期刊论文详细信息
BMC Evolutionary Biology
Genome-wide analysis of putative peroxiredoxin in unicellular and filamentous cyanobacteria
Song Qin1  Yinchu Wang2  Yipeng Wang1  Hongli Cui2 
[1] Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Chunhui Road, Yantai 264003, People’s Republic of China;University of Chinese Academy of Sciences, Yuquan Road, Beijing 100049, People’s Republic of China
关键词: Cyanobacteria;    Comparative genomics;    Phylogeny and evolution;    Structure;    Peroxiredoxin;   
Others  :  1140035
DOI  :  10.1186/1471-2148-12-220
 received in 2012-03-03, accepted in 2012-10-25,  发布年份 2012
PDF
【 摘 要 】

Background

Cyanobacteria are photoautotrophic prokaryotes with wide variations in genome sizes and ecological habitats. Peroxiredoxin (PRX) is an important protein that plays essential roles in protecting own cells against reactive oxygen species (ROS). PRXs have been identified from mammals, fungi and higher plants. However, knowledge on cyanobacterial PRXs still remains obscure. With the availability of 37 sequenced cyanobacterial genomes, we performed a comprehensive comparative analysis of PRXs and explored their diversity, distribution, domain structure and evolution.

Results

Overall 244 putative prx genes were identified, which were abundant in filamentous diazotrophic cyanobacteria, Acaryochloris marina MBIC 11017, and unicellular cyanobacteria inhabiting freshwater andhot-springs, while poor in all Prochlorococcus and marine Synechococcus strains. Among these putative genes,25 open reading frames (ORFs) encoding hypothetical proteins were identified as prx gene family members andthe others were already annotated as prx genes. All 244 putative PRXs were classified into five major subfamilies(1-Cys, 2-Cys, BCP, PRX5_like, and PRX-like) according to their domain structures. The catalytic motifs of the cyanobacterial PRXs were similar to those of eukaryotic PRXs and highly conserved in all but the PRX-like subfamily. Classical motif (CXXC) of thioredoxin was detected in protein sequences from the PRX-like subfamily. Phylogenetic tree constructed of catalytic domains coincided well with the domain structures of PRXs and the phylogenies based on 16s rRNA.

Conclusions

The distribution of genes encoding PRXs in different unicellular and filamentous cyanobacteria especially those sub-families like PRX-like or 1-Cys PRX correlate with the genome size, eco-physiology, and physiological properties of the organisms. Cyanobacterial and eukaryotic PRXs share similar conserved motifs, indicating that cyanobacteria adopt similar catalytic mechanisms as eukaryotes. All cyanobacterial PRX proteins share highly similar structures, implying that these genes may originate from a common ancestor. In this study, a general framework of the sequence-structure-function connections of the PRXs was revealed, which may facilitate functional investigations of PRXs in various organisms.

【 授权许可】

   
2012 Cui et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150324064602505.pdf 1710KB PDF download
Figure 5. 283KB Image download
Figure 4. 83KB Image download
Figure 3. 84KB Image download
Figure 2. 117KB Image download
Figure 1. 171KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Stanier RY, Cohen-Bazire G: Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol 1977, 31:225-274.
  • [2]Blankenship RE, Hartman H: The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 1998, 23(3):94-97.
  • [3]Whitton BA, Potts M: In The ecology of cyanobacteria: their diversity in time and space. Edited by Whitton BA, Potts M. 2000, 1-11.
  • [4]Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, et al.: Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 2003, 424(6952):1042-1047.
  • [5]Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, Barbe V, Duprat S, Galperin MY, Koonin EV, Le Gall F, et al.: Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci U S A 2003, 100(17):10020-10025.
  • [6]Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R: An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 2001, 70(1):85-106.
  • [7]Jiang Q, Qin S, Wu QY: Genome-wide comparative analysis of metacaspases in unicellular and filamentous cyanobacteria. BMC Genomics 2010, 11:198. BioMed Central Full Text
  • [8]Chi XY, Yang QL, Zhao FQ, Qin S, Yang Y, Shen JJ, Lin HZ: Comparative analysis of fatty acid desaturases in cyanobacterial genomes. Comp Funct Genomics 2008, 16:1099-1108.
  • [9]Scanlan D: Cyanobacteria: ecology, niche adaptation and genomics. Microbiol Today 2001, 28:128-130.
  • [10]Partensky F, Hess WR, Vaulot D: Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 1999, 63(1):106-127.
  • [11]Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, Tsuchiya T, Sasamoto S, Watanabe A, Kawashima K, Kishida Y, et al.: Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 2003, 10(4):137-145.
  • [12]Zhang XW, Zhao FQ, Guan XG, Yang Y, Liang CW, Qin S: Genome-wide survey of putative serine/threonine protein kinases in cyanobacteria. BMC Genomics 2007, 8:395. BioMed Central Full Text
  • [13]Wang H, Fewer DP, Sivonen K: Genome mining demonstrates the widespread occurrence of gene clusters encoding bacteriocins in cyanobacteria. PLoS One 2011, 6(7):e22384.
  • [14]Latifi A, Ruiz M, Zhang CC: Oxidative stress in cyanobacteria. FEMS Microbiol Rev 2009, 33(2):258-278.
  • [15]Dietz KJ: The dual function of plant peroxiredoxins in antioxidant defence and redox signaling. Peroxiredoxin Syst 2007, 44:267-294.
  • [16]Benzie IFF: Evolution of antioxidant defence mechanisms. Eur J Nutr 2000, 39(2):53-61.
  • [17]Tripathi BN, Bhatt I, Dietz KJ: Peroxiredoxins: a less studied component of hydrogen peroxide detoxification in photosynthetic organisms. Protoplasma 2009, 235(1–4):3-15.
  • [18]Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, de Miranda SMN, Baier M, Finkemeier I: The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 2006, 57(8):1697-1709.
  • [19]Dietz KJ, Stork T, Finkemeier I, Lamkemeyer P, Li WX, El-Tayeb MA, Michel KP, Pistorius E, Baier M: The role of peroxiredoxins in oxygenic photosynthesis of cyanobacteria and higher plants: peroxide detoxification or redox sensing? Photoprotection, Photoinhibition, Gene Regulation, and Environ 2006, 21:303-319.
  • [20]Regelsberger G, Jakopitsch C, Plasser L, Schwaiger H, Furtmuller PG, Peschek GA, Zamocky M, Obinger C: Occurrence and biochemistry of hydroperoxidases in oxygenic phototrophic prokaryotes (cyanobacteria). Plant Physiol Biochem 2002, 40(6–8):479-490.
  • [21]Mutsuda M, Ishikawa T, Takeda T, Shigeoka S: The catalase-peroxidase of Synechococcus PCC 7942: purification, nucleotide sequence analysis and expression in Escherichia coli. Biochem J 1996, 316(Pt 1):251-257.
  • [22]Tichy M, Vermaas W: In vivo role of catalase-peroxidase in Synechocystis sp. Strain PCC 6803. J Bacteriol 1999, 181(6):1875-1882.
  • [23]Jakopitsch C, Rüker F, Regelsberger G, Dockal M, Peschek GA, Obinger C: Catalase-peroxidase from the cyanobacterium Synechocystis PCC 6803: cloning, overexpression in Escherichia coli, and kinetic characterization. Biol Chem 1999, 380(9):1087-1096.
  • [24]Obinger C, Regelsberger G, Furtmuller PG, Jakopitsch C, Ruker F, Pircher A, Peschek G: Catalase-peroxidases in cyanobacteria similarities and differences to ascorbate peroxidases. Free Radic Res 1999, 31(Suppl 1):243-249.
  • [25]Smulevich G, Jakopitsch C, Droghetti E, Obinger C: Probing the structure and bifunctionality of catalase-peroxidase (KatG). J Inorg Biochem 2006, 100(4):568-585.
  • [26]Priya B, Premanandh J, Dhanalakshmi RT, Seethalakshmi T, Uma L, Prabaharan D, Subramanian G: Comparative analysis of cyanobacterial superoxide dismutases to discriminate canonical forms. BMC Genomics 2007, 8:435. BioMed Central Full Text
  • [27]Baier M, Dietz KJ: Primary structure and expression of plant homologues of animal and fungal thioredoxin-dependent peroxide reductases and bacterial alkyl hydroperoxide reductases. Plant Mol Biol 1996, 31(3):553-564.
  • [28]Kobayashi M, Ishizuka T, Katayama M, Kanehisa M, Bhattacharyya-Pakrasi M, Pakrasi HB, Ikeuchi M: Response to oxidative stress involves a novel peroxiredoxin gene in the unicellular cyanobacterium Synechocystis sp PCC 6803. Plant Cell Physiol 2004, 45(3):290-299.
  • [29]Dietz KJ, Horling F, Konig J, Baier M: The function of the chloroplast 2-cysteine peroxiredoxin in peroxide detoxification and its regulation. J Exp Bot 2002, 53(372):1321-1329.
  • [30]Rouhier N, Jacquot JP: Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynth Res 2002, 74(3):259-268.
  • [31]Brehelin C, Meyer EH, de Souris JP, Bonnard G, Meyer Y: Resemblance and dissemblance of Arabidopsis type II peroxiredoxins: Similar sequences for divergent gene expression, protein localization, and activity. Plant Physiol 2003, 132(4):2045-2057.
  • [32]Fujii J, Ikeda Y: Advances in our understanding of peroxiredoxin, a multifunctional, mammalian redox protein. Redox Rep 2002, 7(3):123-130.
  • [33]Hosoya-Matsuda N, Motohashi K, Yoshimura H, Nozaki A, Inoue K, Ohmori M, Hisabori T: Anti-oxidative stress system in cyanobacteria - Significance of type II peroxiredoxin and the role of 1-Cys peroxiredoxin in Synechocystis sp strain PCC 6803. J Biol Chem 2005, 280(1):840-846.
  • [34]Stork T, Michel KP, Pistorius EK, Dietz KJ: Bioinformatic analysis of the genomes of the cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942 for the presence of peroxiredoxins and their transcript regulation under stress. J Exp Bot 2005, 56(422):3193.
  • [35]Cui H, Wang Y, Qin S: Genome-wide analysis of carotenoid cleavage dioxygenases in unicellular and filamentous cyanobacteria. Comp Funct Genomics 2012. in press
  • [36]Chi XY, Yang QL, Zhao FQ, Qin S, Yang Y, Shen JJ, Lin HZ: Comparative analysis of fatty acid desaturases in cyanobacterial genomes. Comp Funct Genomics 2008, 2008:284508.
  • [37]Zhao FQ, Zhang XW, Liang CW, Wu JY, Bao QY, Qin S: Genome-wide analysis of restriction-modification system in unicellular and filamentous cyanobacteria. Physiol Genomics 2006, 24(3):181-190.
  • [38]Liang C, Zhao F, Wei W, Wen Z, Qin S: Carotenoid biosynthesis in cyanobacteria: structural and evolutionary scenarios based on comparative genomics. Int J Biol Sci 2006, 2(4):197-207.
  • [39]JGIhttp://genome.jgi.doe.gov/ webcite
  • [40]Cyanobasehttp://genome.kazusa.or.jp/cyanobase webcite
  • [41]Wood ZA, Schroder E, Harris JR, Poole LB: Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 2003, 28(1):32-40.
  • [42]Imlay JA: Pathways of oxidative damage. Annu Rev Microbiol 2003, 57:395-418.
  • [43]Noctor G, Veljovic-Jovanovic S, Foyer CH: Peroxide processing in photosynthesis: antioxidant coupling and redox signalling. Philos Trans R Soc Lond B Biol Sci 2000, 355(1402):1465-1475.
  • [44]Chae HZ, Robison K, Poole LB, Church G, Storz G, Rhee SG: Cloning and sequencing of thiol-specific antioxidant from mammalian brain - alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc Natl Acad Sci U S A 1994, 91(15):7017-7021.
  • [45]Chae HZ, Chung SJ, Rhee SG: Thioredoxin-dependent peroxide reductase from Yeast. J Biol Chem 1994, 269(44):27670-27678.
  • [46]Hofmann B, Hecht HJ, Flohe L: Peroxiredoxins. Biol Chem 2002, 383(3–4):347-364.
  • [47]Bryk R, Griffin P, Nathan C: Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 2000, 407(6801):211-215.
  • [48]Peshenko IV, Shichi H: Oxidation of active center cysteine of bovine 1-Cys peroxiredoxin to the cysteine sulfenic acid form by peroxide and peroxynitrite. Free Radic Biol Med 2001, 31(3):292-303.
  • [49]Hillar A, Peters B, Pauls R, Loboda A, Zhang H, Mauk AG, Loewen PC: Modulation of the activities of catalase-peroxidase HPI of Escherichia coli by site-directed mutagenesis. Biochemistry 2000, 39(19):5868-5875.
  • [50]Link AJ, Robison K, Church GM: Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12. Electrophoresis 1997, 18(8):1259-1313.
  • [51]Chae HZ, Kim HJ, Kang SW, Rhee SG: Characterization of three isoforms of mammalian peroxiredoxin that reduce peroxides in the presence of thioredoxin. Diabetes Res Clin Pract 1999, 45(2–3):101-112.
  • [52]Seaver LC, Imlay JA: Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 2001, 183(24):7173.
  • [53]Perelman A, Uzan A, Hacohen D, Schwarz R: Oxidative stress in Synechococcus sp. strain PCC 7942: various mechanisms for H2O2 detoxification with different physiological roles. J Bacteriol 2003, 185(12):3654-3660.
  • [54]Hirotsu S, Abe Y, Okada K, Nagahara N, Hori H, Nishino T, Hakoshima T: Crystal structure of a multifunctional 2-Cys peroxiredoxin heme-binding protein 23 kDa/proliferation-associated gene product. Proc Natl Acad Sci U S A 1999, 96(22):12333-12338.
  • [55]Alphey MS, Bond CS, Tetaud E, Fairlamb AH, Hunter WN: The structure of reduced tryparedoxin peroxidase reveals a decamer and insight into reactivity of 2Cys-peroxiredoxins. J Mol Biol 2000, 300(4):903-916.
  • [56]Wood ZA, Poole LB, Hantgan RR, Karplus PA: Dimers to doughnuts: Redox-sensitive oligomerization of 2-cysteine peroxiredoxins. Biochemistry 2002, 41(17):5493-5504.
  • [57]Declercq JP, Evrard C, Clippe A, Vander Stricht D, Bernard A, Knoops B: Crystal structure of human peroxiredoxin 5, a novel type of mammalian peroxiredoxin at 1.5 angstrom resolution. J Mol Biol 2001, 311(4):751-759.
  • [58]Choi HJ, Kang SW, Yang CH, Rhee SG, Ryu SE: Crystal structure of a novel human peroxidase enzyme at 2.0 Å resolution. Nat Struct Mol Biol 1998, 5(5):400-406.
  • [59]Flohe L, Budde H, Bruns K, Castro H, Clos J, Hofmann B, Kansal-Kalavar S, Krumme D, Menge U, Plank-Schumacher K, et al.: Tryparedoxin peroxidase of Leishmania donovani: molecular cloning, heterologous expression, specificity, and catalytic mechanism. Arch Biochem Biophys 2002, 397(2):324-335.
  • [60]Fomenko DE, Gladyshev VN: Identity and functions of CxxC-derived motifs. Biochemistry 2003, 42(38):11214-11225.
  • [61]Schultz LW, Chivers PT, Raines RT: The CXXC motif: crystal structure of an active-site variant of Escherichia coli thioredoxin. Acta Crystallogr D: Biol Crystallogr 1999, 55(Pt 9):1533-1538.
  • [62]Karplus PA, Hall A: Structural survey of the peroxiredoxins. Peroxiredoxin Syst 2007, 44:41-60.
  • [63]Mazouni K, Domain F, Chauvat F, Cassier-Chauvat C: Expression and regulation of the crucial plant-like ferredoxin of cyanobacteria. Mol Microbiol 2003, 49(4):1019-1029.
  • [64]Dufresne A, Garczarek L, Partensky F: Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 2005, 6(2):R14. BioMed Central Full Text
  • [65]Stacy RAP, Munthe E, Steinum T, Sharma B, Aalen RB: A peroxiredoxin antioxidant is encoded by a dormancy-related gene, Per1, expressed during late development in the aleurone and embryo of barley grains. Plant Mol Biol 1996, 31(6):1205-1216.
  • [66]Haslekas C, Stacy RAP, Nygaard V, Culianez-Macia FA, Aalen RB: The expression of a peroxiredoxin antioxidant gene, AtPer1, in Arabidopsis thaliana is seed-specific and related to dormancy. Plant Mol Biol 1998, 36(6):833-845.
  • [67]Mowla SB, Thomson JA, Farrant JM, Mundree SG: A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker. Planta 2002, 215(5):716-726.
  • [68]Stacy RAP, Nordeng TW, Culiáñez-Macià FA, Aalen RB: The dormancy-related peroxiredoxin anti-oxidant, PER1, is localized to the nucleus of barley embryo and aleurone cells. Plant J 1999, 19(1):1-8.
  • [69]Rhee SG, Chae HZ, Kim K: Peroxiredoxins: A historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med 2005, 38(12):1543-1552.
  • [70]Baier M, Dietz KJ: The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. Plant J 1997, 12(1):179-190.
  • [71]Jang HH, Chi YH, Park SK, Lee SS, Lee JR, Park JH, Moon JC, Lee YM, Kim SY, Lee KO, et al.: Structural and functional regulation of eukaryotic 2-Cys peroxiredoxins including the plant ones in cellular defense-signaling mechanisms against oxidative stress. Physiol Plant 2006, 126(4):549-559.
  • [72]Kong W, Shiota S, Shi YX, Nakayama H, Nakayama K: A novel peroxiredoxin of the plant Sedum lineare is a homologue of Escherichia coli bacterioferritin co-migratory protein (Bcp). Biochem J 2000, 351:107-114.
  • [73]NCBIhttp://www.ncbi.nlm.nih.gov/sites/gquery
  • [74]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410.
  • [75]Mount DW: Using the Basic Local Alignment Search Tool (BLAST). CSH Protoc 2007, 2007:pdb top17.
  • [76]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
  • [77]Gertz EM, Yu YK, Agarwala R, Schaffer AA, Altschul SF: Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol 2006, 4:41. BioMed Central Full Text
  • [78]Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J: The Pfam protein families database. Nucleic Acids Res 2004, 32(suppl 1):D138-D141.
  • [79]Johnson LS, Eddy SR, Portugaly E: Hidden Markov model speed heuristic and iterative HMM search. BMC Bioinforma 2010, 11:431. BioMed Central Full Text
  • [80]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al.: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
  • [81]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22(22):4673-4680.
  • [82]Schultz J, Milpetz F, Bork P, Ponting CP: SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 1998, 95(11):5857-5864.
  • [83]Marchler-Bauer A, Bryant SH: CD-Search: protein domain annotations on the fly. Nucleic Acids Res 2004, 32(Web Server issue):W327-W331.
  • [84]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704.
  • [85]Kern R, Bauwe H, Hagemann M: Evolution of enzymes involved in the photorespiratory 2-phosphoglycolate cycle from cyanobacteria via algae toward plants. Photosynth Res 2011, 109(1–3):103-114.
  • [86]Le SQ, Gascuel O: An improved general amino acid replacement matrix. Mol Biol Evol 2008, 25(7):1307-1320.
  • [87]Chevenet F, Brun C, Banuls AL, Jacq B, Christen R: TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinforma 2006, 7:439-445. BioMed Central Full Text
  • [88]Team R: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2010.
  文献评价指标  
  下载次数:10次 浏览次数:9次