期刊论文详细信息
BMC Genomics
A pangenomic analysis of the Nannochloropsis organellar genomes reveals novel genetic variations in key metabolic genes
Rose Ann Cattolico2  Gabrielle Rocap1  Scott Twary3  Olga Chertkov3  Michael Jacobs2  Cedar McKay1  Ramesh K Jha3  Kyungyoon J Kwon4  Shawn R Starkenburg3 
[1] School of Oceanography, University of Washington, Seattle 98195, WA, USA;Biology Department, University of Washington, Seattle 98195, WA, USA;Bioscience Division, Los Alamos National Laboratory, Los Alamos 87545, NM, USA;Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley 94720, CA, USA
关键词: Gene divergence;    Genome evolution;    Stramenopiles;    Genome;    Mitochondria;    Chloroplast;    Nannochloropsis;   
Others  :  1217668
DOI  :  10.1186/1471-2164-15-212
 received in 2013-04-24, accepted in 2014-03-11,  发布年份 2014
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【 摘 要 】

Background

Microalgae in the genus Nannochloropsis are photosynthetic marine Eustigmatophytes of significant interest to the bioenergy and aquaculture sectors due to their ability to efficiently accumulate biomass and lipids for utilization in renewable transportation fuels, aquaculture feed, and other useful bioproducts. To better understand the genetic complement that drives the metabolic processes of these organisms, we present the assembly and comparative pangenomic analysis of the chloroplast and mitochondrial genomes from Nannochloropsis salina CCMP1776.

Results

The chloroplast and mitochondrial genomes of N. salina are 98.4% and 97% identical to their counterparts in Nannochloropsis gaditana. Comparison of the Nannochloropsis pangenome to other algae within and outside of the same phyla revealed regions of significant genetic divergence in key genes that encode proteins needed for regulation of branched chain amino synthesis (acetohydroxyacid synthase), carbon fixation (RuBisCO activase), energy conservation (ATP synthase), protein synthesis and homeostasis (Clp protease, ribosome).

Conclusions

Many organellar gene modifications in Nannochloropsis are unique and deviate from conserved orthologs found across the tree of life. Implementation of secondary and tertiary structure prediction was crucial to functionally characterize many proteins and therefore should be implemented in automated annotation pipelines. The exceptional similarity of the N. salina and N. gaditana organellar genomes suggests that N. gaditana be reclassified as a strain of N. salina.

【 授权许可】

   
2014 Starkenburg et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Green BR: Chloroplast genomes of photosynthetic eukaryotes. Plant J 2011, 66:34-44.
  • [2]Andersen RA, Brett RW, Potter D, Sexton JP: Phylogeny of the Eustigmatophyceae based upon 18S rDNA, with emphasis on Nannochloropsis. Protist 1998, 149:61-74.
  • [3]Rodolfi L, Chini Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR: Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 2009, 102:100-112.
  • [4]Chiu SY, Kao CY, Tsai MT, Ong SC, Chen CH, Lin CS: Lipid accumulation and CO2 utilization of Nannochloropsis oculata in response to CO2 aeration. Bioresour Technol 2009, 100:833-838.
  • [5]Van Vooren G, Le Grand F, Legrand J, Cuine S, Peltier G, Pruvost J: Investigation of fatty acids accumulation in Nannochloropsis oculata for biodiesel application. Bioresour Technol 2012, 124:421-432.
  • [6]Bucy H, Marchese AJ: Oxidative stability of algae derived methyl esters. J Eng Gas Turbines Power Trans 2012., 134
  • [7]Simionato D, Block MA, La Rocca N, Jouhet J, Marechal E, Finazzi G, Morosinotto T: Response of nannochloropsis gaditana to nitrogen starvation includes a De novo biosynthesis of triacylglycerols, a decrease of chloroplast galactolipids and a reorganization of the photosynthetic apparatus. Eukaryot Cell 2013, 12(5):665-76.
  • [8]Mohammady NG: Characterization of the fatty acid composition of Nannochloropsis salina as a determinant of biodiesel properties. J Biosci 2011, 66:328-332.
  • [9]Quinn JC, Yates T, Douglas N, Weyer K, Butler J, Bradley TH, Lammers PJ: Nannochloropsis production metrics in a scalable outdoor photobioreactor for commercial applications. Bioresour Technol 2012, 117:164-171.
  • [10]Wahidin S, Idris A, Shaleh SR: The influence of light intensity and photoperiod on the growth and lipid content of microalgae Nannochloropsis sp. Bioresour Technol 2013, 129:7-11.
  • [11]Hoffmann M, Marxen K, Schulz R, Vanselow KH: TFA and EPA productivities of Nannochloropsis salina influenced by temperature and nitrate stimuli in turbidostatic controlled experiments. Mar Drugs 2010, 8:2526-2545.
  • [12]Wei L, Xin Y, Wang D, Jing X, Zhou Q, Su X, Jia J, Ning K, Chen F, Hu Q, Xu J: Nannochloropsis plastid and mitochondrial phylogenomes reveal organelle diversification mechanism and intragenus phylotyping strategy in microalgae. BMC Genomics 2013, 14:534. BioMed Central Full Text
  • [13]Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC: Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 2012, 3:686.
  • [14]Pan K, Qin JJ, Li S, Dai WK, Zhu BH, Jin YC, Yu WG, Yang GP, Li DF: Nuclear monoploidy and asexual propagation of Nannochloropsis oceanica (Eustigmatophyceae) as revealed by its genome sequence. J Psychol 2011, 47:1425-1432.
  • [15]Guillard RR, Ryther JH: Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol 1962, 8:229-239.
  • [16]Bennett S: Solexa Ltd. Pharmacogenomics 2004, 5:433-438.
  • [17]Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, et al.: Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437:376-380.
  • [18]Zerbino DR, Birney E: Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18:821-829.
  • [19]Raymond CK, Subramanian S, Paddock M, Qiu RL, Deodato C, Palmieri A, Chang J, Radke T, Haugen E, Kas A, Waring D, Bovee D, Stacy R, Kaul R, Olson MV: Targeted, haplotype-resolved resequencing of long segments of the human genome. Genomics 2005, 86:759-766.
  • [20]Cattolico RA, Jacobs MA, Zhou Y, Chang J, Duplessis M, Lybrand T, McKay J, Ong HC, Sims E, Rocap G: Chloroplast genome sequencing analysis of Heterosigma akashiwo CCMP452 (West Atlantic) and NIES293 (West Pacific) strains. BMC Genomics 2008, 9:211. BioMed Central Full Text
  • [21]Hayden HS, Lim R, Brittnacher MJ, Sims EH, Ramage ER, Fong C, Wu Z, Crist E, Chang J, Zhou Y, Radey M, Rohmer L, Haugen E, Gillett W, Wuthiekanun V, Peacock SJ, Kaul R, Miller SI, Manoil C, Jacobs MA: Large-insert genome analysis technology detects structural variation in Pseudomonas aeruginosa clinical strains from cystic fibrosis patients. Genomics 2008, 91:530-537.
  • [22]Gordon D, Desmarais C, Green P: Automated finishing with autofinish. Genome Res 2001, 11:614-625.
  • [23]Hayden HS, Gillett W, Saenphimmachak C, Lim R, Zhou Y, Jacobs MA, Chang J, Rohmer L, D'Argenio DA, Palmieri A, Levy R, Haugen E, Wong GK, Brittnacher MJ, Burns JL, Miller SI, Olson MV, Kaul R: Evolution of Burkholderia pseudomallei in recurrent melioidosis. PLoS One 2012, 7:e36507.
  • [24]Delcher AL, Bratke KA, Powers EC, Salzberg SL: Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007, 23:673-679.
  • [25]Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW: RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007, 35:3100-3108.
  • [26]Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964.
  • [27]Laslett D, Canback B: ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 2004, 32:11-16.
  • [28]Regalia M, Rosenblad MA, Samuelsson T: Prediction of signal recognition particle RNA genes. Nucleic Acids Res 2002, 30:3368-3377.
  • [29]Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A: The Pfam protein families database. Nucleic Acids Res 2010, 38:D211-D222.
  • [30]Benson G: Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999, 27:573-580.
  • [31]Rice P, Longden I, Bleasby A: EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 2000, 16:276-277.
  • [32]Lohse M, Drechsel O, Bock R: OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 2007, 52:267-274.
  • [33]Le Corguille G, Pearson G, Valente M, Viegas C, Gschloessl B, Corre E, Bailly X, Peters AF, Jubin C, Vacherie B, Cock JM, Leblanc C: Plastid genomes of two brown algae. Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids. BMC Evol Biol 2009, 9:253. BioMed Central Full Text
  • [34]Ong HC, Wilhelm SW, Gobler CJ, Bullerjahn G, Jacobs MA, McKay J, Sims EH, Gillett WG, Zhou Y, Haugen E, Rocap G, Cattolico RA: Analyses of the complete chloroplast genome sequences of two members of the Pelagophyceae: Aureococcus anophagefferens Ccmp 1984 and Aureoumbra lagunensis Ccmp1507. J Phycol 2010, 46:602-615.
  • [35]Oudot-Le Secq MP, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BR: Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol Genet Genomics 2007, 277:427-439.
  • [36]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
  • [37]Zhang Y: I-TASSER server for protein 3D structure prediction. BMC Bioinforma 2008, 9:40. BioMed Central Full Text
  • [38]Bradley P, Misura KM, Baker D: Toward high-resolution de novo structure prediction for small proteins. Science 2005, 309:1868-1871.
  • [39]Raman S, Vernon R, Thompson J, Tyka M, Sadreyev R, Pei J, Kim D, Kellogg E, DiMaio F, Lange O, Kinch L, Sheffler W, Kim BH, Das R, Grishin NV, Baker D: Structure prediction for CASP8 with all-atom refinement using Rosetta. Proteins 2009, 77(Suppl 9):89-99.
  • [40]Kim DE, Chivian D, Baker D: Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 2004, 32:W526-W531.
  • [41]Jones DT: Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 1999, 292:195-202.
  • [42]Wilkens S, Dunn SD, Chandler J, Dahlquist FW, Capaldi RA: Solution structure of the N-terminal domain of the delta subunit of the E. coli ATP synthase. Nat Struct Biol 1997, 4:198-201.
  • [43]Carbajo RJ, Kellas FA, Runswick MJ, Montgomery MG, Walker JE, Neuhaus D: Structure of the F1-binding domain of the stator of bovine F1Fo-ATPase and how it binds an alpha-subunit. J Mol Biol 2005, 351:824-838.
  • [44]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
  • [45]Buchan DW, Ward SM, Lobley AE, Nugent TC, Bryson K, Jones DT: Protein annotation and modelling servers at University College London. Nucleic Acids Res 2010, 38:W563-W568.
  • [46]Pollastri G, McLysaght A: Porter: a new, accurate server for protein secondary structure prediction. Bioinformatics 2005, 21:1719-1720.
  • [47]Soding J, Biegert A, Lupas AN: The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005, 33:W244-W248.
  • [48]Chaudhury S, Berrondo M, Weitzner BD, Muthu P, Bergman H, Gray JJ: Benchmarking and analysis of protein docking performance in Rosetta v3.2. PLoS One 2011, 6:e22477.
  • [49]Gray JJ, Moughon S, Wang C, Schueler-Furman O, Kuhlman B, Rohl CA, Baker D: Protein-protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations. J Mol Biol 2003, 331:281-299.
  • [50]Racine J: gnuplot 4.0: A portable interactive plotting utility. J Appl Econ 2006, 21:133-141.
  • [51]Rohl CA, Strauss CEM, Misura KMS, Baker D: Protein structure prediction using rosetta. Num Comput Methods 2004, 383:66-+.
  • [52]Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J: ACT: the artemis comparison tool. Bioinformatics 2005, 21:3422-3423.
  • [53]Thorvaldsdottir H, Robinson JT, Mesirov JP: Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2012.
  • [54]Lambowitz AM, Zimmerly S: Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol 2011, 3:a003616.
  • [55]Oudot-Le Secq MP, Fontaine JM, Rousvoal S, Kloareg B, Loiseaux-De Goer S: The complete sequence of a brown algal mitochondrial genome, the ectocarpale Pylaiella littoralis (L.) Kjellm. J Mol Evol 2001, 53(2):80-88.
  • [56]Ikuta K, Kawai H, Muller DG, Ohama T: Recurrent invasion of mitochondrial group II introns in specimens of Pylaiella littoralis (brown alga), collected worldwide. Curr Genet 2008, 53:207-216.
  • [57]Ravin NV, Galachyants YP, Mardanov AV, Beletsky AV, Petrova DP, Sherbakova TA, Zakharova YR, Likhoshway YV, Skryabin KG, Grachev MA: Complete sequence of the mitochondrial genome of a diatom alga Synedra acus and comparative analysis of diatom mitochondrial genomes. Curr Genet 2010, 56:215-223.
  • [58]Wang RJ, Cheng CL, Chang CC, Wu CL, Su TM, Chaw SM: Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol Biol 2008., 8
  • [59]Wicke S, Schneeweiss GM, dePamphilis CW, Muller KF, Quandt D: The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol 2011, 76:273-297.
  • [60]Bourne CM, Palmer JD, Stoermer EF: Organization of the chloroplast genome of the fresh-water centric diatom Cyclotella meneghiniana. J Psychol 1992, 28:347-355.
  • [61]Udy DB, Belcher S, Williams-Carrier R, Gualberto JM, Barkan A: Effects of reduced chloroplast gene copy number on chloroplast gene expression in Maize. Plant Physiol 2012, 160:1420-1431.
  • [62]Hollingshead S, Kopecna J, Jackson PJ, Canniffe DP, Davison PA, Dickman MJ, Sobotka R, Hunter CN: Conserved chloroplast open-reading frame ycf54 is required for activity of the magnesium protoporphyrin monomethylester oxidative cyclase in Synechocystis PCC 6803. J Biol Chem 2012, 287:27823-27833.
  • [63]Oudot MP, Kloareg B, Loiseaux-de Goer S: The mitochondrial Pylaiella littoralis nad11 gene contains only the N-terminal FeS-binding domain. Gene 1999, 235:131-137.
  • [64]Vanselow C, Weber AP, Krause K, Fromme P: Genetic analysis of the Photosystem I subunits from the red alga, Galdieria sulphuraria. Biochim Biophys Acta 2009, 1787:46-59.
  • [65]Mueller-Cajar O, Stotz M, Wendler P, Hartl FU, Bracher A, Hayer-Hartl M: Structure and function of the AAA + protein CbbX, a red-type Rubisco activase. Nature 2011, 479:194-199.
  • [66]Tchernov D, Livne A, Kaplan A, Sukenik A: The kinetic properties of ribulose-1,5-bisphosphate carboxylase/oxygenase may explain the high apparent photosynthetic affinity of Nannochloropsis sp to ambient inorganic carbon. Isr J Plant Sci 2008, 56:37-44.
  • [67]Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, Manhart JR: Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc Natl Acad Sci USA 2008, 105:17867-17871.
  • [68]Stec B: Structural mechanism of RuBisCO activation by carbamylation of the active site lysine. Proc Natl Acad Sci USA 2012, 109:18785-18790.
  • [69]Moreno J, Garcia-Murria MJ, Marin-Navarro J: Redox modulation of Rubisco conformation and activity through its cysteine residues. J Exp Bot 2008, 59:1605-1614.
  • [70]Sakihama Y, Nakamura S, Yamasaki H: Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organisms. Plant Cell Physiol 2002, 43:290-297.
  • [71]Barak Z, Chipman DM: Allosteric regulation in Acetohydroxyacid Synthases (AHASs)–different structures and kinetic behavior in isozymes in the same organisms. Arch Biochem Biophys 2012, 519:167-174.
  • [72]Belenky I, Steinmetz A, Vyazmensky M, Barak Z, Tittmann K, Chipman DM: Many of the functional differences between acetohydroxyacid synthase (AHAS) isozyme I and other AHASs are a result of the rapid formation and breakdown of the covalent acetolactate-thiamin diphosphate adduct in AHAS I. FEBS J 2012, 279:1967-1979.
  • [73]Lee YT, Duggleby RG: Regulatory interactions in Arabidopsis thaliana acetohydroxyacid synthase. FEBS Lett 2002, 512:180-184.
  • [74]Duggleby RG, McCourt JA, Guddat LW: Structure and mechanism of inhibition of plant acetohydroxyacid synthase. Plant Physiol Biochem 2008, 46:309-324.
  • [75]Boczar BA, Delaney TP, Cattolico RA: Gene for the ribulose-1,5-bisphosphate carboxylase small subunit protein of the marine chromophyte Olisthodiscus luteus is similar to that of a chemoautotrophic bacterium. Proc Natl Acad Sci USA 1989, 86:4996-4999.
  • [76]von Ballmoos C, Wiedenmann A, Dimroth P: Essentials for ATP synthesis by F1F0 ATP synthases. Annu Rev Biochem 2009, 78:649-672.
  • [77]von Ballmoos C, Cook GM, Dimroth P: Unique rotary ATP synthase and its biological diversity. Annu Rev Biophys 2008, 37:43-64.
  • [78]Vieler A, Wu G, Tsai CH, Bullard B, Cornish AJ, Harvey C, Reca IB, Thornburg C, Achawanantakun R, Buehl CJ, Campbell MS, Cavalier D, Childs KL, Clark TJ, Deshpande R, Erickson E, Armenia Ferguson A, Handee W, Kong Q, Li X, Liu B, Lundback S, Peng C, Roston RL, Sanjaya , Simpson JP, Terbush A, Warakanont J, Zauner S, Farre EM: Genome, functional gene annotation, and nuclear transformation of the Heterokont Oleaginous Alga Nannochloropsis oceanica CCMP1779. PLoS Genet 2012, 8:e1003064.
  • [79]Stoebe B, Kowallik KV: Gene-cluster analysis in chloroplast genomics. Trends Genet 1999, 15:344-347.
  • [80]Prescott M, Bush NC, Nagley P, Devenish RJ: Properties of yeast cells depleted of the OSCP subunit of mitochondrial ATP synthase by regulated expression of the ATP5 gene. Biochem Mol Biol Int 1994, 34:789-799.
  • [81]Hazard AL, Senior AE: Defective energy coupling in delta-subunit mutants of Escherichia coli F1F0-ATP synthase. J Biol Chem 1994, 269:427-432.
  • [82]Stack AE, Cain BD: Mutations in the delta subunit influence the assembly of F1F0 ATP synthase in Escherichia coli. J Bacteriol 1994, 176:540-542.
  • [83]Maiwald D, Dietzmann A, Jahns P, Pesaresi P, Joliot P, Joliot A, Levin JZ, Salamini F, Leister D: Knock-out of the genes coding for the Rieske protein and the ATP-synthase delta-subunit of Arabidopsis. Effects on photosynthesis, thylakoid protein composition, and nuclear chloroplast gene expression. Plant Physiol 2003, 133:191-202.
  • [84]Rees DM, Leslie AG, Walker JE: The structure of the membrane extrinsic region of bovine ATP synthase. Proc Natl Acad Sci USA 2009, 106:21597-21601.
  • [85]Wilkens S, Borchardt D, Weber J, Senior AE: Structural characterization of the interaction of the delta and alpha subunits of the Escherichia coli F1F0-ATP synthase by NMR spectroscopy. Biochemistry 2005, 44:11786-11794.
  • [86]Wang F, Mei Z, Qi Y, Yan C, Hu Q, Wang J, Shi Y: Structure and mechanism of the hexameric MecA-ClpC molecular machine. Nature 2011, 471:331-335.
  • [87]Zeth K, Ravelli RB, Paal K, Cusack S, Bukau B, Dougan DA: Structural analysis of the adaptor protein ClpS in complex with the N-terminal domain of ClpA. Nat Struct Biol 2002, 9:906-911.
  • [88]Schuenemann VJ, Kralik SM, Albrecht R, Spall SK, Truscott KN, Dougan DA, Zeth K: Structural basis of N-end rule substrate recognition in Escherichia coli by the ClpAP adaptor protein ClpS. Embo Rep 2009, 10:508-514.
  • [89]Kirstein J, Moliere N, Dougan DA, Turgay K: Adapting the machine: adaptor proteins for Hsp100/Clp and AAA + proteases. Nat Rev Microbiol 2009, 7:589-599.
  • [90]Tryggvesson A, Stahlberg FM, Mogk A, Zeth K, Clarke AK: Interaction specificity between the chaperone and proteolytic components of the cyanobacterial Clp protease. Biochem J 2012, 446:311-320.
  • [91]Andersson FI, Blakytny R, Kirstein J, Turgay K, Bukau B, Mogk A, Clarke AK: Cyanobacterial ClpC/HSP100 protein displays intrinsic chaperone activity. J Biol Chem 2006, 281:5468-5475.
  • [92]Kress W, Maglica Z, Weber-Ban E: Clp chaperone-proteases: structure and function. Res Microbiol 2009, 160:618-628.
  • [93]Wickner S, Gottesman S, Skowyra D, Hoskins J, McKenney K, Maurizi MR: A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc Natl Acad Sci USA 1994, 91:12218-12222.
  • [94]Weibezahn J, Schlieker C, Bukau B, Mogk A: Characterization of a trap mutant of the AAA + chaperone ClpB. J Biol Chem 2003, 278:32608-32617.
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