Evolution of acyl-ACP thioesterases and β-ketoacyl-ACP synthases revealed by protein-protein interactions

Journal of Applied Phycology

Volumn 26, Issue 4, 2014, Pages 1619-1629

  Beld, Joris ^a   Blatti, Jillian L ^a   Behnke, Craig ^b   Mendez, Michael ^b   Burkart, Michael D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Sapphire Energy Inc   (United States)

Author keywords

Acyl carrier protein; Algae; Bacteria; Chlamydomonas reinhardtii; Evolution; Fatty acid synthase

Indexed keywords

EID: 84905264609     PISSN: 09218971     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10811-013-0203-4     Document Type: Article

References (63)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Andre C, Haslam RP, Shanklin J (2012) Feedback regulation of plastidic acetyl-CoA carboxylase by 18: 1-acyl carrier protein in Brassica napus. Proc Natl Acad Sci U S A 109: 10107-10112.
3. Atteia A, Adrait A, Brugière S, Tardif M, van Lis R, Deusch O, Dagan T, Kuhn L, Gontero B, Martin W (2009) A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the α-proteobacterial mitochondrial ancestor. Mol Biol Evol 26: 1533-1548.
4. Blatti JL, Beld J, Behnke CA, Mendez M, Mayfield SP, Burkart MD (2012) Manipulating fatty acid biosynthesis in microalgae for biofuel through protein-protein interactions. PLoS ONE 7(9).
5. Campbell JW, Cronan JE (2001) Bacterial fatty acid biosynthesis: targets for antibacterial drug discovery. Annu Rev Microbiol 55: 305-332.
6. Cantu DC, Chen Y, Reilly PJ (2010) Thioesterases: a new perspective based on their primary and tertiary structures. Protein Sci 19: 1281-1295.
7. Cantu DC, Chen Y, Lemons ML, Reilly PJ (2011) ThYme: a database for thioester-active enzymes. Nucleic Acids Res 39/suppl 1: D342-D346.
8. Cantu DC, Dai T, Beversdorf ZS, Reilly PJ (2012a) Structural classification and properties of ketoacyl reductases, hydroxyacyl dehydratases, and enoyl reductases. Protein Eng Des Sel 25: 803-811.
9. Cantu DC, Forrester MJ, Charov K, Reilly PJ (2012b) Acyl carrier protein structural classification and normal mode analysis. Protein Sci 21: 655-666.
10. Chen Y, Kelly EE, Masluk RP, Nelson CL, Cantu DC, Reilly PJ (2011) Structural classification and properties of ketoacyl synthases. Protein Sci 20: 1659-1667.
11. Cho H, Cronan JE (1993) Escherichia coli thioesterase I, molecular cloning, and sequencing of the structural gene and identification as a periplasmic enzyme. J Biol Chem 268: 9238-9245.
12. Comeau SR, Gatchell DW, Vajda S, Camacho CJ (2004) ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20: 45-50.
13. Crosby J, Crump MP (2012) The structural role of the carrier protein-active controller or passive carrier. Nat Prod Rep 29: 1111-1137.
14. Cryle MJ (2010) Selectivity in a barren landscape: the P450BioIACP complex. Biochem Soc Trans 38: 934.
15. Davies HM, Anderson L, Fan C, Hawkins DJ (1991) Developmental induction, purification, and further characterization of 12: 0-ACP thioesterase from immature cotyledons of Umbellularia californica. Arch Biochem Biophys 290: 37-45.
16. Davis MS, Cronan JE (2001) Inhibition of Escherichia coli acetyl coenzyme A carboxylase by acyl-acyl carrier protein. J Bacteriol 183: 1499-1503.
17. De Lay NR, Cronan JE (2007) In vivo functional analyses of the type II acyl carrier proteins of fatty acid biosynthesis. J Biol Chem 282: 20319-20328.
18. Dörmann P, Spener F, Ohlrogge JB (1993) Characterization of two acyl-acyl carrier protein thioesterases from developing Cuphea seeds specific for medium-chain- and oleoyl-acyl carrier protein. Planta 189: 425-432.
19. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
20. Feng Y, Cronan JE (2009) Escherichia coli unsaturated fatty acid synthesis: complex transcription of the FabA gene and in vivo identification of the essential reaction catalyzed by FabB. J Biol Chem 284: 29526-29535.
21. Florova G, Kazanina G, Reynolds KA (2002) Enzymes involved in fatty acid and polyketide biosynthesis in Streptomyces glaucescens: role of FabH and FabD and their acyl carrier protein specificity. Biochemistry 41: 10462-10471.
22. Goldschmidt-Clermont M (1991) Transgenic expression of aminoglycoside adenine transferase in the chloroplast: a selectable marker for site-directed transformation of Chlamydomonas. Nucleic Acids Res 19: 4083-4089.
23. Gong Y, Guo X, Wan X, Liang Z, Jiang M (2011) Characterization of a novel thioesterase (PtTE) from Phaeodactylum tricornutum. J Basic Microbiol 51: 666-672.
24. Gorman DS, Levine RP (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 54: 1665-1669.
25. Gouet P, Courcelle E, Stuart DI, Métoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.
26. Guerra DJ, Browse JA (1990) Escherichia coli β-hydroxydecanoyl thioester dehydrase reacts with native C10 acyl-acyl-carrier proteins of plant and bacterial origin. Arch Biochem Biophys 280: 336-345.
27. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
28. Jiang C, Kim SY, Suh DY (2008) Divergent evolution of the thiolase superfamily and chalcone synthase family. Mol Phylogenet Evol 49: 691-701.
29. Jing F, Cantu DC, Tvaruzkova J, Chipman JP, Nikolau BJ, Yandeau-Nelson MD, Reilly PJ (2011) Phylogenetic and experimental characterization of an acyl-ACP thioesterase family reveals significant diversity in enzymatic specificity and activity. BMC Biochem 12: 44 d oi: 10. 1186/1471-2091-12-44.
30. Jones A, Davies HM, Voelker TA (1995) Palmitoyl-acyl carrier protein (ACP) thioesterase and the evolutionary origin of plant acyl-ACP thioesterases. Plant Cell 7: 359-371.
31. Kaewsuwan S, Bunyapraphatsara N, Cove DJ, Quatrano RS, Chodok P (2010) High level production of adrenic acid in Physcomitrella patens using the algae Pavlova sp. Δ5-elongase gene. Bioresour Technol 101: 4081-4088.
32. Kan Y, Pan J (2010) A one-shot solution to bacterial and fungal contamination in the green alga Chlamydomonas reinhardtii culture by using an antibiotic cocktail. J Phycol 46: 1356-1358.
33. Kay SA, Lis E, Golden S, Melnick M, Adin DM, Golden JW (2012) Methods and compositions for the production of fatty acids in photosynthetic prokaryotic microorganisms. US Patent Application 2012/0184004 A1.
34. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H (2006) Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res 12: 291-299.
35. Kosa NM, Haushalter RW, Smith AR, Burkart MD (2012) Reversible labeling of native and fusion-protein motifs. Nat Methods 9: 981-984.
36. Lambalot RH, Gehring AM, Flugel RS, Zuber P, LaCelle M, Marahiel MA, Reid R, Khosla C, Walsh CT (1996) A new enzyme superfamily: the phosphopantetheinyl transferases. Chem Biol 3: 923-936.
37. Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16: 750-759.
38. Liu X, Sheng J, Curtiss III R (2011) Fatty acid production in genetically modified cyanobacteria. Proc Natl Acad Sci U S A 108: 6899-6904.
39. Lo YC, Lin SC, Shaw JF, Liaw YC (2003) Crystal structure of Escherichia coli thioesterase I/protease I/lysophospholipase L1: Consensus sequence blocks constitute the catalytic center of SGNH-hydrolases through a conserved hydrogen bond network. J Mol Biol 330: 539-551.
40. McCarthy AD, Hardie DG (1984) Fatty acid synthase-an example of protein evolution by gene fusion. Trends Biochem Sci 9: 60-63.
41. Meuser JE, Boyd ES, Ananyev G, Karns D, Radakovits R, Murthy UMN, Ghirardi ML, Dismukes GC, Peters JW, Posewitz MC (2011) Evolutionary significance of an algal gene encoding an [FeFe]-hydrogenase with F-domain homology and hydrogenase activity in Chlorella variabilis NC64A. Planta 234: 829-843.
42. Notredame C, Higgins DG, Heringa J (2000) T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.
43. Price MN, Dehal PS, Arkin AP (2010) FastTree 2-Approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3).
44. Pymol (2012). The PyMOL Molecular Graphics System, Version 1504 Schrödinger, LLC.
45. Radakovits R, Eduafo PM, Posewitz MC (2011) Genetic engineering of fatty acid chain length in Phaeodactylum tricornutum. Metab Eng 13: 89-95.
46. Rambaut A (2009)http://tree. bio. ed. ac. uk/software/figtree/.
47. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
48. Ryall K, Harper JT, Keeling PJ (2003) Plastid-derived type II fatty acid biosynthetic enzymes in chromists. Gene 313: 139-148.
49. Saito K, Hamajima A, Ohkuma M, Murakoshi I, Ohmori S, Kawaguchi A, Teeri TH, Cronan Jnr JE (1995) Expression of the Escherichia coli FabA gene encoding beta-hydroxydecanoyl thioester dehydrase and transport to chloroplasts in transgenic tobacco. Transgenic Res 4: 60-69.
50. Salas JJ, Ohlrogge JB (2002) Characterization of substrate specificity of plant FatA and FatB acyl-ACP thioesterases. Arch Biochem Biophys 403: 25-34.
51. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385.
52. Srikanta Dani KG, Hatti KS, Ravikumar P, Kush A (2011) Structural and functional analyses of a saturated acyl ACP thioesterase, type B from immature seed tissue of Jatropha curcas. Plant Biol 13: 453-461.
53. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
54. Tardif M, Atteia A, Specht M, Cogne G, Rolland N, Brugière S, Hippler M, Ferro M, Bruley C, Peltier G (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol 29: 3625-3639.
55. Thelen JJ, Ohlrogge JB (2002) Metabolic engineering of fatty acid biosynthesis in plants. Metab Eng 4: 12-21.
56. Voelker TA, Davies HM (1994) Alteration of the specificity and regulation of fatty acid synthesis of Escherichia coli by expression of a plant medium-chain acyl-acyl carrier protein thioesterase. J Bacteriol 176: 7320-7327.
57. Volkmann G, Murphy PW, Rowland EE, Cronan JE Jr, Liu XQ, Blouin C, Byers DM (2010) Intein-mediated cyclization of bacterial acyl carrier protein stabilizes its folded conformation but does not abolish function. J Biol Chem 285: 8605-8614.
58. Worthington AS, Rivera H, Torpey JW, Alexander MD, Burkart MD (2006) Mechanism-based protein cross-linking probes to investigate carrier protein-mediated biosynthesis. ACS Chem Biol 1: 687-691.
59. Worthington AS, Hur GH, Meier JL, Cheng Q, Moore BS, Burkart MD (2008) Probing the compatibility of type II ketosynthase-carrier protein partners. ChemBioChem 9: 2096-2103.
60. Yu XH, Rawat R, Shanklin J (2011) Characterization and analysis of the cotton cyclopropane fatty acid synthase family and their contribution to cyclopropane fatty acid synthesis. BMC Plant Biol 11: 97. doi: 10. 1186/1471-2229-11-97.
61. Yuan L, Voelker TA, Hawkins DJ (1995) Modification of the substrate specificity of an acyl-acyl carrier protein thioesterase by protein engineering. Proc Natl Acad Sci U S A 92: 10639-10643.
62. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinforma 9.
63. Zornetzer GA, Tanem J, Fox BG, Markley JL (2010) The length of the bound fatty acid influences the dynamics of the acyl carrier protein and the stability of the thioester bond. Biochemistry 49/3: 470-477.