Abstract
Since the beginning of written history, diverse texts have reported the use of enzymatic preparations in food processing and have described the medicinal properties of crude and fractionated venoms to treat various diseases and injuries. With the biochemical characterization of enzymes from distinct sources and bioactive polypeptides from animal venoms, the last sixty years have testified the advent of industrial enzymology and protein therapeutics, which are currently applicable in a wide variety of industrial processes, household products, and pharmaceuticals. Bioprospecting of novel biocatalysts and bioactive peptides is propelled by their unsurpassed properties that are applicable for current and future green industrial processes, biotechnology, and biomedicine. The demand for both novel enzymes with desired characteristics and novel peptides that lead to drug development, has experienced a steady increase in response to the expanding global market for industrial enzymes and peptidebased drugs. Moreover, although largely unexplored, oceans and marine realms, with their unique ecosystems inhabited by a large variety of species, including a considerable number of venomous animals, are recognized as untapped reservoirs of molecules and macromolecules (enzymes and bioactive venom-derived peptides) that can potentially be converted into highly valuable biopharmaceutical products. In this review, we have focused on enzymes and animal venom (poly)peptides that are presently in biotechnological use, and considering the state of prospection of marine resources, on the discovery of useful industrial biocatalysts and drug leads with novel structures exhibiting selectivity and improved performance.
Keywords: Industrial enzymes, therapeutic polypeptides, therapeutic enzymes, therapeutic peptides, venom-derived peptides, biopharmaceuticals, peptide drug discovery, marine biotechnology, green technology.
Graphical Abstract
[1]
Lewis, C.A.; Wolfenden, R. Uroporphyrinogen decarboxylation as a benchmark for the catalytic proficiency of enzymes. Proc. Natl. Acad. Sci. USA, 2008, 105(45), 17328-17333.
[2]
Patel, R.N. Biocatalytic synthesis of chiral alcohols and amino acids for development of pharmaceuticals. Biomolecules, 2013, 3(4), 741-777.
[4]
Zhang, Z.J.; Pan, J.; Ma, B.D.; Xu, J.H. Efficient biocatalytic synthesis of chiral chemicals. Adv. Biochem. Eng. Biotechnol., 2016, 155, 55-106.
[5]
Rat’ko, A.A.; Stefan-van Staden, R.I. Determination of baclofen enantiomers in pharmaceutical formulations using maltodextrin-based enantioselective, potentiometric membrane electrodes. Farmaco, 2004, 59(12), 993-997.
[6]
Smith, S.W. Chiral toxicology: It’s the same thing...only different. Toxicol. Sci., 2009, 110(1), 4-30.
[7]
Nguyen, L.A.; He, H.; Pham-Huy, C. Chiral drugs: An overview. Int. J. Biomed. Sci., 2006, 2(2), 85-100.
[8]
Calcaterra, A.; D’Acquarica, I. The market of chiral drugs: Chiral switches versus de novo enantiomerically pure compounds. J. Pharm. Biomed. Anal., 2018, 147, 323-340.
[9]
Kisukuri, C.M.; Andrade, L.H. Production of chiral compounds using immobilized cells as a source of biocatalysts. Org. Biomol. Chem., 2015, 13(40), 10086-10107.
[10]
Piasecki, S.K.; Taylor, C.A.; Detelich, J.F.; Liu, J.; Zheng, J.; Komsoukaniants, A.; Siegel, D.R.; Keatinge-Clay, A.T. Employing modular polyketide synthase ketoreductases as biocatalysts in the preparative chemoenzymatic syntheses of diketide chiral building blocks. Chem. Biol., 2011, 18(10), 1331-1340.
[11]
Solomon, M.; Muro, S. Lysosomal enzyme replacement therapies: Historical development, clinical outcomes, and future perspectives. Adv. Drug Deliv. Rev., 2017, 118, 109-134.
[12]
Schoni, R. The use of snake venom-derived compounds for new functional diagnostic test kits in the field of haemostasis. Pathophysiol. Haemost. Thromb., 2005, 34(4-5), 234-240.
[13]
Ali Khan, A.; Alzohairy, M.A. Recent advances and applications of immobilized enzyme technologies: A review. Res. J. Biol. Sci., 2010, 5(8), 565-575.
[14]
Asanomi, Y.; Yamaguchi, H.; Miyazaki, M.; Maeda, H. Enzyme-immobilized microfluidic process reactors. Molecules, 2011, 16(7), 6041-6059.
[15]
Das, P.; Das, M.; Chinnadayyala, S.R.; Singha, I.M.; Goswami, P. Recent advances on developing 3rd generation enzyme electrode for biosensor applications. Biosens. Bioelectron., 2016, 79, 386-397.
[16]
Bilal, M.; Asgher, M.; Parra-Saldivar, R.; Hu, H.; Wang, W.; Zhang, X.; Iqbal, H.M.N. Immobilized ligninolytic enzymes: An innovative and environmental responsive technology to tackle dye-based industrial pollutants - A review. Sci. Total Environ., 2017, 576, 646-659.
[17]
DiCosimo, R.; McAuliffe, J.; Poulose, A.J.; Bohlmann, G. Industrial use of immobilized enzymes. Chem. Soc. Rev., 2013, 42(15), 6437-6474.
[18]
Perumal Samy, R.; Stiles, B.G.; Franco, O.L.; Sethi, G.; Lim, L.H.K. Animal venoms as antimicrobial agents. Biochem. Pharmacol., 2017, 134, 127-138.
[20]
Komives, C.F.; Sanchez, E.E.; Rathore, A.S.; White, B.; Balderrama, M.; Suntravat, M.; Cifelli, A.; Joshi, V. Opossum peptide that can neutralize rattlesnake venom is expressed in Escherichia coli. Biotechnol. Prog., 2017, 33(1), 81-86.
[21]
Stocker, K.; Barlow, G.H. The coagulant enzyme from Bothrops atrox venom (batroxobin). Methods Enzymol., 1976, 45, 214-223.
[22]
Takacs, Z.; Nathan, S. Animal Venoms in Medicine.Encyclopedia of Toxicology; Elsevier, 2014, pp. 252-259.
[23]
Radis-Baptista, G. Vipericidins, snake venom cathelicidin-related peptides, in the milieu of reptilian antimicrobial polypeptides., 2015.
[24]
Falcao, C.B.; de La Torre, B.G.; Perez-Peinado, C.; Barron, A.E.; Andreu, D.; Radis-Baptista, G. Vipericidins: A novel family of cathelicidin-related peptides from the venom gland of South American pit vipers. Amino Acids, 2014, 46(11), 2561-2571.
[25]
Bandeira, I.C.J.; Bandeira-Lima, D.; Mello, C.P.; Pereira, T.P.; De Menezes, R.; Sampaio, T.L.; Falcao, C.B.; Radis-Baptista, G.; Martins, A.M.C. Antichagasic effect of crotalicidin, a cathelicidin-like vipericidin, found in Crotalus durissus terrificus rattlesnake’s venom gland. Parasitology, 2018, 145(8), 1059-1064.
[27]
Vieira-Girao, P.R.N.; Falcao, C.B.; Rocha, I.; Lucena, H.M.R.; Costa, F.H.F.; Radis-Baptista, G. Antiviral activity of Ctn [15
-
34], A cathelicidin-derived eicosapeptide, against infectious myonecrosis virus in litopenaeus vannamei primary hemocyte cultures. Food Environ. Virol., 2017, 9(3), 277-286.
[28]
Perez-Peinado, C.; Dias, S.A.; Domingues, M.M.; Benfield, A.H.; Freire, J.M.; Radis-Baptista, G.; Gaspar, D.; Castanho, M.; Craik, D.J.; Henriques, S.T.; Veiga, A.S.; Andreu, D. Mechanisms of bacterial membrane permeabilization by crotalicidin (Ctn) and its fragment Ctn(15-34), antimicrobial peptides from rattlesnake venom. J. Biol. Chem., 2018, 293(5), 1536-1549.
[29]
Wang, L.; Chan, J.Y.; Rego, J.V.; Chong, C.M.; Ai, N.; Falcao, C.B.; Radis-Baptista, G.; Lee, S.M. Rhodamine B-conjugated encrypted vipericidin nonapeptide is a potent toxin to zebrafish and associated with in vitro cytotoxicity. Biochim. Biophys. Acta, 2015, 1850(6), 1253-1260.
[30]
Falcao, C.B.; Perez-Peinado, C.; de la Torre, B.G.; Mayol, X.; Zamora-Carreras, H.; Jimenez, M.A.; Radis-Baptista, G.; Andreu, D. Structural dissection of crotalicidin, a rattlesnake venom cathelicidin, retrieves a fragment with antimicrobial and antitumor activity. J. Med. Chem., 2015, 58(21), 8553-8563.
[31]
Deák, F.; Liu, X.; Khvotchev, M.; Li, G.; Kavalali, E.T.; Sugita, S.; Südhof, T.C. Alpha-latrotoxin stimulates a novel pathway of Ca2+-dependent synaptic exocytosis independent of the classical synaptic fusion machinery. J. Neurosci., 2009, 29(27), 8639-8648.
[32]
Vulfius, C.A.; Kasheverov, I.E.; Kryukova, E.V.; Spirova, E.N.; Shelukhina, I.V.; Starkov, V.G.; Andreeva, T.V.; Faure, G.; Zouridakis, M.; Tsetlin, V.I.; Utkin, Y.N. Pancreatic and snake venom presynaptically active phospholipases A2 inhibit nicotinic acetylcholine receptors. PLoS One, 2017, 12(10), e0186206.
[33]
Sanahuja, G.; Banakar, R.; Twyman, R.M.; Capell, T.; Christou, P. Bacillus thuringiensis: A century of research, development and commercial applications. Plant Biotechnol. J., 2011, 9(3), 283-300.
[34]
Bende, N.S.; Dziemborowicz, S.; Herzig, V.; Ramanujam, V.; Brown, G.W.; Bosmans, F.; Nicholson, G.M.; King, G.F.; Mobli, M. The insecticidal spider toxin SFI1 is a knottin peptide that blocks the pore of insect voltage-gated sodium channels via a large β-hairpin loop. FEBS J., 2015, 282(5), 904-920.
[35]
Windley, M.J.; Vetter, I.; Lewis, R.J.; Nicholson, G.M. Lethal effects of an insecticidal spider venom peptide involve positive allosteric modulation of insect nicotinic acetylcholine receptors. Neuropharmacology, 2017, 127, 224-242.
[36]
Fletcher, J.I.; Smith, R.; O’Donoghue, S.I.; Nilges, M.; Connor, M.; Howden, M.E.; Christie, M.J.; King, G.F. The structure of a novel insecticidal neurotoxin, omega-atracotoxin-HV1, from the venom of an Australian funnel web spider. Nat. Struct. Biol., 1997, 4(7), 559-566.
[37]
Herzig, V.; King, G.F. The cystine knot is responsible for the exceptional stability of the insecticidal spider toxin ω-hexatoxin-Hv1a. Toxins (Basel), 2015, 7(10), 4366-4380.
[38]
Nakasu, E.Y.T.; Williamson, S.M.; Edwards, M.G.; Fitches, E.C.; Gatehouse, J.A.; Wright, G.A.; Gatehouse, A.M.R. Novel biopesticide based on a spider venom peptide shows no adverse effects on honeybees. Proc. Biol. Sci., 1787, 2014(281), 20140619.
[42]
Research, B.C.C. Global Markets and Manufacturing Technologies
for Protein Drugs - BIO021E 2016.
[45]
Camargo, L.C.; Campos, G.A.A.; Galante, P.; Biolchi, A.M.; Gonçalves, J.C.; Lopes, K.S.; Mortari, M.R. Peptides isolated from animal venom as a platform for new therapeutics for the treatment of Alzheimer’s disease. Neuropeptides, 2018, 67, 79-86.
[46]
Chassagnon, I.R.; McCarthy, C.A.; Chin, Y.K.Y.; Pineda, S.S.; Keramidas, A.; Mobli, M.; Pham, V.; De Silva, T.M.; Lynch, J.W.; Widdop, R.E.; Rash, L.D.; King, G.F. Potent neuroprotection after stroke afforded by a double-knot spider-venom peptide that inhibits acid-sensing ion channel 1a. Proc. Natl. Acad. Sci. USA, 2017, 114(14), 3750-3755.
[47]
Chen, Y.C.; Ho, C.C.; Yi, C.H.; Liu, X.Z.; Cheng, T.T.; Lam, C.F. Exendin-4, a glucagon-like peptide-1 analogue accelerates healing of chronic gastric ulcer in diabetic rats. PLoS One, 2017, 12(11), e0187434.
[48]
Jimenez, R.; Ikonomopoulou, M.P.; Lopez, J.A.; Miles, J.J. Immune drug discovery from venoms. Toxicon, 2018, 141, 18-24.
[49]
Rady, I.; Siddiqui, I.A.; Rady, M.; Mukhtar, H. Melittin, a major peptide component of bee venom, and its conjugates in cancer therapy. Cancer Lett., 2017, 402, 16-31.
[50]
Robinson, S.D.; Safavi-Hemami, H. Venom peptides as pharmacological tools and therapeutics for diabetes. Neuropharmacology, 2017, 127, 79-86.
[51]
Wang, Y.; Li, X.; Yang, M.; Wu, C.; Zou, Z.; Tang, J.; Yang, X. Centipede venom peptide SsmTX-I with two intramolecular disulfide bonds shows analgesic activities in animal models. J. Pept. Sci., 2017, 23(5), 384-391.
[52]
Yoshida, S.; Hiraga, K.; Takehana, T.; Taniguchi, I.; Yamaji, H.; Maeda, Y.; Toyohara, K.; Miyamoto, K.; Kimura, Y.; Oda, K. A bacterium that degrades and assimilates poly(ethylene terephthalate). Science, 2016, 351(6278), 1196-1199.
[53]
Baldo, B.A. Enzymes approved for human therapy: indications, mechanisms and adverse effects. BioDrugs, 2015, 29(1), 31-55.
[54]
Mishra, M.; Arukha, A.P.; Patel, A.K.; Behera, N.; Mohanta, T.K.; Yadav, D. Multi-drug resistant coliform: Water sanitary standards and health hazards. Front. Pharmacol., 2018, 9, 311.
[55]
Berlin, A.; Maximenko, V.; Gilkes, N.; Saddler, J. Optimization of enzyme complexes for lignocellulose hydrolysis. Biotechnol. Bioeng., 2007, 97(2), 287-296.
[56]
de Souza, A.P.; Leite, D.C.C.; Pattathil, S.; Hahn, M.G.; Buckeridge, M.S. Composition and structure of sugarcane cell wall polysaccharides: Implications for second-generation bioethanol production. BioEnergy Res., 2013, 6(2), 564-579.
[57]
Hu, J.; Arantes, V.; Saddler, J.N. The enhancement of enzymatic hydrolysis of lignocellulosic substrates by the addition of accessory enzymes such as xylanase: Is it an additive or synergistic effect? Biotechnol. Biofuels, 2011, 4, 36.
[58]
Jeremic, D.; Goacher, R.E.; Yan, R.; Karunakaran, C.; Master, E.R. Direct and up-close views of plant cell walls show a leading role for lignin-modifying enzymes on ensuing xylanases. Biotechnol. Biofuels, 2014, 7(1), 496.
[59]
Himmel, M.E.; Ding, S.Y.; Johnson, D.K.; Adney, W.S.; Nimlos, M.R.; Brady, J.W.; Foust, T.D. Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science, 2007, 315(5813), 804-807.
[60]
McCann, M.C.; Carpita, N.C. Biomass recalcitrance: A multi-scale, multi-factor, and conversion-specific property. J. Exp. Bot., 2015, 66(14), 4109-4118.
[61]
Matsumoto, K.I.; Taguchi, S. Enzyme and metabolic engineering for the production of novel biopolymers: Crossover of biological and chemical processes. Curr. Opin. Biotechnol., 2013, 24(6), 1054-1060.
[62]
Tsuge, Y.; Kawaguchi, H.; Sasaki, K.; Kondo, A. Engineering cell factories for producing building block chemicals for bio-polymer synthesis. Microb. Cell Fact., 2016, 15, 19.
[63]
Wei, R.; Zimmermann, W. Microbial enzymes for the recycling of recalcitrant petroleum-based plastics: How far are we? Microb. Biotechnol., 2017, 10(6), 1308-1322.
[64]
Gasser, C.A.; Yu, L.; Svojitka, J.; Wintgens, T.; Ammann, E.M.; Shahgaldian, P.; Corvini, P.F.; Hommes, G. Advanced enzymatic elimination of phenolic contaminants in wastewater: A nano approach at field scale. Appl. Microbiol. Biotechnol., 2014, 98(7), 3305-3316.
[66]
Pollmann, K.; Kutschke, S.; Matys, S.; Kostudis, S.; Hopfe, S.; Raff, J. Novel biotechnological approaches for the recovery of metals from primary and secondary resources. Minerals, 2016, 6(2), 54.
[67]
Aresta, M.; Dibenedetto, A.; Quaranta, E. Enzymatic Conversion of
CO2 (Carboxylation Reactions and Reduction to Energy-Rich C1
Molecules) In: Reaction Mechanisms in Carbon Dioxide Conversion; Springer Berlin Heidelberg: Berlin, Heidelberg. , 2016. pp.
347-371
[68]
Shi, J.; Jiang, Y.; Jiang, Z.; Wang, X.; Wang, X.; Zhang, S.; Han, P.; Yang, C. Enzymatic conversion of carbon dioxide. Chem. Soc. Rev., 2015, 44(17), 5981-6000.
[69]
Bao, L.; Huang, Q.; Chang, L.; Sun, Q.; Zhou, J.; Lu, H. Cloning and characterization of two β-glucosidase/xylosidase enzymes from yak rumen metagenome. Appl. Biochem. Biotechnol., 2012, 166(1), 72-86.
[70]
Chang, L.; Ding, M.; Bao, L.; Chen, Y.; Zhou, J.; Lu, H. Characterization of a bifunctional xylanase/endoglucanase from yak rumen microorganisms. Appl. Microbiol. Biotechnol., 2011, 90(6), 1933-1942.
[71]
Liu, G.; Wu, S.; Jin, W.; Sun, C. Amy63, a novel type of marine bacterial multifunctional enzyme possessing amylase, agarase and carrageenase activities. Sci. Rep., 2016, 6, 18726.
[72]
Rashamuse, K.J.; Visser, D.F.; Hennessy, F.; Kemp, J.; Roux-van der Merwe, M.P.; Badenhorst, J.; Ronneburg, T.; Francis-Pope, R.; Brady, D. Characterisation of two bifunctional cellulase-xylanase enzymes isolated from a bovine rumen metagenome library. Curr. Microbiol., 2013, 66(2), 145-151.
[73]
Fisher, A.K.; Freedman, B.G.; Bevan, D.R.; Senger, R.S. A review of metabolic and enzymatic engineering strategies for designing and optimizing performance of microbial cell factories. Comput. Struct. Biotechnol. J., 2014, 11(18), 91-99.
[74]
Guo, W.; Sheng, J.; Feng, X. Mini-review: In vitro metabolic engineering for biomanufacturing of high-value products. Comput. Struct. Biotechnol. J., 2017, 15, 161-167.
[75]
Jin, Y.S.; Cate, J.H. Metabolic engineering of yeast for lignocellulosic biofuel production. Curr. Opin. Chem. Biol., 2017, 41, 99-106.
[76]
Pröschel, M.; Detsch, R.; Boccaccini, A.R.; Sonnewald, U. Engineering of metabolic pathways by artificial enzyme channels. Front. Bioeng. Biotechnol., 2015, 3, 168.
[77]
Tatsis, E.C.; O’Connor, S.E. New developments in engineering plant metabolic pathways. Curr. Opin. Biotechnol., 2016, 42, 126-132.
[78]
Narcross, L.; Bourgeois, L.; Fossati, E.; Burton, E.; Martin, V.J.J. Mining enzyme diversity of transcriptome libraries through dna synthesis for benzylisoquinoline alkaloid pathway optimization in yeast. ACS Synth. Biol., 2016, 5(12), 1505-1518.
[79]
Miyahisa, I.; Kaneko, M.; Funa, N.; Kawasaki, H.; Kojima, H.; Ohnishi, Y.; Horinouchi, S. Efficient production of (2S)-flavanones by Escherichia coli containing an artificial biosynthetic gene cluster. Appl. Microbiol. Biotechnol., 2005, 68(4), 498-504.
[80]
Walther, T.; Topham, C.M.; Irague, R.; Auriol, C.; Baylac, A.; Cordier, H.; Dressaire, C.; Lozano-Huguet, L.; Tarrat, N.; Martineau, N.; Stodel, M.; Malbert, Y.; Maestracci, M.; Huet, R.; André, I.; Remaud-Siméon, M.; François, J.M. Construction of a synthetic metabolic pathway for biosynthesis of the non-natural methionine precursor 2,4-dihydroxybutyric acid. Nat. Commun., 2017, 8, 15828.
[81]
Andrade, A.F.; Borges, K.S.; Silveira, V.S. Update on the use of L-asparaginase in infants and adolescent patients with acute lymphoblastic leukemia. Clin. Med. Insights Oncol., 2014, 8, 95-100.
[82]
Brooks, P.J.; Tagle, D.A.; Groft, S. Expanding rare disease drug trials based on shared molecular etiology. Nat. Biotechnol., 2014, 32(6), 515-518.
[83]
Reis, E.S.; Mastellos, D.C.; Yancopoulou, D.; Risitano, A.M.; Ricklin, D.; Lambris, J.D. Applying complement therapeutics to rare diseases. Clin. Immunol., 2015, 161(2), 225-240.
[84]
Pennington, M.W.; Czerwinski, A.; Norton, R.S. Peptide therapeutics from venom: Current status and potential. Bioorg. Med. Chem., 2018, 26(10), 2738-2758.
[85]
Thayer, A.M. Improving peptides (Small firms develop better peptide drug candidates to expand this pharmaceutical class and attract big pharma partners). Chem. Eng. News, 2011, 89(22), 13-20.
[86]
King, G.F. Venoms as a platform for human drugs: Translating toxins into therapeutics. Expert Opin. Biol. Ther., 2011, 11(11), 1469-1484.
[87]
Bruno, B.J.; Miller, G.D.; Lim, C.S. Basics and recent advances in peptide and protein drug delivery. Ther. Deliv., 2013, 4(11), 1443-1467.
[88]
Craik, D.J.; Fairlie, D.P.; Liras, S.; Price, D. The future of peptide-based drugs. Chem. Biol. Drug Des., 2013, 81(1), 136-147.
[89]
Robinson, S.D.; Undheim, E.A.B.; Ueberheide, B.; King, G.F. Venom peptides as therapeutics: Advances, challenges and the future of venom-peptide discovery. Expert Rev. Proteomics, 2017, 14(10), 931-939.
[90]
Carter, P.J. Introduction to current and future protein therapeutics: A protein engineering perspective. Exp. Cell Res., 2011, 317(9), 1261-1269.
[91]
Chung, J. Special issue on therapeutic antibodies and biopharmaceuticals. Exp. Mol. Med., 2017, 49(3), e304.
[92]
Appeltans, W.; Ahyong, S.T.; Anderson, G.; Angel, M.V.; Artois, T.; Bailly, N.; Bamber, R.; Barber, A.; Bartsch, I.; Berta, A.; Błażewicz-Paszkowycz, M.; Bock, P.; Boxshall, G.; Boyko, C.B.; Brandão, S.N.; Bray, R.A.; Bruce, N.L.; Cairns, S.D.; Chan, T.Y.; Cheng, L.; Collins, A.G.; Cribb, T.; Curini-Galletti, M.; Dahdouh-Guebas, F.; Davie, P.J.F.; Dawson, M.N.; De Clerck, O.; Decock, W.; De Grave, S.; de Voogd, N.J.; Domning, D.P.; Emig, C.C.; Erséus, C.; Eschmeyer, W.; Fauchald, K.; Fautin, D.G.; Feist, S.W.; Fransen, C.H.J.M.; Furuya, H.; Garcia-Alvarez, O.; Gerken, S.; Gibson, D.; Gittenberger, A.; Gofas, S.; Gómez-Daglio, L.; Gordon, D.P.; Guiry, M.D.; Hernandez, F.; Hoeksema, B.W.; Hopcroft, R.R.; Jaume, D.; Kirk, P.; Koedam, N.; Koenemann, S.; Kolb, J.B.; Kristensen, R.M.; Kroh, A.; Lambert, G.; Lazarus, D.B.; Lemaitre, R.; Longshaw, M.; Lowry, J.; Macpherson, E.; Madin, L.P.; Mah, C.; Mapstone, G.; McLaughlin, P.A.; Mees, J.; Meland, K.; Messing, C.G.; Mills, C.E.; Molodtsova, T.N.; Mooi, R.; Neuhaus, B.; Ng, P.K.L.; Nielsen, C.; Norenburg, J.; Opresko, D.M.; Osawa, M.; Paulay, G.; Perrin, W.; Pilger, J.F.; Poore, G.C.B.; Pugh, P.; Read, G.B.; Reimer, J.D.; Rius, M.; Rocha, R.M.; Saiz-Salinas, J.I.; Scarabino, V.; Schierwater, B.; Schmidt-Rhaesa, A.; Schnabel, K.E.; Schotte, M.; Schuchert, P.; Schwabe, E.; Segers, H.; Self-Sullivan, C.; Shenkar, N.; Siegel, V.; Sterrer, W.; Stöhr, S.; Swalla, B.; Tasker, M.L.; Thuesen, E.V.; Timm, T.; Todaro, M.A.; Turon, X.; Tyler, S.; Uetz, P.; van der Land, J.; Vanhoorne, B.; van Ofwegen, L.P.; van Soest, R.W.M.; Vanaverbeke, J.; Walker-Smith, G.; Walter, T.C.; Warren, A.; Williams, G.C.; Wilson, S.P.; Costello, M.J. The magnitude of global marine species diversity. Curr. Biol., 2012, 22(23), 2189-2202.
[93]
Mora, C.; Tittensor, D.P.; Adl, S.; Simpson, A.G.B.; Worm, B. How many species are there on Earth and in the ocean? PLoS Biol., 2011, 9(8), e1001127.
[94]
Amaral-Zettler, L.; Artigas, L.F.; Baross, J.; Bharathi, P.A.L.; Boetius, A.; Chandramohan, D.; Herndl, G.; Kogure, K.; Neal, P.; Pedrós-Alió, C.; Ramette, A.; Schouten, S.; Stal, L.; Thessen, A.; Leeuw, J.D.; Sogin, M. A Global Census of Marine Microbes.Life in the World’s Oceans; McIntyre, A.D., Ed.; Wiley-Blackwell: Oxford, UK, 2010, pp. 221-245.
[95]
van de Water, J.; Allemand, D.; Ferrier-Pages, C. Host-microbe interactions in octocoral holobionts - recent advances and perspectives. Microbiome, 2018, 6(1), 64.
[96]
Goulletquer, P.; Gros, P.; Boeuf, G.; Weber, J. The Importance of Marine Biodiversity.Biodiversity in the Marine Environment; Springer Netherlands: Dordrecht, 2014, pp. 1-13.
[97]
Smith, W.L.; Stern, J.H.; Girard, M.G.; Davis, M.P. Evolution of venomous cartilaginous and ray-finned fishes. Integr. Comp. Biol., 2016, 56(5), 950-961.
[98]
Smith, W.L.; Wheeler, W.C. Venom evolution widespread in fishes: A phylogenetic road map for the bioprospecting of piscine venoms. J. Hered., 2006, 97(3), 206-217.
[99]
Amann, R.I.; Ludwig, W.; Schleifer, K.H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev., 1995, 59(1), 143-169.
[100]
Ponce, D.; Brinkman, D.L.; Potriquet, J.; Mulvenna, J. Tentacle transcriptome and venom proteome of the pacific sea nettle, Chrysaora fuscescens (Cnidaria: Scyphozoa). Toxins (Basel), 2016, 8(4), 102.
[101]
Brinkman, D.L.; Jia, X.; Potriquet, J.; Kumar, D.; Dash, D.; Kvaskoff, D.; Mulvenna, J. Transcriptome and venom proteome of the box jellyfish Chironex fleckeri. BMC Genomics, 2015, 16, 407.
[102]
Verdes, A.; Anand, P.; Gorson, J.; Jannetti, S.; Kelly, P.; Leffler, A.; Simpson, D.; Ramrattan, G.; Holford, M. From mollusks to medicine: A venomics approach for the discovery and characterization of therapeutics from terebridae peptide toxins. Toxins (Basel), 2016, 8(4), 117.
[103]
Hennebert, E.; Leroy, B.; Wattiez, R.; Ladurner, P. An integrated transcriptomic and proteomic analysis of sea star epidermal secretions identifies proteins involved in defense and adhesion. J. Proteomics, 2015, 128, 83-91.
[104]
Gutleben, J.; Chaib De Mares, M.; van Elsas, J.D.; Smidt, H.; Overmann, J.; Sipkema, D. The multi-omics promise in context: From sequence to microbial isolate. Crit. Rev. Microbiol., 2018, 44(2), 212-229.
[105]
Jeon, J.H.; Lee, H.S.; Kim, J.T.; Kim, S.J.; Choi, S.H.; Kang, S.G.; Lee, J.H. Identification of a new subfamily of salt-tolerant esterases from a metagenomic library of tidal flat sediment. Appl. Microbiol. Biotechnol., 2012, 93(2), 623-631.
[106]
Kim, E.Y.; Oh, K.H.; Lee, M.H.; Kang, C.H.; Oh, T.K.; Yoon, J.H. Novel cold-adapted alkaline lipase from an intertidal flat metagenome and proposal for a new family of bacterial lipases. Appl. Environ. Microbiol., 2009, 75(1), 257-260.
[107]
Kim, W.J.; Park, J.W.; Park, J.K.; Choi, D.J.; Park, Y.I. Purification and characterization of a fucoidanase (FNase S) from a marine bacterium Sphingomonas paucimobilis PF-1. Mar. Drugs, 2015, 13(7), 4398-4417.
[108]
Kimura, K.; Okuda, S.; Nakayama, K.; Shikata, T.; Takahashi, F.; Yamaguchi, H.; Skamoto, S.; Yamaguchi, M.; Tomaru, Y. RNA sequencing revealed numerous polyketide synthase genes in the harmful dinoflagellate Karenia mikimotoi. PLoS One, 2015, 10(11), e0142731.
[109]
Makhdoumi, A.; Dehghani-Joybari, Z.; Mashreghi, M.; Jamialahmadi, K.; Asoodeh, A. A novel halo-alkali-tolerant and thermo-tolerant chitinase from Pseudoalteromonas sp. DC14 isolated from the Caspian Sea. Int. J. Environ. Sci. Technol., 2015, 12(12), 3895-3904.
[110]
Park, H.J.; Lee, Y.M.; Kim, S.; Wi, A.R.; Han, S.J.; Kim, H.W.; Kim, I.C.; Yim, J.H.; Kim, D. Identification of proteolytic bacteria from the Arctic Chukchi Sea expedition cruise and characterization of cold-active proteases. J. Microbiol., 2014, 52(10), 825-833.
[111]
Wang, L.; Wang, W.; Lai, Q.; Shao, Z. Gene diversity of CYP153A and AlkB alkane hydroxylases in oil-degrading bacteria isolated from the Atlantic Ocean. Environ. Microbiol., 2010, 12(5), 1230-1242.
[112]
Wang, Q.F.; Wang, Y.F.; Hou, Y.H.; Shi, Y.L.; Han, H.; Miao, M.; Wu, Y.Y.; Liu, Y.P.; Yue, X.N.; Li, Y.J. Cloning, expression and biochemical characterization of recombinant superoxide dismutase from Antarctic psychrophilic bacterium Pseudoalteromonas sp. ANT506. J. Basic Microbiol., 2016, 56(7), 753-761.
[113]
Inoue, A.; Anraku, M.; Nakagawa, S.; Ojima, T. Discovery of a novel alginate lyase from nitratiruptor sp. SB155-2 thriving at deep-sea hydrothermal vents and identification of the residues responsible for its heat stability. J. Biol. Chem., 2016, 291(30), 15551-15563.
[114]
Placido, A.; Hai, T.; Ferrer, M.; Chernikova, T.N.; Distaso, M.; Armstrong, D.; Yakunin, A.F.; Toshchakov, S.V.; Yakimov, M.M.; Kublanov, I.V.; Golyshina, O.V.; Pesole, G.; Ceci, L.R.; Golyshin, P.N. Diversity of hydrolases from hydrothermal vent sediments of the Levante Bay, Vulcano Island (Aeolian archipelago) identified by activity-based metagenomics and biochemical characterization of new esterases and an arabinopyranosidase. Appl. Microbiol. Biotechnol., 2015, 99(23), 10031-10046.
[115]
Zhang, L.; Huang, Y.; Xu, D.; Yang, L.; Qian, K.; Chang, G.; Gong, Y.; Zhou, X.; Ma, K. Biochemical characterization of a thermostable HNH endonuclease from deep-sea thermophilic bacteriophage GVE2. Appl. Microbiol. Biotechnol., 2016, 100(18), 8003-8012.
[116]
Shao, X.; Ran, L.Y.; Liu, C.; Chen, X.L.; Zhang, X.Y.; Qin, Q.L.; Zhou, B.C.; Zhang, Y.Z. Culture condition optimization and pilot scale production of the M12 metalloprotease myroilysin produced by the deep-sea bacterium Myroides profundi D25. Molecules, 2015, 20(7), 11891-11901.
[117]
Yu, P.; Wang, X.T.; Liu, J.W. Purification and characterization of a novel cold-adapted phytase from Rhodotorula mucilaginosa strain JMUY14 isolated from Antarctic. J. Basic Microbiol., 2015, 55(8), 1029-1039.
[118]
Zeng, R.; Xiong, P.; Wen, J. Characterization and gene cloning of a cold-active cellulase from a deep-sea psychrotrophic bacterium Pseudoalteromonas sp. DY3. Extremophiles, 2006, 10(1), 79-82.
[119]
Zhang, Y.; Hao, J.; Zhang, Y.Q.; Chen, X.L.; Xie, B.B.; Shi, M.; Zhou, B.C.; Zhang, Y.Z.; Li, P.Y. Identification and characterization of a novel salt-tolerant esterase from the deep-sea sediment of the South China Sea. Front. Microbiol., 2017, 8, 441.
[120]
Borchert, E.; Jackson, S.A.; O’Gara, F.; Dobson, A.D.W. Diversity of natural product biosynthetic genes in the microbiome of the deep sea sponges Inflatella pellicula, Poecillastra compressa, and Stelletta normani. Front. Microbiol., 2016, 07, 1027.
[121]
Cristóbal, H.A.; Breccia, J.D.; Abate, C.M. Isolation and molecular characterization of Shewanella sp. G5, a producer of cold-active beta-D-glucosidases. J. Basic Microbiol., 2008, 48(1), 16-24.
[122]
De Santi, C.; Leiros, H.K.S.; Di Scala, A.; de Pascale, D.; Altermark, B.; Willassen, N.P. Biochemical characterization and structural analysis of a new cold-active and salt-tolerant esterase from the marine bacterium Thalassospira sp. Extremophiles, 2016, 20(3), 323-336.
[123]
Del-Cid, A.; Ubilla, P.; Ravanal, M.C.; Medina, E.; Vaca, I.; Levicán, G.; Eyzaguirre, J.; Chávez, R. Cold-active xylanase produced by fungi associated with Antarctic marine sponges. Appl. Biochem. Biotechnol., 2014, 172(1), 524-532.
[124]
Fu, X.T.; Lin, H.; Kim, S.M. Purification and characterization of a novel beta-agarase, AgaA34, from Agarivorans albus YKW-34. Appl. Microbiol. Biotechnol., 2008, 78(2), 265-273.
[125]
Inoue, A.; Satoh, A.; Morishita, M.; Tokunaga, Y.; Miyakawa, T.; Tanokura, M.; Ojima, T. Functional heterologous expression and characterization of mannuronan C5-epimerase from the brown alga Saccharina japonica. Algal Res., 2016, 16, 282-291.
[126]
Irwin, J.A.; Lynch, S.V.; Coughlan, S.; Baker, P.J.; Gudmundsson, H.M.; Alfredsson, G.A.; Rice, D.W.; Engel, P.C. Alanine dehydrogenase from the psychrophilic bacterium strain PA-43: Overexpression, molecular characterization, and sequence analysis. Extremophiles, 2003, 7(2), 135-143.
[127]
Itoi, S.; Kanomata, Y.; Koyama, Y.; Kadokura, K.; Uchida, S.; Nishio, T.; Oku, T.; Sugita, H. Identification of a novel endochitinase from a marine bacterium Vibrio proteolyticus strain No. 442. Biochim. Biophys. Acta, 2007, 1774(9), 1099-1107.
[128]
Lario, L.D.; Chaud, L.; Almeida, M.D.G.; Converti, A.; Durães Sette, L.; Pessoa, A. Production, purification, and characterization of an extracellular acid protease from the marine Antarctic yeast Rhodotorula mucilaginosa L7. Fungal Biol., 2015, 119(11), 1129-1136.
[129]
Le Goff, C.; Ganot, P.; Zoccola, D.; Caminiti-Segonds, N.; Allemand, D.; Tambutté, S. Carbonic anhydrases in cnidarians: Novel perspectives from the octocorallian Corallium rubrum. PLoS One, 2016, 11(8), e0160368.
[130]
Liao, M.L.; Zhang, S.; Zhang, G.Y.; Chu, Y.M.; Somero, G.N.; Dong, Y.W. Heat-resistant cytosolic malate dehydrogenases (cMDHs) of thermophilic intertidal snails (genus Echinolittorina): Protein underpinnings of tolerance to body temperatures reaching 55°C. J. Exp. Biol., 2017, 220(Pt 11), 2066-2075.
[131]
Lipowicz, B.; Hanekop, N.; Schmitt, L.; Proksch, P. An aeroplysinin-1 specific nitrile hydratase isolated from the marine sponge Aplysina cavernicola. Mar. Drugs, 2013, 11(8), 3046-3067.
[132]
Otero, I.V.R.; Ferro, M.; Bacci, M.; Ferreira, H.; Sette, L.D. De novo transcriptome assembly: A new laccase multigene family from the marine-derived basidiomycete Peniophora sp. CBMAI 1063. AMB Express, 2017, 7(1), 222.
[133]
Thapa, H.R.; Naik, M.T.; Okada, S.; Takada, K.; Molnár, I.; Xu, Y.; Devarenne, T.P. A squalene synthase-like enzyme initiates production of tetraterpenoid hydrocarbons in Botryococcus braunii Race L. Nat. Commun., 2016, 7, 11198.
[134]
Zhu, B.; Ning, L. Purification and characterization of a new κ-carrageenase from the marine bacterium vibrio sp. NJ-2. J. Microbiol. Biotechnol., 2016, 26(2), 255-262.
[135]
Morlighem, R.L. J.É.; Huang, C.; Liao, Q.; Braga Gomes, P.; Daniel Pérez, C.; de Brandão Prieto-da-Silva, Á.; Ming-Yuen Lee, S.; Rádis-Baptista, G. The holo-transcriptome of the zoantharian Protopalythoa variabilis (Cnidaria: Anthozoa): A plentiful source of enzymes for potential application in green chemistry, industrial and pharmaceutical biotechnology. Mar. Drugs, 2018, 16(6), 207.
[136]
Gao, B.; Peng, C.; Yang, J.; Yi, Y.; Zhang, J.; Shi, Q. Cone snails: A big store of conotoxins for novel drug discovery. Toxins (Basel), 2017, 9(12), E397.
[137]
Robinson, S.D.; Norton, R.S. Conotoxin gene superfamilies. Mar. Drugs, 2014, 12(12), 6058-6101.
[138]
Safavi-Hemami, H.; Gajewiak, J.; Karanth, S.; Robinson, S.D.; Ueberheide, B.; Douglass, A.D.; Schlegel, A.; Imperial, J.S.; Watkins, M.; Bandyopadhyay, P.K.; Yandell, M.; Li, Q.; Purcell, A.W.; Norton, R.S.; Ellgaard, L.; Olivera, B.M. Specialized insulin is used for chemical warfare by fish-hunting cone snails. Proc. Natl. Acad. Sci. USA, 2015, 112(6), 1743-1748.
[139]
Karthik, R.; Manigandan, V.; Ebenezar, K.K.; Vijayashree, R.; Saravanan, R. In vitro and in vivo anticancer activity of posterior salivary gland toxin from the cuttlefish Sepia pharaonis, Ehrenberg (1831). Chem. Biol. Interact., 2017, 272, 10-20.
[140]
Liao, Q.; Gong, G.; Siu, S.; Wong, C.; Yu, H.; Tse, Y.; Rádis-Baptista, G.; Lee, S. A novel ShK-Like toxic peptide from the transcriptome of the cnidarian Palythoa caribaeorum displays neuroprotection and cardioprotection in Zebrafish. Toxins (Basel), 2018, 10(6), 238.
[141]
Huang, C.; Morlighem, J.R.; Zhou, H.; Lima, E.P.; Gomes, P.B.; Cai, J.; Lou, I.; Perez, C.D.; Lee, S.M.; Radis-Baptista, G. The transcriptome of the zoanthid Protopalythoa variabilis (Cnidaria, Anthozoa) predicts a basal repertoire of toxin-like and venom-auxiliary polypeptides. Genome Biol. Evol., 2016, 8(9), 3045-3064.
[142]
Prentis, P.J.; Pavasovic, A.; Norton, R.S. Sea anemones: Quiet achievers in the field of peptide toxins. Toxins (Basel), 2018, 10(1), E36.
[143]
Berio, A.; Piazzi, A. Activity of drugs and components of natural origin in the severe myoclonic epilepsy of infancy (Dravet syndrome). Cent. Nerv. Syst. Agents Med. Chem., 2015, 15(2), 95-98.
[144]
Logashina, Y.A.; Mosharova, I.V.; Korolkova, Y.V.; Shelukhina, I.V.; Dyachenko, I.A.; Palikov, V.A.; Palikova, Y.A.; Murashev, A.N.; Kozlov, S.A.; Stensvåg, K.; Andreev, Y.A. Peptide from sea anemone Metridium senile affects transient receptor potential ankyrin-repeat 1 (TRPA1) function and produces analgesic effect. J. Biol. Chem., 2017, 292(7), 2992-3004.
[145]
Shen, B.; Cao, Z.; Li, W.; Sabatier, J.M.; Wu, Y. Treating autoimmune disorders with venom-derived peptides. Expert Opin. Biol. Ther., 2017, 17(9), 1065-1075.
[146]
Monastyrnaya, M.; Peigneur, S.; Zelepuga, E.; Sintsova, O.; Gladkikh, I.; Leychenko, E.; Isaeva, M.; Tytgat, J.; Kozlovskaya, E. Kunitz-type peptide HCRG21 from the sea anemone Heteractis crispa is a full antagonist of the TRPV1 receptor. Mar. Drugs, 2016, 14(12), E229.
[147]
Wang, N.; Huang, Y.; Li, A.; Jiang, H.; Wang, J.; Li, J.; Qiu, L.; Li, K.; Lu, Y. Hydrostatin-TL1, an anti-inflammatory active peptide from the venom gland of Hydrophis cyanocinctus in the South China Sea. Int. J. Mol. Sci., 2016, 17(11), E1940.
[148]
Wu, G.; Wang, J.; Luo, P.; Li, A.; Tian, S.; Jiang, H.; Zheng, Y.; Zhu, F.; Lu, Y.; Xia, Z. Hydrostatin-SN1, a sea snake-derived bioactive peptide, reduces inflammation in a mouse model of acute lung injury. Front. Pharmacol., 2017, 8, 246.
[149]
Houyvet, B.; Bouchon-Navaro, Y.; Bouchon, C.; Goux, D.; Bernay, B.; Corre, E.; Zatylny-Gaudin, C. Identification of a moronecidin-like antimicrobial peptide in the venomous fish Pterois volitans: Functional and structural study of pteroicidin-α. Fish Shellfish Immunol., 2018, 72, 318-324.
[150]
Nsrelden, R.M.; Horiuchi, H.; Furusawa, S. Expression of ayu antimicrobial peptide genes after LPS stimulation. J. Vet. Med. Sci., 2017, 79(6), 1072-1080.
[151]
Komegae, E.N.; Souza, T.A.M.; Grund, L.Z.; Lima, C.; Lopes-Ferreira, M. Multiple functional therapeutic effects of TnP: A small stable synthetic peptide derived from fish venom in a mouse model of multiple sclerosis. PLoS One, 2017, 12(2), e0171796.
[152]
Baumann, K.; Casewell, N.R.; Ali, S.A.; Jackson, T.N.W.; Vetter, I.; Dobson, J.S.; Cutmore, S.C.; Nouwens, A.; Lavergne, V.; Fry, B.G. A ray of venom: Combined proteomic and transcriptomic investigation of fish venom composition using barb tissue from the blue-spotted stingray (Neotrygon kuhlii). J. Proteomics, 2014, 109, 188-198.
[153]
Xie, B.; Li, X.; Lin, Z.; Ruan, Z.; Wang, M.; Liu, J.; Tong, T.; Li, J.; Huang, Y.; Wen, B.; Sun, Y.; Shi, Q. Prediction of toxin genes from chinese yellow catfish based on transcriptomic and proteomic sequencing. Int. J. Mol. Sci., 2016, 17(4), 556.
[154]
Ziegman, R.; Alewood, P. Bioactive components in fish venoms. Toxins (Basel), 2015, 7(5), 1497-1531.
[155]
Campos, F.V.; Menezes, T.N.; Malacarne, P.F.; Costa, F.L.S.; Naumann, G.B.; Gomes, H.L.; Figueiredo, S.G. A review on the Scorpaena plumieri fish venom and its bioactive compounds. J. Venom. Anim. Toxins Incl. Trop. Dis., 2016, 22, 35.
[156]
Essack, M.; Bajic, V.B.; Archer, J.A.C. Conotoxins that confer therapeutic possibilities. Mar. Drugs, 2012, 10(6), 1244-1265.
Related Journals
Protein & Peptide Letters
Related Books
Frontiers in Protein and Peptide Sciences
Article Metrics
40
6