Skip to main content

Classification of Lipolytic Enzymes from Bacteria

Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Lipolytic enzymes including lipases and esterases comprise a versatile group of enzymes with diverse amino acid sequences but related three-dimensional structures. Despite the large number of bacterial lipolytic enzymes so far identified (~5000), only a small portion (<10%) was cloned, expressed, and experimentally studied. Twenty years ago, Arpigny and Jaeger published a seminal study which systematically grouped bacterial lipolytic enzymes into eight families according to similarity of their amino acid sequences and physiological properties (Arpigny and Jaeger, Biochem J 343:177–183, 1999). Here, we present a comprehensive overview as an extension of the original classification covering all 19 presently known families of lipolytic enzymes. The conserved features of sequences and structures are described for all families in order to simplify the assignment of newly discovered lipolytic enzymes to the respective family. Furthermore, we have correlated the biochemical properties of some enzymes with the nature of the often extremophilic microorganism from which the respective enzyme was isolated. This may help to identify lipase families with potential as biocatalysts in industrial applications. As an example, family XV enzymes are stable and active at elevated temperatures; thus, enzymes of this family represent a potential source for novel biocatalysts.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Aamand JL, Hobson AH, Buckley CM, Jorgensen ST, Diderichsen B, McConnell DJ (1994) Chaperone-mediated activation in vivo of a Pseudomonas cepacia lipase. Mol Gen Genet 245:556–564

    CrossRef  CAS  PubMed  Google Scholar 

  • Akatsuka H, Kawai E, Omori K, Komatsubara S, Shibatani T, Tosa T (1994) The lipA gene of Serratia marcescens which encodes an extracellular lipase having no N-terminal signal peptide. J Bacteriol 176:1949–1956

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Akoh CC, Lee GC, Liaw YC, Huang TH, Shaw JF (2004) GDSL family of serine esterases/lipases. Prog Lipid Res 43:534–552

    CrossRef  CAS  PubMed  Google Scholar 

  • Akutsu-Shigeno Y, Teeraphatpornchai T, Teamtisong K, Nomura N, Uchiyama H, Nakahara T, Nakajima-Kambe T (2003) Cloning and sequencing of a poly(DL-lactic acid) depolymerase gene from Paenibacillus amylolyticus strain TB-13 and its functional expression in Escherichia coli. Appl Environ Microbiol 69:2498–2504

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali YB, Verger R, Abousalham A (2012) Lipases or esterases: does it really matter? Toward a new bio-physico-chemical classification. Methods Mol Biol 861:31–51

    CrossRef  PubMed  CAS  Google Scholar 

  • Amada K, Haruki M, Imanaka T, Morikawa M, Kanaya S (2000) Overproduction in Escherichia coli, purification and characterization of a family I3 lipase from Pseudomonas sp. MIS38. Biochim Biophys Acta 1478:201–210

    CrossRef  CAS  PubMed  Google Scholar 

  • Arpigny JL, Jaeger K-E (1999) Bacterial lipolytic enzymes: classification properties. Biochem J 343:177–183

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassegoda A, Pastor FI, Diaz P (2012) Rhodococcus sp. strain CR-53 LipR, the first member of a new bacterial lipase family (family X) displaying an unusual Y-type oxyanion hole, similar to the Candida antarctica lipase clan. Appl Environ Microbiol 78:1724–1732

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Bauche C, Chenal A, Knapp O, Bodenreider C, Benz R, Chaffotte A, Ladant D (2006) Structural and functional characterization of an essential RTX subdomain of Bordetella pertussis adenylate cyclase toxin. J Biol Chem 281:16914–16926

    CrossRef  CAS  PubMed  Google Scholar 

  • Ben Ali Y, Chahinian H, Petry S, Muller G, Carriere F, Verger R, Abousalham A (2004) Might the kinetic behavior of hormone-sensitive lipase reflect the absence of the lid domain? Biochemistry 43:9298–9306

    CrossRef  CAS  PubMed  Google Scholar 

  • Ben Ali Y, Chahinian H, Petry S, Muller G, Lebrun R, Verger R, Carrière F, Mandrich L, Rossi M, Manco G, Sarda L, Abousalham A (2006) Use of an inhibitor to identify members of the hormone-sensitive lipase family. Biochemistry 45:14183–14191

    CrossRef  CAS  PubMed  Google Scholar 

  • Brady L, Brzozowski AM, Derewenda ZS, Dodson E, Dodson G, Tolley S, Turkenburg JP, Christiansen L, Huge-Jensen B, Norskov L et al (1990) A serine protease triad forms the catalytic centre of a triacylglycerol lipase. Nature 343:767–770

    CrossRef  CAS  PubMed  Google Scholar 

  • Braun P, Tommassen J, Filloux A (1996) Role of the propeptide in folding and secretion of elastase of Pseudomonas aeruginosa. Mol Microbiol 19:297–306

    CrossRef  CAS  PubMed  Google Scholar 

  • Brenner S (1988) The molecular evolution of genes and proteins: a tale of two serines. Nature 334:528–530

    CrossRef  CAS  PubMed  Google Scholar 

  • Brockerhoff J, Jensen RG (1974) Lipolytic enzymes. Academic, New York

    CrossRef  Google Scholar 

  • Brzozowski AM, Derewenda U, Derewenda ZS, Dodson GG, Lawson DM, Turkenburg JP, Bjorkling F, Huge-Jensen B, Patkar SA, Thim L (1991) A model for interfacial activation in lipases from the structure of a fungal lipase-inhibitor complex. Nature 351:491–494

    CrossRef  CAS  PubMed  Google Scholar 

  • Castilla A, Panizza P, Rodriguez D, Bonino L, Diaz P, Irazoqui G, Rodriguez Giordano S (2017) A novel thermophilic and halophilic esterase from Janibacter sp. R02, the first member of a new lipase family (Family XVII). Enzyme Microb Technol 98:86–95

    CrossRef  CAS  PubMed  Google Scholar 

  • Chahinian H, Ali YB, Abousalham A, Petry S, Mandrich L, Manco G, Canaan S, Sarda L (2005) Substrate specificity and kinetic properties of enzymes belonging to the hormone-sensitive lipase family: comparison with non-lipolytic and lipolytic carboxylesterases. Biochim Biophys Acta 1738:29–36

    CrossRef  CAS  PubMed  Google Scholar 

  • Charbonneau DM, Beauregard M (2013) Role of key salt bridges in thermostability of G. thermodenitrificans EstGtA2: distinctive patterns within the new bacterial lipolytic enzyme subfamily XIII2 [corrected]. PLoS One 8:e76675

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Charbonneau DM, Meddeb-Mouelhi F, Beauregard M (2010) A novel thermostable carboxylesterase from Geobacillus thermodenitrificans: evidence for a new carboxylesterase family. J Biochem 148:299–308

    CrossRef  CAS  PubMed  Google Scholar 

  • Chow J, Kovacic F, Dall Antonia Y, Krauss U, Fersini F, Schmeisser C, Lauinger B, Bongen P, Pietruszka J, Schmidt M, Menyes I, Bornscheuer UT, Eckstein M, Thum O, Liese A, Mueller-Dieckmann J, Jaeger KE, Streit WR (2012) The metagenome-derived enzymes LipS and LipT increase the diversity of known lipases. PLoS One 7:e47665

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Cruz H, Perez C, Wellington E, Castro C, Servin-Gonzalez L (1994) Sequence of the Streptomyces albus G lipase-encoding gene reveals the presence of a prokaryotic lipase family. Gene 144:141–142

    CrossRef  CAS  PubMed  Google Scholar 

  • Dautin N, Bernstein HD (2007) Protein secretion in Gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 61:89–112

    CrossRef  CAS  PubMed  Google Scholar 

  • de Pascale D, Cusano AM, Autore F, Parrilli E, di Prisco G, Marino G, Tutino ML (2008) The cold-active Lip1 lipase from the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125 is a member of a new bacterial lipolytic enzyme family. Extremophiles 12:311–323

    CrossRef  CAS  PubMed  Google Scholar 

  • De Simone G, Galdiero S, Manco G, Lang D, Rossi M, Pedone C (2000) A snapshot of a transition state analogue of a novel thermophilic esterase belonging to the subfamily of mammalian hormone-sensitive lipase. J Mol Biol 303:761–771

    CrossRef  PubMed  CAS  Google Scholar 

  • De Simone G, Menchise V, Manco G, Mandrich L, Sorrentino N, Lang D, Rossi M, Pedone C (2001) The crystal structure of a hyper-thermophilic carboxylesterase from the archaeon Archaeoglobus fulgidus. J Mol Biol 314:507–518

    CrossRef  CAS  PubMed  Google Scholar 

  • Devedjiev Y, Dauter Z, Kuznetsov SR, Jones TL, Derewenda ZS (2000) Crystal structure of the human acyl protein thioesterase I from a single X-ray data set to 1.5 Å. Structure 8:1137–1146

    CrossRef  CAS  PubMed  Google Scholar 

  • Downie MM, Guy R, Kealey T (2004) Advances in sebaceous gland research: potential new approaches to acne management. Int J Cosmet Sci 26:291–311

    CrossRef  CAS  PubMed  Google Scholar 

  • Driessen AJ, Fekkes P, van der Wolk JP (1998) The Sec system. Curr Opin Microbiol 1:216–222

    CrossRef  CAS  PubMed  Google Scholar 

  • Duncan JA, Gilman AG (1998) A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21(RAS). J Biol Chem 273:15830–15837

    CrossRef  CAS  PubMed  Google Scholar 

  • Duong F, Wickner W (1997) Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J 16:2756–2768

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Economou A (1998) Bacterial preprotein translocase: mechanism and conformational dynamics of a processive enzyme. Mol Microbiol 27:511–518

    CrossRef  CAS  PubMed  Google Scholar 

  • El Khattabi M, Ockhuijsen C, Bitter W, Jaeger K-E, Tommassen J (1999) Specificity of the lipase-specific foldases of Gram-negative bacteria and the role of the membrane anchor. Mol Gen Genet 261:770–776

    CrossRef  PubMed  Google Scholar 

  • Elend C, Schmeisser C, Leggewie C, Babiak P, Carballeira JD, Steele HL, Reymond JL, Jaeger K-E, Streit WR (2006) Isolation and biochemical characterization of two novel metagenome-derived esterases. Appl Environ Microbiol 72:3637–3645

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Evangelista-Martinez Z, Gonzalez-Ceron G, Servin-Gonzalez L (2006) A conserved inverted repeat, the LipR box, mediates transcriptional activation of the Streptomyces exfoliatus lipase gene by LipR, a member of the STAND class of P-loop nucleoside triphosphatases. J Bacteriol 188:7082–7089

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Ewis HE, Abdelal AT, Lu CD (2004) Molecular cloning and characterization of two thermostable carboxyl esterases from Geobacillus stearothermophilus. Gene 329:187–195

    CrossRef  CAS  PubMed  Google Scholar 

  • Feller G, Thiry M, Gerday C (1990) Sequence of a lipase gene from the antarctic psychrotroph Moraxella TA144. Nucleic Acids Res 18:6431

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Frenken LG, Bos JW, Visser C, Muller W, Tommassen J, Verrips CT (1993a) An accessory gene, lipB, required for the production of active Pseudomonas glumae lipase. Mol Microbiol 9:579–589

    CrossRef  CAS  PubMed  Google Scholar 

  • Frenken LG, de Groot A, Tommassen J, Verrips CT (1993b) Role of the lipB gene product in the folding of the secreted lipase of Pseudomonas glumae. Mol Microbiol 9:591–599

    CrossRef  CAS  PubMed  Google Scholar 

  • Goosens VJ, van Dijl JM (2017) Twin-arginine protein translocation. Curr Top Microbiol Immunol 404:69–94

    CAS  PubMed  Google Scholar 

  • Gotz F, Verheij HM, Rosenstein R (1998) Staphylococcal lipases: molecular characterisation, secretion, and processing. Chem Phys Lipids 93:15–25

    CrossRef  CAS  PubMed  Google Scholar 

  • Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38:695–699

    CrossRef  CAS  Google Scholar 

  • Govardhan CP, Pratt RF (1987) Kinetics and mechanism of the serine beta-lactamase catalyzed hydrolysis of depsipeptides. Biochemistry 26:3385–3395

    CrossRef  CAS  PubMed  Google Scholar 

  • Hanada M, Nishiyama KI, Mizushima S, Tokuda H (1994) Reconstitution of an efficient protein translocation machinery comprising SecA and the three membrane proteins, SecY, SecE, and SecG (p12). J Biol Chem 269:23625–23631

    CAS  PubMed  Google Scholar 

  • Handrick R, Reinhardt S, Focarete ML, Scandola M, Adamus G, Kowalczuk M, Jendrossek D (2001) A new type of thermoalkalophilic hydrolase of Paucimonas lemoignei with high specificity for amorphous polyesters of short chain-length hydroxyalkanoic acids. J Biol Chem 276:36215–36224

    CrossRef  CAS  PubMed  Google Scholar 

  • Hashizume S, Sekiguchi T, Nosoh Y (1976) Effect of temperature on the viability of Bacillus stearothermophilus. Arch Microbiol 107:75–80

    CrossRef  CAS  PubMed  Google Scholar 

  • Hassing GS (1971) Partial purification and some properties of a lipase from Corynebacterium acnes. Biochim Biophys Acta 242:381–394

    CrossRef  CAS  PubMed  Google Scholar 

  • Hausmann S, Jaeger K-E (2010) Lypolytic enzymes from bacteria. In: Timmis K (ed) Handbook of hydrocarbon and lipid microbiology, vol 77. Springer, Berlin/Heidelberg, pp 1099–1126

    CrossRef  Google Scholar 

  • Heikinheimo P, Goldman A, Jeffries C, Ollis DL (1999) Of barn owls and bankers: a lush variety of alpha/beta hydrolases. Structure 7:141–146

    CrossRef  Google Scholar 

  • Hemila H, Koivula TT, Palva I (1994) Hormone-sensitive lipase is closely related to several bacterial proteins, and distantly related to acetylcholinesterase and lipoprotein lipase: identification of a superfamily of esterases and lipases. Biochim Biophys Acta 1210:249–253

    CrossRef  CAS  PubMed  Google Scholar 

  • Henderson IR, Navarro-Garcia F, Nataro JP (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6:370–378

    CrossRef  CAS  PubMed  Google Scholar 

  • Higaki S, Morohashi M (2003) Propionibacterium acnes lipase in seborrheic dermatitis and other skin diseases and Unsei. Drugs Exp Clin Res 29:157–159

    CAS  PubMed  Google Scholar 

  • Hobson AH, Buckley CM, Aamand JL, Jorgensen ST, Diderichsen B, McConnell DJ (1993) Activation of a bacterial lipase by its chaperone. Proc Natl Acad Sci USA 90:5682–5686

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Holmstrom C, James S, Neilan BA, White DC, Kjelleberg S (1998) Pseudoalteromonas tunicata sp. nov., a bacterium that produces antifouling agents. Int J Syst Bacteriol 48:1205–1212

    CrossRef  CAS  PubMed  Google Scholar 

  • Hong KH, Jang WH, Choi KD, Yoo OJ (1991) Characterization of Pseudomonas fluorescens carboxylesterase: cloning and expression of the esterase gene in Escherichia coli. Agric Biol Chem 55:2839–2845

    CAS  PubMed  Google Scholar 

  • Ihara F, Okamoto I, Akao K, Nihira T, Yamada Y (1995) Lipase modulator protein (LimL) of Pseudomonas sp. strain 109. J Bacteriol 177:1254–1258

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Imamura S, Kitaura S (2000) Purification and characterization of a monoacylglycerol lipase from the moderately thermophilic Bacillus sp. H-257. J Biochem 127:419–425

    CrossRef  CAS  PubMed  Google Scholar 

  • Ingham E, Holland KT, Gowland G, Cunliffe WJ (1981) Partial purification and characterization of lipase (EC 3113) from Propionibacterium acnes. J Gen Microbiol 124:393–401

    CAS  PubMed  Google Scholar 

  • Jaeger K-E, Reetz MT (1998) Microbial lipases form versatile tools for biotechnology. Trends Biotechnol 16:396–403

    CrossRef  CAS  PubMed  Google Scholar 

  • Jaeger KE, Ransac S, Koch HB, Ferrato F, Dijkstra BW (1993) Topological characterization and modeling of the 3D structure of lipase from Pseudomonas aeruginosa. FEBS Lett 332:143–149

    CrossRef  CAS  PubMed  Google Scholar 

  • Jaeger K-E, Ransac S, Dijkstra BW, Colson C, van Heuvel M, Misset O (1994) Bacterial lipases. FEMS Microbiol Rev 15:29–63

    CrossRef  CAS  PubMed  Google Scholar 

  • Jaeger KE, Dijkstra BW, Reetz MT (1999) Bacterial biocatalysts: molecular biology, three-dimensional structures, and biotechnological applications of lipases. Annu Rev Microbiol 53:315–351

    CrossRef  CAS  PubMed  Google Scholar 

  • Jeong H, Yim JH, Lee C, Choi SH, Park YK, Yoon SH, Hur CG, Kang HY, Kim D, Lee HH, Park KH, Park SH, Park HS, Lee HK, Oh TK, Kim JF (2005) Genomic blueprint of Hahella chejuensis, a marine microbe producing an algicidal agent. Nucleic Acids Res 33:7066–7073

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Jørgensen S, Skov KW, Diderichsen B (1991) Cloning, sequence, and expression of a lipase gene from Pseudomonas cepacia: lipase production in heterologous hosts requires two Pseudomonas genes. J Bacteriol 173:559–567

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Jürgens D, Huser H (1981) Large-scale purification of staphylococcal lipase by hydrophobic interaction chromatography. J Chromatogr A 216:295–301

    CrossRef  Google Scholar 

  • Kashima Y, Nakajima Y, Nakano T, Tayama K, Koizumi Y, Udaka S, Yanagida F (1999) Cloning and characterization of ethanol-regulated esterase genes in Acetobacter pasteurianus. J Biosci Bioeng 87:19–27

    CrossRef  CAS  PubMed  Google Scholar 

  • Kim YS, Lee HB, Choi KD, Park S, Yoo OJ (1994) Cloning of Pseudomonas fluorescens carboxylesterase gene and characterization of its product expressed in Escherichia coli. Biosci Biotechnol Biochem 58:111–116

    CrossRef  CAS  PubMed  Google Scholar 

  • Kim KK, Song HK, Shin DH, Hwang KY, Choe S, Yoo OJ, Suh SW (1997) Crystal structure of carboxylesterase from Pseudomonas fluorescens, an alpha/beta hydrolase with broad substrate specificity. Structure 5:1571–1584

    CrossRef  CAS  PubMed  Google Scholar 

  • Kim HK, Park SY, Lee JK, Oh TK (1998) Gene cloning and characterization of thermostable lipase from Bacillus stearothermophilus L1. Biosci Biotechnol Biochem 62:66–71

    CrossRef  CAS  PubMed  Google Scholar 

  • Kim HK, Choi HJ, Kim MH, Sohn CB, Oh TK (2002) Expression and characterization of Ca2+-independent lipase from Bacillus pumilus B26. Biochim Biophys Acta 1583:205–212

    CrossRef  CAS  PubMed  Google Scholar 

  • Kim YJ, Choi GS, Kim SB, Yoon GS, Kim YS, Ryu YW (2006) Screening and characterization of a novel esterase from a metagenomic library. Protein Expr Purif 45:315–323

    CrossRef  CAS  PubMed  Google Scholar 

  • Kim EY, Oh KH, Lee MH, Kang CH, Oh TK, Yoon JH (2009) Novel cold-adapted alkaline lipase from an intertidal flat metagenome and proposal for a new family of bacterial lipases. Appl Environ Microbiol 75:257–260

    CrossRef  CAS  PubMed  Google Scholar 

  • Kitaura S, Suzuki K, Imamura S (2001) Monoacylglycerol lipase from moderately thermophilic Bacillus sp. strain H-257: molecular cloning, sequencing, and expression in Escherichia coli of the gene. J Biochem 129:397–402

    CrossRef  CAS  PubMed  Google Scholar 

  • Kleeberg I, Welzel K, Vandenheuvel J, Muller RJ, Deckwer WD (2005) Characterization of a new extracellular hydrolase from Thermobifida fusca degrading aliphatic-aromatic copolyesters. Biomacromolecules 6:262–270

    CrossRef  CAS  PubMed  Google Scholar 

  • Kok RG, van Thor JJ, Nugteren-Roodzant IM, Vosman B, Hellingwerf KJ (1995) Characterization of lipase-deficient mutants of Acinetobacter calcoaceticus BD413: identification of a periplasmic lipase chaperone essential for the production of extracellular lipase. J Bacteriol 177:3295–3307

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Koster M, Bitter W, Tommassen J (2000) Protein secretion mechanisms in Gram-negative bacteria. Int J Med Microbiol 290:325–331

    CrossRef  CAS  PubMed  Google Scholar 

  • Kwon HJ, Haruki M, Morikawa M, Omori K, Kanaya S (2002) Role of repetitive nine-residue sequence motifs in secretion, enzymatic activity, and protein conformation of a family I3 lipase. J Biosci Bioeng 93:157–164

    CrossRef  CAS  PubMed  Google Scholar 

  • Lee D, Koh Y, Kim K, Kim B, Choi H, Kim D, Suhartono MT, Pyun Y (1999) Isolation and characterization of a thermophilic lipase from Bacillus thermoleovorans ID-1. FEMS Microbiol Lett 179:393–400

    CrossRef  CAS  PubMed  Google Scholar 

  • Lee MH, Lee CH, Oh TK, Song JK, Yoon JH (2006) Isolation and characterization of a novel lipase from a metagenomic library of tidal flat sediments: evidence for a new family of bacterial lipases. Appl Environ Microbiol 72:7406–7409

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Lescic Asler I, Ivic N, Kovacic F, Schell S, Knorr J, Krauss U, Wilhelm S, Kojic-Prodic B, Jaeger K-E (2010) Probing enzyme promiscuity of SGNH hydrolases. Chembiochem 11:2158–2167

    CrossRef  PubMed  CAS  Google Scholar 

  • Lesuisse E, Schanck K, Colson C (1993) Purification and preliminary characterization of the extracellular lipase of Bacillus subtilis 168, an extremely basic pH-tolerant enzyme. Eur J Biochem 216:155–160

    CrossRef  CAS  PubMed  Google Scholar 

  • Levisson M, van der Oost J, Kengen SW (2007) Characterization and structural modeling of a new type of thermostable esterase from Thermotoga maritima. FEBS J 274:2832–2842

    CrossRef  CAS  PubMed  Google Scholar 

  • Li M, Yang L-R, Xu G, Wu J-P (2016) Cloning and characterization of a novel lipase from Stenotrophomonas maltophilia GS11: the first member of a new bacterial lipase family XVI. J Biotechnol 228:30–36

    CrossRef  CAS  PubMed  Google Scholar 

  • Liebeton K, Zacharias A, Jaeger K-E (2001) Disulfide bond in Pseudomonas aeruginosa lipase stabilizes the structure but is not required for interaction with its foldase. J Bacteriol 183:597–603

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Lilie H, Haehnel W, Rudolph R, Baumann U (2000) Folding of a synthetic parallel beta-roll protein. FEBS Lett 470:173–177

    CrossRef  CAS  PubMed  Google Scholar 

  • Liu P, Wang YF, Ewis HE, Abdelal AT, Lu CD, Harrison RW, Weber IT (2004) Covalent reaction intermediate revealed in crystal structure of the Geobacillus stearothermophilus carboxylesterase Est30. J Mol Biol 342:551–561

    CrossRef  CAS  PubMed  Google Scholar 

  • 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

    CrossRef  CAS  PubMed  Google Scholar 

  • Loveless BJ, Saier MH (1997) A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol Membr Biol 14:113–123

    CrossRef  CAS  PubMed  Google Scholar 

  • Ma Q, Zhai Y, Schneider JC, Ramseier TM, Saier MH (2003) Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens. Biochim Biophys Acta 1611:223–233

    CrossRef  CAS  PubMed  Google Scholar 

  • Manco G, Febbraio F, Adinolfi E, Rossi M (1999) Homology modeling and active-site residues probing of the thermophilic Alicyclobacillus acidocaldarius esterase 2. Protein Sci 8:1789–1796

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Maqbool QA, Johri S, Verma L, Riyaz-ul-Hassan S, Verma V, Koul S, Taneja SC, Parshad R, Qazi GN (2002) Purification and characterization of a novel enantioselective hydrolase from Bacillus subtilis. Biotechnol Appl Biochem 36:227–234

    CrossRef  CAS  PubMed  Google Scholar 

  • Maqbool QU, Johri S, Rasool S, Riyaz-ul-Hassan S, Verma V, Nargotra A, Koul S, Qazi GN (2006) Molecular cloning of carboxylesterase gene and biochemical characterization of encoded protein from Bacillus subtilis (RRL BB1). J Biotechnol 125:1–10

    CrossRef  CAS  PubMed  Google Scholar 

  • McKay DB, Jennings MP, Godfrey EA, MacRae IC, Rogers PJ, Beacham IR (1992) Molecular analysis of an esterase-encoding gene from a lipolytic psychrotrophic pseudomonad. J Gen Microbiol 138:701–708

    CrossRef  CAS  PubMed  Google Scholar 

  • Meier R, Drepper T, Svensson V, Jaeger K-E, Baumann U (2007) A calcium-gated lid and a large beta-roll sandwich are revealed by the crystal structure of extracellular lipase from Serratia marcescens. J Biol Chem 282:31477–31483

    CrossRef  CAS  PubMed  Google Scholar 

  • Methe BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang X, Moult J, Madupu R, Nelson WC, Dodson RJ, Brinkac LM, Daugherty SC, Durkin AS, DeBoy RT, Kolonay JF, Sullivan SA, Zhou L, Davidsen TM, Wu M, Huston AL, Lewis M, Weaver B, Weidman JF, Khouri H, Utterback TR, Feldblyum TV, Fraser CM (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci USA 102:10913–10918

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Minh BQ, Nguyen MA, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Miskin JE, Farrell AM, Cunliffe WJ, Holland KT (1997) Propionibacterium acnes, a resident of lipid-rich human skin, produces a 33 kDa extracellular lipase encoded by gehA. Microbiology 143:1745–1755

    CrossRef  CAS  PubMed  Google Scholar 

  • Missiakas D, Raina S (1997) Protein folding in the bacterial periplasm. J Bacteriol 179:2465–2471

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Mølgaard A (2002) Rhamnogalacturonan acetylesterase, a member of the SGNH-hydrolase family. In: Voragen F, Schols H, Visser RGF (eds) Advances in pectin and pectinase research. Kluwer, Dordrecht, pp 299–313

    Google Scholar 

  • Mølgaard A, Kauppinen S, Larsen S (2000) Rhamnogalacturonan acetylesterase elucidates the structure and function of a new family of hydrolases. Structure 8:373–383

    CrossRef  PubMed  Google Scholar 

  • Nardini M, Lang DA, Liebeton K, Jaeger K-E, Dijkstra BW (2000) Crystal structure of Pseudomonas aeruginosa lipase in the open conformation. The prototype for family I1 of bacterial lipases. J Biol Chem 275:31219–31225

    CrossRef  CAS  PubMed  Google Scholar 

  • Nikoleit K, Rosenstein R, Verheij HM, Gotz F (1995) Comparative biochemical and molecular analysis of the Staphylococcus hyicus, Staphylococcus aureus and a hybrid lipase. Indication for a C-terminal phospholipase domain. Eur J Biochem 228:732–738

    CrossRef  CAS  PubMed  Google Scholar 

  • Nishizawa M, Shimizu M, Ohkawa H, Kanaoka M (1995) Stereoselective production of (+)-trans-chrysanthemic acid by a microbial esterase: cloning, nucleotide sequence, and overexpression of the esterase gene of Arthrobacter globiformis in Escherichia coli. Appl Environ Microbiol 61:3208–3215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nthangeni MB, Patterton H, van Tonder A, Vergeer WP, Litthauer D (2001) Over-expression and properties of a purified recombinant Bacillus licheniformis lipase: a comparative report on Bacillus lipases. Enzyme Microb Technol 28:705–712

    CrossRef  CAS  PubMed  Google Scholar 

  • Nthangeni MB, Ramagoma F, Tlou MG, Litthauer D (2005) Development of a versatile cassette for directional genome walking using cassette ligation-mediated PCR and its application in the cloning of complete lipolytic genes from Bacillus species. J Microbiol Methods 61:225–234

    CrossRef  CAS  PubMed  Google Scholar 

  • Ogierman MA, Fallarino A, Riess T, Williams SG, Attridge SR, Manning PA (1997) Characterization of the Vibrio cholerae El Tor lipase operon lipAB and a protease gene downstream of the hly region. J Bacteriol 179:7072–7080

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogino H, Mimitsuka T, Muto T, Matsumura M, Yasuda M, Ishimi K, Ishikawa H (2004) Cloning, expression, and characterization of a lipolytic enzyme gene (lip8) from Pseudomonas aeruginosa LST-03. J Mol Microbiol Biotechnol 7:212–223

    CrossRef  CAS  PubMed  Google Scholar 

  • Ollis DL, Cheah E, Cygler M, Dijkstra B, Frolow F, Franken SM, Harel M, Remington SJ, Silman I, Schrag J et al (1992) The alpha/beta hydrolase fold. Protein Eng 5:197–211

    CrossRef  CAS  PubMed  Google Scholar 

  • Oomen CJ, van Ulsen P, van Gelder P, Feijen M, Tommassen J, Gros P (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J 23:1257–1266

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Parapouli M, Foukis A, Stergiou P-Y, Koukouritaki M, Magklaras P, Gkini OA, Papamichael EM, Afendra A-S, Hatziloukas E (2018) Correction to: molecular, biochemical and kinetic analysis of a novel, thermostable lipase (LipSm) from Stenotrophomonas maltophilia Psi-1, the first member of a new bacterial lipase family (XVIII). J Biol Res 25:4

    Google Scholar 

  • Pauwels K, Loris R, Vandenbussche G, Ruysschaert JM, Wyns L, Van Gelder P (2005) Crystallization and crystal manipulation of a steric chaperone in complex with its lipase substrate. Acta Crystallogr Sect F Struct Biol Cryst Commun 61:791–795

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Pauwels K, Lustig A, Wyns L, Tommassen J, Savvides SN, Van Gelder P (2006) Structure of a membrane-based steric chaperone in complex with its lipase substrate. Nat Struct Mol Biol 13:374–375

    CrossRef  CAS  PubMed  Google Scholar 

  • Pauwels K, Van Molle I, Tommassen J, Van Gelder P (2007) Chaperoning anfinsen: the steric foldases. Mol Microbiol 64:917–922

    CrossRef  CAS  PubMed  Google Scholar 

  • Perez C, Juarez K, Garcia-Castells E, Soberon G, Servin-Gonzalez L (1993) Cloning, characterization, and expression in Streptomyces lividans 66 of an extracellular lipase-encoding gene from Streptomyces sp. M11. Gene 123:109–114

    CrossRef  CAS  PubMed  Google Scholar 

  • Pesaresi A, Lamba D (2005) Crystallization, X-ray diffraction analysis and phasing of carboxylesterase PA3859 from Pseudomonas aeruginosa. Biochim Biophys Acta 1752:197–201

    CrossRef  CAS  PubMed  Google Scholar 

  • Pesaresi A, Devescovi G, Lamba D, Venturi V, Degrassi G (2005) Isolation, characterization, and heterologous expression of a carboxylesterase of Pseudomonas aeruginosa PAO1. Curr Microbiol 50:102–109

    CrossRef  CAS  PubMed  Google Scholar 

  • Petersen EI, Valinger G, Solkner B, Stubenrauch G, Schwab H (2001) A novel esterase from Burkholderia gladioli which shows high deacetylation activity on cephalosporins is related to beta-lactamases and DD-peptidases. J Biotechnol 89:11–25

    CrossRef  CAS  PubMed  Google Scholar 

  • Pharkya P, Nikolaev EV, Maranas CD (2003) Review of the BRENDA database. Metab Eng 5:71–73

    CrossRef  CAS  PubMed  Google Scholar 

  • Pohlenz HD, Boidol W, Schuttke I, Streber WR (1992) Purification and properties of an Arthrobacter oxydans P52 carbamate hydrolase specific for the herbicide phenmedipham and nucleotide sequence of the corresponding gene. J Bacteriol 174:6600–6607

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Pratt RF, Govardhan CP (1984) Beta-lactamase-catalyzed hydrolysis of acyclic depsipeptides and acyl transfer to specific amino acid acceptors. Proc Natl Acad Sci USA 81:1302–1306

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Prim N, Bofill C, Pastor FI, Diaz P (2006) Esterase EstA6 from Pseudomonas sp. CR-611 is a novel member in the utmost conserved cluster of family VI bacterial lipolytic enzymes. Biochimie 88:859–867

    CrossRef  CAS  PubMed  Google Scholar 

  • Pugsley AP (1992) Translocation of a folded protein across the outer membrane in Escherichia coli. Proc Natl Acad Sci USA 89:12058–12062

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao L, Xue Y, Zhou C, Tao J, Li G, Lu JR, Ma Y (2011) A thermostable esterase from Thermoanaerobacter tengcongensis opening up a new family of bacterial lipolytic enzymes. Biochim Biophys Acta 1814:1695–1702

    CrossRef  CAS  PubMed  Google Scholar 

  • Rao L, Xue Y, Zheng Y, Lu JR, Ma Y (2013) A novel alkaliphilic bacillus esterase belongs to the 13th bacterial lipolytic enzyme family. PLoS One 8:e60645

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Rashamuse KJ, Burton SG, Stafford WH, Cowan DA (2007) Molecular characterization of a novel family VIII esterase from Burkholderia multivorans UWC10. J Mol Microbiol Biotechnol 13:181–188

    CrossRef  CAS  PubMed  Google Scholar 

  • Rauwerdink A, Kazlauskas RJ (2015) How the same core catalytic machinery catalyzes 17 different reactions: the serine-histidine-aspartate catalytic triad of α/β-hydrolase fold enzymes. ACS Catal 5:6153–6176

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Rengachari S, Bezerra GA, Riegler-Berket L, Gruber CC, Sturm C, Taschler U, Boeszoermenyi A, Dreveny I, Zimmermann R, Gruber K, Oberer M (2012) The structure of monoacylglycerol lipase from Bacillus sp. H257 reveals unexpected conservation of the cap architecture between bacterial and human enzymes. Biochim Biophys Acta 1821:1012–1021

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Rose T, Sebo P, Bellalou J, Ladant D (1995) Interaction of calcium with Bordetella pertussis adenylate cyclase toxin: characterization of multiple calcium-binding sites and calcium-induced conformational changes. J Biol Chem 270:26370–26376

    CrossRef  CAS  PubMed  Google Scholar 

  • Rosenau F, Jaeger K-E (2000) Bacterial lipases from Pseudomonas: regulation of gene expression and mechanisms of secretion. Biochimie 82:1023–1032

    CrossRef  CAS  PubMed  Google Scholar 

  • Rosenau F, Tommassen J, Jaeger K-E (2004) Lipase-specific foldases. Chembiochem 5:152–161

    CrossRef  CAS  PubMed  Google Scholar 

  • Rosenstein R, Götz F (2000) Staphylococcal lipases: biochemical and molecular characterization. Biochimie 82:1005–1014

    CrossRef  CAS  PubMed  Google Scholar 

  • Rua ML, Schmidt-Dannert C, Wahl S, Sprauer A, Schmid RD (1997) Thermoalkalophilic lipase of Bacillus thermocatenulatus large-scale production, purification and properties: aggregation behaviour and its effect on activity. J Biotechnol 56:89–102

    CrossRef  CAS  PubMed  Google Scholar 

  • Ruiz C, Falcocchio S, Pastor FI, Saso L, Diaz P (2007) Helicobacter pylori EstV: identification, cloning, and characterization of the first lipase isolated from an epsilon-proteobacterium. Appl Environ Microbiol 73:2423–2431

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai Y, Ishikawa J, Fukasaka S, Yurimoto H, Mitsui R, Yanase H, Kato N (1999) A new carboxylesterase from Brevibacterium linens IFO 12171 responsible for the conversion of 1,4-butanediol diacrylate to 4-hydroxybutyl acrylate: purification, characterization, gene cloning, and gene expression in Escherichia coli. Biosci Biotechnol Biochem 63:688–697

    CrossRef  CAS  PubMed  Google Scholar 

  • Sakinc T, Woznowski M, Ebsen M, Gatermann SG (2005) The surface-associated protein of Staphylococcus saprophyticus is a lipase. Infect Immun 73:6419–6428

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Samoylova YV, Sorokina KN, Romanenko MV, Parmon VN (2018) Cloning, expression and characterization of the esterase estUT1 from Ureibacillus thermosphaericus which belongs to a new lipase family XVIII. Extremophiles 22:271–285

    CrossRef  CAS  PubMed  Google Scholar 

  • Sandkvist M (2001) Biology of type II secretion. Mol Microbiol 40:271–283

    CrossRef  CAS  PubMed  Google Scholar 

  • Sarda L, Desnuelle P (1958) Actions of pancreatic lipase on esters in emulsions. Biochim Biophys Acta 30:513–521

    CrossRef  CAS  PubMed  Google Scholar 

  • Sayari A, Agrebi N, Jaoua S, Gargouri Y (2001) Biochemical and molecular characterization of Staphylococcus simulans lipase. Biochimie 83:863–871

    CrossRef  CAS  PubMed  Google Scholar 

  • Schomburg I, Chang A, Ebeling C, Gremse M, Heldt C, Huhn G, Schomburg D (2004) BRENDA, the enzyme database: updates and major new developments. Nucleic Acids Res 32:431–433

    CrossRef  CAS  Google Scholar 

  • Schrag JD, Li YG, Wu S, Cygler M (1991) Ser-His-Glu triad forms the catalytic site of the lipase from Geotrichum candidum. Nature 351:761–764

    CrossRef  CAS  PubMed  Google Scholar 

  • Semeriva M, Chapus C, Bouvier-Lapierre C, Desnuelle P (1974) On the transient formation of an acetyl enzyme intermediate during the hydrolysis of p-nitrophenyl acetate by pancreatic lipase. Biochem Biophys Res Commun 58:808–813

    CrossRef  CAS  PubMed  Google Scholar 

  • Servin-Gonzalez L, Castro C, Perez C, Rubio M, Valdez F (1997) BldA-dependent expression of the Streptomyces exfoliatus M11 lipase gene (lipA) is mediated by the product of a contiguous gene, lipR, encoding a putative transcriptional activator. J Bacteriol 179:7816–7826

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Shah DS, Russell RR (2004) A novel glucan-binding protein with lipase activity from the oral pathogen Streptococcus mutans. Microbiology 150:1947–1956

    CrossRef  CAS  PubMed  Google Scholar 

  • Shibata H, Kato H, Oda J (1998) Random mutagenesis on the Pseudomonas lipase activator protein, LipB: exploring amino acid residues required for its function. Protein Eng 11:467–472

    CrossRef  CAS  PubMed  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Simons JW, van Kampen MD, Riel S, Gotz F, Egmond MR, Verheij HM (1998) Cloning, purification and characterisation of the lipase from Staphylococcus epidermidis – comparison of the substrate selectivity with those of other microbial lipases. Eur J Biochem 253:675–683

    CrossRef  CAS  PubMed  Google Scholar 

  • Simons JW, van Kampen MD, Ubarretxena-Belandia I, Cox RC, Alves dos Santos CM, Egmond MR, Verheij HM (1999) Identification of a calcium binding site in Staphylococcus hyicus lipase: generation of calcium-independent variants. Biochemistry 38:2–10

    CrossRef  CAS  PubMed  Google Scholar 

  • Skjøt M, De Maria L, Chatterjee R, Svendsen A, Patkar SA, Ostergaard PR, Brask J (2009) Understanding the plasticity of the α/β hydrolase fold: lid swapping on the Candida antarctica lipase B results in chimeras with interesting biocatalytic properties. Chembiochem 10:520–527

    CrossRef  PubMed  CAS  Google Scholar 

  • Sommer P, Bormann C, Gotz F (1997) Genetic and biochemical characterization of a new extracellular lipase from Streptomyces cinnamomeus. Appl Environ Microbiol 63:3553–3560

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamm LK, Arora A, Kleinschmidt JH (2001) Structure and assembly of beta-barrel membrane proteins. J Biol Chem 276:32399–32402

    CrossRef  CAS  PubMed  Google Scholar 

  • Thomassin JL, Santos Moreno J, Guilvout I, Tran Van Nhieu G, Francetic O (2017) The trans-envelope architecture and function of the type 2 secretion system: new insights raising new questions. Mol Microbiol 105:211–226

    CrossRef  CAS  PubMed  Google Scholar 

  • Tiesinga JJ, van Pouderoyen G, Nardini M, Ransac S, Dijkstra BW (2007) Structural basis of phospholipase activity of Staphylococcus hyicus lipase. J Mol Biol 371:447–456

    CrossRef  CAS  PubMed  Google Scholar 

  • Tommassen J, Filloux A, Bally M, Murgier M, Lazdunski A (1992) Protein secretion in Pseudomonas aeruginosa. FEMS Microbiol Rev 9:73–90

    CrossRef  CAS  PubMed  Google Scholar 

  • Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:232–235

    CrossRef  CAS  Google Scholar 

  • Tsirigotaki A, De Geyter J, Sostaric N, Economou A, Karamanou S (2017) Protein export through the bacterial Sec pathway. Nat Rev Microbiol 15:21–36

    CrossRef  CAS  PubMed  Google Scholar 

  • Tyndall JD, Sinchaikul S, Fothergill-Gilmore LA, Taylor P, Walkinshaw MD (2002) Crystal structure of a thermostable lipase from Bacillus stearothermophilus P1. J Mol Biol 323:859–869

    CrossRef  CAS  PubMed  Google Scholar 

  • Tyski S, Hryniewicz W, Jeljaszewicz J (1983) Purification and some properties of the staphylococcal extracellular lipase. Biochim Biophys Acta 749:312–317

    CrossRef  CAS  PubMed  Google Scholar 

  • Uchida H, Shigeno-Akutsu Y, Nomura N, Nakahara T, Nakajima-Kambe T (2002) Cloning and sequence analysis of poly(tetramethylene succinate) depolymerase from Acidovorax delafieldii strain BS-3. J Biosci Bioeng 93:245–247

    CrossRef  CAS  PubMed  Google Scholar 

  • Upton C, Buckley JT (1995) A new family of lipolytic enzymes? Trends Biochem Sci 20:178–179

    CrossRef  CAS  PubMed  Google Scholar 

  • van Oort MG, Deveer AM, Dijkman R, Tjeenk ML, Verheij HM, de Haas GH, Wenzig E, Gotz F (1989) Purification and substrate specificity of Staphylococcus hyicus lipase. Biochemistry 28:9278–9285

    CrossRef  PubMed  Google Scholar 

  • van Pouderoyen G, Eggert T, Jaeger KE, Dijkstra BW (2001) The crystal structure of Bacillus subtilis lipase: a minimal alpha/beta hydrolase fold enzyme. J Mol Biol 309:215–226

    CrossRef  CAS  PubMed  Google Scholar 

  • van Tilbeurgh H, Egloff MP, Martinez C, Rugani N, Verger R, Cambillau C (1993) Interfacial activation of the lipase-procolipase complex by mixed micelles revealed by X-ray crystallography. Nature 362:814–820

    CrossRef  PubMed  Google Scholar 

  • Veerassamy S, Smith A, Tillier ER (2003) A transition probability model for amino acid substitutions from blocks. J Comput Biol 10:997–1010

    CrossRef  CAS  PubMed  Google Scholar 

  • Verger R (1997) Interfacial activation of lipases: facts and artifacts. Trends Biotechnol 15:32–38

    CrossRef  CAS  Google Scholar 

  • Wagner UG, Petersen EI, Schwab H, Kratky C (2002) EstB from Burkholderia gladioli: a novel esterase with a beta-lactamase fold reveals steric factors to discriminate between esterolytic and beta-lactam cleaving activity. Protein Sci 11:467–478

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Wakadkar S, Hermawan S, Jendrossek D, Papageorgiou AC (2010) The structure of PhaZ7 at atomic (12 Å) resolution reveals details of the active site and suggests a substrate-binding mode. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:648–654

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Shen WJ, Patel S, Harada K, Kraemer FB (2005) Mutational analysis of the “regulatory module” of hormone-sensitive lipase. Biochemistry 44:1953–1959

    CrossRef  CAS  PubMed  Google Scholar 

  • Wei Y, Swenson L, Castro C, Derewenda U, Minor W, Arai H, Aoki J, Inoue K, Servin-Gonzalez L, Derewenda ZS (1998) Structure of a microbial homologue of mammalian platelet-activating factor acetylhydrolases: Streptomyces exfoliatus lipase at 1.9 Å resolution. Structure 6:511–519

    CrossRef  CAS  PubMed  Google Scholar 

  • Wei Y, Contreras JA, Sheffield P, Osterlund T, Derewenda U, Kneusel RE, Matern U, Holm C, Derewenda ZS (1999) Crystal structure of brefeldin A esterase, a bacterial homolog of the mammalian hormone-sensitive lipase. Nat Struct Biol 6:340–345

    CrossRef  CAS  PubMed  Google Scholar 

  • Welch RA (2001) RTX toxin structure and function: a story of numerous anomalies and few analogies in toxin biology. Curr Top Microbiol Immunol 257:85–111

    CAS  PubMed  Google Scholar 

  • Wilhelm S, Tommassen J, Jaeger K-E (1999) A novel lipolytic enzyme located in the outer membrane of Pseudomonas aeruginosa. J Bacteriol 181:6977–6986

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wodak SJ, Janin J (2002) Structural basis of macromolecular recognition. Adv Protein Chem 61:9–73

    CrossRef  PubMed  Google Scholar 

  • Wohlfarth S, Hoesche C, Strunk C, Winkler UK (1992) Molecular genetics of the extracellular lipase of Pseudomonas aeruginosa PAO1. J Gen Microbiol 138:1325–1335

    CrossRef  CAS  PubMed  Google Scholar 

  • Wu JP, Li M, Zhou Y, Yang LR, Xu G (2015) Introducing a salt bridge into the lipase of Stenotrophomonas maltophilia results in a very large increase in thermal stability. Biotechnol Lett 37:403–407

    CrossRef  CAS  PubMed  Google Scholar 

  • Yuan D, Lan D, Xin R, Yang B, Wang Y (2014) Biochemical properties of a new cold-active mono- and diacylglycerol lipase from marine member Janibacter sp. strain HTCC2649. Int J Mol Sci 15:10554–10566

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarafeta D, Szabo Z, Moschidi D, Phan H, Chrysina ED, Peng X, Ingham CJ, Kolisis FN, Skretas G (2016) EstDZ3: a new esterolytic enzyme exhibiting remarkable thermostability. Front Microbiol 7:1779

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Larsen NA, Basran A, Bruce NC, Wilson IA (2003) Observation of an arsenic adduct in an acetyl esterase crystal structure. J Biol Chem 278:2008–2014

    CrossRef  CAS  PubMed  Google Scholar 

  • Zock J, Cantwell C, Swartling J, Hodges R, Pohl T, Sutton K, Rosteck P, McGilvray D, Queener S (1994) The Bacillus subtilis pnbA gene encoding p-nitrobenzyl esterase: cloning, sequence and high-level expression in Escherichia coli. Gene 151:37–43

    CrossRef  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

NB is a recipient of a PhD grant from the Manchot Graduate School “Molecules of Infection” at Heinrich Heine University Düsseldorf, Germany.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karl-Erich Jaeger .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and Permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this entry

Verify currency and authenticity via CrossMark

Cite this entry

Kovacic, F., Babic, N., Krauss, U., Jaeger, KE. (2019). Classification of Lipolytic Enzymes from Bacteria. In: Rojo, F. (eds) Aerobic Utilization of Hydrocarbons, Oils and Lipids. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-39782-5_39-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-39782-5_39-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-39782-5

  • Online ISBN: 978-3-319-39782-5

  • eBook Packages: Springer Reference Biomedicine & Life SciencesReference Module Biomedical and Life Sciences