proteins is explained without a need to invoke horizontal transfer.
Keywords Cyanobacteria Green sulfur bacteria Heliobacteria Phylogeny Photosystem I Photosystem II Reaction center 1 Reaction center 2 Reviewing Editor: Dr. W. Ford Doolittle
This article contains online-only supplementary material.
References Barber, J, Morris, E, Buchel, C 2000 Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47 Biochim Biophys Acta Bioenerg 1459 239 247 Google Scholar Baymann, D, Brugna, M, Muhlenhoff, U, Nitschke, W 2001 Daddy, where did (PS)I come from? Biochim Biophys Acta Bioenerg 1507 291 310 Google Scholar Beja, O, Aravind, L, Koonin, EV, Suzuki, MT, Hadd, A, Nguyen, LP, Jovanovich, S, Gates, CM, Feldman, RA, Spudich, JL, Spudich, EN, DeLong, EF 2000 Bacterial rhodopsin: Evidence for a new type of phototrophy in the sea Science 289 1902 1906 CrossRef PubMed Google Scholar Bibby, TS, Nield, J, Barber, J 2001 Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria Nature 412 743 745 Google Scholar Bibby, TS, Mary, I, Nield, J, Barber, J 2003 Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem Nature 424 1051 1054 Google Scholar Bieszke, JA, Braun, EL, Bean, LE, Kang, S, Natvig, DO, Borkovich, KA 1999 The nop-1 gene of Neurospora crassa encodes a seven transmembrane helix retinal-binding protein homologous to archaeal rhodopsins Proc Natl Acad Sci USA 96 8034 8039 Google Scholar Blankenship, RE 1992 Origin and early evolution of photosynthesis Photosynth Res 33 91 111 Google Scholar Blankenship, RE 2002Molecular Mechanisms of Photosynthesis Blackwell Science Maiden, MA Google Scholar Blankenship, RE, Hartman, H 1998 The origin and evolution of oxygenic photosynthesis Trends Biochem Sci 23 94 97 Google Scholar Boekema, EJ, Hifney, A, Yakushevska, AE, Piotrowski, M, Keegstra, W, Berry, S, Michel, KP, Pistorius, EK, Kruip, J 2001 A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria Nature 412 745 748 Google Scholar Brown, JR, Douady, CJ, Italia, MJ, Marshall, WE, Stanhope, MJ 2001 Universal trees based on large combined protein sequence data sets Nature Genet 28 281 285 Google Scholar Deisenhofer, J, Epp, O, Sinning, I, Michel, H 1995 Crystallographic refinement at 2.3 angstrom resolution and refined model of the photosynthetic reaction center from Rhodopseudomonas viridis J Mol Biol 246 429 457 Google Scholar Des Marais, DJ 2000 Evolution—When did photosynthesis emerge on earth? Science 289 1703 1705 Google Scholar 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 Google Scholar Doolittle, WE 1999 Phylogenetic classification and the universal tree Science 284 2124 2128 CrossRef Google Scholar Feick, R, Ertlmaier, A, Ermler, U 1996 Crystallization and X-ray analysis of the reaction center from the thermophilic green bacterium Chloroflexus aurantiacus FEBS Lett 396 161 164 Google Scholar Felsenstein, J 1989 PHYLIP—Phylogeny inference package (version 3.2) Cladistics 5 164 166 Google Scholar Garczarek, L, Hess, WR, Holtzendorff, J, Staay, GWM, Partensky, F 2000 Multiplication of antenna genes as a major adaptation to low light in a marine prokaryote Proc Natl Acad Sci USA 97 4098 4101 Google Scholar Garczarek, L, Staay, GWM, Hess, WR, Le Gall, F, Partensky, F 2001 Expression and phylogeny of the multiple antenna genes of the low-light-adapted strain Prochlorococcus marinus SS120 (Oxyphotobacteria) Plant Mol Biol 46 683 693 Google Scholar Gupta, RS, Mukhtar, T, Singh, B 1999 Evolutionary relationships among photosynthetic prokaryotes ( Heliobacterium chlorum, Chloroflexus aurantiacus. cyanobacteria, Chlorobium tepidum and proteobacteria): Implications regarding the origin of photosynthesis Mol Microbiol 32 893 906 Google Scholar Hall, TA 1999 BIOEDIT: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acid Symp Series 41 95 98 Google Scholar Hauska, G, Schoedl, T, Remigy, H, Tsiotis, G 2001 The reaction center of green sulfur bacteria Biochim Biophys Acta Bioenerg 1507 260 277 Google Scholar 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 Google Scholar Ivancich, A, Mattioli, TA 1998 A comparative study of conserved protein interactions of the primary electron donor in photosynthetic purple bacterial reaction centers Photosynth Res 55 207 215 Google Scholar Ivancich, A, Artz, K, Williams, JC, Allen, JP, Mattioli, TA 1998 Effects of hydrogen bonds on the redox potential and electronic structure of the bacterial primary electron donor Biochemistry 37 11812 11820 Google Scholar Jones, DT, Taylor, WR, Thornton, JM 1994 A mutation data matrix for transmembrane proteins FEES Lett 339 269 275 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 angstrom resolution Nature 411 909 917 CrossRef PubMed Google Scholar LaRoche, J, Staay, GWM, Partensky, F, Ducret, A, Aebersold, R, Li, R, Golden, SS, Hiller, RG, Wrench, PM, Larkum, AWD, Green, BR 1996 Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins Proc Natl Acad Sci USA 93 15244 15248 Google Scholar Liebl, U, Mockensturm-Wilson, M, Trost, JT, Brune, DC, Blankenship, RE, Vermaas, W 1993 Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis—structural implications and relations to other photosystems Proc Natl Acad Sci USA 90 7124 7128 Google Scholar Mann, NH, Cook, A, Millard, A, Bailey, S, Clokie, M 2003 Bacterial photosynthesis genes in a virus Nature 424 741 Google Scholar Mathis, P 1990 Compared structure of plant and bacterial photosynthetic reaction centers—evolutionary implications Biochim Biophys Acta 1018 163 167 Google Scholar Mix, LJ, Harmer, TL, Cavanaugh, CM 2004 Sequence of the core antenna domain from the anoxygenic phototroph Meliophilum fasciatum: Implications for diversity of reaction Center type I Curr Microbiol 48 438 440 Google Scholar McFadden, GI 2001 Primary and secondary endosymbiosis and the origin of plastids J Phycol 37 951 959 CrossRef Google Scholar Mulkidjanian, AY, Junge, W 1997 On the origin of photosynthesis as inferred from sequence analysis—A primordial UV-protector as common ancestor of reaction centers and antenna proteins Photosynth Res 51 27 42 Google Scholar Neerken, S, Amesz, J 2001 The antenna reaction center complex of heliobacteria: Composition, energy conversion and electron transfer Biochim Biophys Acta Bioenerg 1507 278 290 Google Scholar Nitschke, W, Rutherford, AW 1991 Photosynthetic reaction centers—Variations on a common structural theme Trends Biochem Sci 16 241 245 Google Scholar Otsuka, J, Miyachi, H, Horimoto, K 1992 Structure model of core proteins in photosystem I inferred from the comparison with those in photosystem II and bacteria: An application of principal component analysis to detect the similar regions between distantly related families of proteins Biochim Biophys Acta 1118 194 210 Google Scholar Pace, NR 1996 New perspective on the natural microbial world: Molecular microbial ecology ASM News 62 463 470 Google Scholar Raymond, J, Zhaxybayeva, O, Gogarten, JP, Gerdes, SY, Blankenship, RE 2002 Whole genome analysis of photosynthetic prokaryotes Science 298 1616 1620 CrossRef PubMed Google Scholar Redding, K, MacMillan, F, Leibl, W, Brettel, K, Hanley, J, Rutherford, AW, Breton, J, Rochaix, JD 1998 A systematic survey of conserved histidines in the core subunits of Photosystem I by site-directed mutagenesis reveals the likely axial ligands of P-700 EMBO J 17 50 60 Google Scholar Rhee, KH, Morriss, EP, Barber, J, Kuhlbrandt, W 1998 Three-dimensional structure of the plant photosystem II reaction centre at 8 angstrom resolution Nature 396 283 286 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 Google Scholar Shiozawa, JA, Lottspeich, F, Oesterhelt, D, Feick, R 1989 The primary structure of the Chloroflexus aurantiacus reaction-center polypeptides Eur J Biochem 180 75 84 Google Scholar Staay, GWM, Yurkova, N, Green, BR 1998 The 38 kDa chlorophyll a/b protein of the prokaryote Prochlorothrix hollandica is encoded by a divergent pcb gene Plant Mol Biol 36 709 716 Google Scholar Niel, CB 1944 The culture, general physiology, morphology, and general classification of the non-sulfur purple and brown bacteria Bacteriol Rev 8 1 118 Google Scholar Xiong, J, Inoue, K, Bauer, CE 1998 Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis Proc Natl Acad Sci USA 95 14851 14856 Google Scholar Xiong, J, Fischer, WM, Inoue, K, Nakahara, M, Bauer, CE 2000 Molecular evidence for the early evolution of photosynthesis Science 289 1724 1730 CrossRef PubMed Google Scholar Zouni, A, Witt, HT, Kern, J, Fromme, P, Krauss, N, Saenger, W, Orth, P 2001 Crystal structure of photosystem II from Synechococcus elongatus at 3.8 angstrom resolution Nature 409 739 743 Google Scholar Copyright information
© Springer Science+Business Media, Inc. 2005