Peptidomic analysis of bioactive peptides in zebra blenny (Salaria basilisca) muscle protein hydrolysate exhibiting antimicrobial activity obtained by fermentation with Bacillus mojavensis A21

Process Biochemistry

Volumn 51, Issue 12, 2016, Pages 2186-2197

  Jemil, Ines ^a   Abdelhedi, Ola ^a   Mora, Leticia ^b   Nasri, Rim ^a   Aristoy, Maria Concepción ^b   Jridi, Mourad ^a   Hajji, Mohamed ^a   Toldrá, Fidel ^b   Nasri, Moncef ^a  

^a UNIVERSITY OF SFAX   (Tunisia)

^b INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

Author keywords

Antibacterial peptides; Bacillus mojavensis A21; Fermentation; Protein hydrolysates; Salaria basilisca

Indexed keywords

BACTERIA; BACTERIOLOGY; CHROMATOGRAPHY; FERMENTATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; ION EXCHANGE; LIQUID CHROMATOGRAPHY; MICROORGANISMS; PEPTIDES; SIZE EXCLUSION CHROMATOGRAPHY;

ANTI-BACTERIAL ACTIVITY; ANTI-MICROBIAL ACTIVITY; ANTIBACTERIAL PEPTIDES; BACILLUS MOJAVENSIS; NATURAL-ANTIMICROBIALS; PROTEIN HYDROLYSATE; REVERSED-PHASE HIGH-PERFORMANCE LIQUID CHROMATOGRAPHY; SALARIA BASILISCA;

PROTEINS;

EID: 85002940310     PISSN: 13595113     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.procbio.2016.08.021     Document Type: Article

References (74)

1. [1] Van't Hof, W., Veerman, E.C., Helmerhorst, E.J., Amerongen, A.V., Antimicrobial peptides: properties and applicability. Biol. Chem. 382 (2001), 597–619.
2. [2] Sugiarto, H., Yu, P.L., Avian antimicrobial peptides: the defense role of beta-defensins. Biochem. Biophys. Res. Commun. 323 (2004), 721–727.
3. [3] Ennaas, N., Hammami, R., Beaulieu, L., Fliss, I., Purification and characterization of four antibacterial peptides from protames hydrolysate of Atlantic mackerel (Scomber scombrus) by-products. Biochem. Biophys. Res. Commun. 462 (2015), 195–200.
4. [4] Tang, W., Zhang, H., Wang, L., Qian, H., Qi, X., Targeted separation of antibacterial peptide from protein hydrolysate of anchovy cooking wastewater by equilibrium dialysis. Food Chem. 168 (2015), 115–123.
5. [5] Beaulieu, L., Thibodeau, J., Desbiens, M., Saint-Louis, R., Zatylny-Gaudin, C., Thibault, S., Evidence of antibacterial activities in peptide fractions originating from snow crab (Chionoecetes opilio) by-product. Probiotics Antimicrob. Proteins 2 (2010), 197–209.
6. [6] Beaulieu, L., Thibodeau, J., Bonnet, C., Bryl, P., Carbonneau, M.E., Detection of antibacterial activity in an enzymatic hydrolysate fraction obtained from processing of Atlantic rock crab (Cancer irroratus) by-products. PharmaNutrition 1 (2013), 149–157.
7. [7] Balakrishnan, B., Prasad, B., Rai, A.K., Velappan, S.P., Subbanna, M.N., Narayan, B., In vitro antioxidant and antibacterial properties of hydrolysed proteins of delimed tannery fleshings: comparison of acid hydrolysis and fermentation methods. Biodegradation 22 (2011), 287–295.
8. [8] Kim Sk Wijesekara, I., Development and biological activities of marine-derived bioactive peptides: a review. J. Funct. Foods 2 (2010), 1–9.
9. [9] Jemil, I., Jridi, M., Nasri, R., Ktari, N., Ben Slama-Ben Salem, R., Hajji, M., et al. Functional, antioxidant and antibacterial properties of protein hydrolysates prepared from fish meat fermented by Bacillus subtilis A26. Process Biochem. 49 (2014), 963–972.
10. [10] Haddar, A., Bougatef, A., Agrebi, R., Sellami-Kamoun, A., Nasri, M., A novel surfactant-stable alkaline serine-protease from a newly isolated Bacillus mojavensis A21: Purification and characterization. Process Biochem. 44 (2009), 9–35.
11. [11] Miller, J.H., Experiments in Molecular Genetics. 1972, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 431–435.
12. [12] Nielsen, P.M., Petersen, D., Dambmann, C., Improved method for determining food protein degree of hydrolysis. J. Food Sci. 66 (2001), 642–646.
13. [13] AOAC, Official Methods of Analysis. 17th edn., 2000, Association of Official Analytical Chemists, Washington.
14. [14] Aristoy, M.C., Toldrá, F., Deproteinization techniques for HPLC amino acid analyses in fresh pork muscle and dry cured ham. J. Agric. Food Chem. 39 (1991), 1792–1795.
15. [15] Hernández-Cázares, A., Aristoy, M.C., Toldrá, F., An enzyme sensor for the determination of total amines in dry-fermented sausages. J. Food Ingred. 106 (2011), 166–169.
16. [16] Bidlingmeyer, B.A., Cohen, S.A., Tarvin, T.L., Rapid analysis of amino acids using pre-column derivatization. J. Chromatogr. 33 (1984), 93–104.
17. [17] Berghe, V.A., Vlietinck, A.J., Screening methods for antibacterial and antiviral agents from higher plants. Method Plant Biochem. 6 (1991), 47–68.
18. [18] Eloff, J.N., A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med. 64 (1998), 711–713.
19. [19] Mora, L., Escudero, E., Aristoy, M.C., Toldrá, F., A peptidomic approach to study the contribution of added casein proteins to the peptide profile in Spanish dry-fermented sausages. Int. J. Food Microbiol. 212 (2015), 41–48.
20. [20] Bouckenooghe, T., Remacle, C., Reusens, B., Is taurine a functional nutrient?. Curr. Opin. Clin. Nutr. Metab. Care 9 (2006), 723–733.
21. [21] Surette, M.E., Gill, T.A., LeBlanc, P.J., Biochemical basis of postmortem nucleotide catabolism in cod (Gadus morhua) and its relationship to spoilage. J. Agric. Food Chem. 36 (1988), 19–22.
22. [22] Kobayashi, Y., Habara, M., Ikezazki, H., Chen, R., Naito, Y., Toko, K., Advanced taste sensors based on artificial lipids with global selectivity to basic taste qualities and high correlation to sensory scores. Sensors 10 (2010), 3411–3443.
23. [23] Liaset, B., Espe, M., Nutritional composition of soluble and insoluble fractions obtained by enzymatic hydrolysis of fish-raw materials. Process Biochem. 43 (2008), 42–48.
24. [24] Mullally, M.M., Meisel, H., FitzGeral, R.J., Identification of a novel angiotensin-Iconverting enzyme inhibitory peptide corresponding to a tryptic fragment of bovine ß-lactoglobulin. FEBS Lett. 402 (1997), 99–101.
25. [25] Lassoued, I., Mora, L., Nasri, R., Aydi, M., Toldrá, F., Aristoy, M.C., et al. Characterization, antioxidative and ACE inhibitory properties of hydrolysates obtained from thornback ray (Raja clavata) muscle. J. Proteomics 128 (2015), 458–468.
26. [26] Brogden, K.A., Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev. Microbiol. 3 (2005), 238–250.
27. [27] Wieprecht, T., Dathe, M., Epand, R.M., Beyermann, M., Krause, E., Maloy, W.L., et al. Influence of the angle subtended by the positively charged helix face on the membrane activity of amphipathic, antibacterial peptides. Biochemistry 36 (1997), 12869–12880.
28. [28] Otvos, L., The short proline-rich antibacterial peptide family. Cell. Mol. Life Sci. 59 (2002), 1138–1150.
29. [29] Dong, N., Ma, Q., Shan, A., Lv, Y., Hu, W., Gu, Y., et al. Strand length-dependent antimicrobial activity and membrane active mechanism of arginine- and valine-rich β-hairpin-like antimicrobial peptides. Antimicrob. Agents Chemother. 56 (2012), 2994–3003.
30. [30] Ilic’, N., Novkovic’, M., Guida, F., Xhindoli, D., Benincasa, M., Tossi, A., et al. Selective antimicrobial activity and mode of action of adepantins, glycine-rich peptide antibiotics based on anuran antimicrobial peptide sequences. Biochim. Biophys. Acta 1828 (2013), 1004–1012.
31. [31] Hayes, M., Stanton, C., Fitzgerald, G.F., Ross, R.P., Putting microbes to work: dairy fermentation, cell factories and bioactive peptides: part II: bioactive peptide functions. Biotechnol. J. 2 (2007), 435–449.
32. [32] Byun, H.G., Kim, S.K., Structure and activity of angiotensin I-converting enzyme inhibitory peptides derived from Alaskan pollack skin. Biochem. Mol. Biol. 35 (2002), 239–243.
33. [33] Simmaco, M., Mignogna, G., Canofeni, S., Miele, R., Mangoni, M.L., Barra, D., Temporins, antimicrobial peptides from the European red frog Rana temporaria. Eur. J. Biochem. 242 (1996), 788–792.
34. [34] Lopez-Exposito, I., Minervini, F., Amigo, L., Recio, I., Identification of antibacterial peptides from bovine kappa-casein. J. Food Prot. 69 (2006), 2992–2997.
35. [35] Lopez-Exposito, I., Quiros, A., Amigo, L., Recio, I., Casein hydrolysates as a source of antimicrobial, antioxidant and antihypertensive peptides. Lait 87 (2007), 241–249.
36. [36] Gomez-Ruiz, J.A., Ramos, M., Recio, I., Identification of novel angiotensin-converting enzyme-inhibitory peptides from ovine milk proteins by CE-MS and chromatographic techniques. Electrophoresis 28 (2007), 4202–4211.
37. [37] Torres-Larios, A., Gurrola, G.B., Zamudio, F.Z., Possani, L.D., Hadrurin, a new antimicrobial peptide from the venom of the scorpion Hadrurus aztecus. Eur. J. Biochem. 267 (2000), 5023–5031.
38. [38] Hancock, R.E.W., Diamond, G., The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol. 9 (2000), 402–410.
39. [39] Zasloff, M., Antimicrobial peptides of multicellular organisms. Nature 415 (2002), 389–395.
40. [40] Hancock, R.E.W., Patrzykat, A., Clinical development of cationic antimicrobial peptides: from natural to novel antibiotics. Curr. Drug Targets Infect. Disord. 2 (2002), 79–83.
41. [41] Shai, Y., From innate immunity to de-novo designed antimicrobial peptides. Curr. Pharm. Des. 8 (2002), 715–725.
42. [42] Meisel, H., Walsh, D.J., Murray, B., FitzGerald, R.J., ACE inhibitory peptides. Mine, Y., Shahidi, F., (eds.) Nutraceutical Proteins and Peptides in Health and Disease, 2006, CRC Taylor & Francis Group, Boca Raton, London, New York, 269–315.
43. [43] Appendini, P., Hotchkiss, J.H., Antimicrobial activity of a 14-residue synthetic peptide against foodborne microorganisms. J. Food Prot. 63 (2000), 889–893.
44. [44] Ukeda, H., Matsuda, H., Osajima, K., Matsufuji, H., Matsui, T., Osajima, Y., Peptides from peptic hydrolysate of heated sardine meat that inhibit angiotensin I converting enzyme. Nippon Nōgeik Kaishi 66 (1992), 25–29.
45. [45] Lee, N.Y., Cheng, J.T., Enomoto, T., Nakano, Y., One peptide derived from hen ovotransferrin as pro-drug to inhibit angiotensin converting enzyme. J. Food Sci. Drug Anal. 14 (2006), 31–35.
46. [46] Minervini, F., Algaron, F., Rizzello, C.G., Fox, P.F., Monnet, V., Gobbetti, M., Angiotensin I-Converting-Enzyme-Inhibitory and antibacterial peptides from Lactobacillus helveticus PR4 proteinase-Hydrolyzed caseins of milk from six species. Appl. Environ. Microb. 69 (2003), 5297–5305.
47. [47] Chen, H.M., Muramoto, K., Yamauchi, F., Nokihara, K., Antioxidant activity of designed peptides based on the antioxidant peptide isolated from digests of a soybean protein. J. Agric. Food Chem. 44 (1996), 2619–2623.
48. [48] Loponen, J., Angiotensin converting enzyme inhibitory peptides in Finnish cereals: a database survey. Agric. Food Sci. 13 (2004), 39–45.
49. [49] Lee, K.H., Hong, Y.S., Oh, J.E., Kwon, M., Yoon, J.H., Lee, J., et al. Identification and characterization of the antimicrobial peptide corresponding to C-terminal b-sheet domain of tenecin 1, an antibacterial protein of larvae of Tenebrio molitor. Biochem. J 334 (1998), 99–105.
50. [50] Qian, Z.J., Jung, W.K., Kim, S.K., Free radical scavenging activity of a novel antioxidative peptide purified from hydrolysate of bullfrog skin, Rana catesbeiana Shaw. Bioresour. Technol. 99 (2008), 1690–1698.
51. [51] Zucht, H.D., Raida, M., Adermann, K., Mägert, H.J., Forssmann, W.G., Casocidin I: a casein-as2 derived peptide exhibits antibacterial activity. FEBS Lett. 372 (1995), 185–188.
52. [52] Tsopmo, A., Romanowski, A., Banda, L., Lavoie, J.C., Jenssen, H., Novel anti-oxidative peptides from enzymatic digestion of human milk. Food Chem. 126 (2011), 1138–1143.
53. [53] Escudero, E., Mora, L., Fraser, P.D., Aristoy, M.C., Arihara, K., Toldra, F., Purification and Identification of antihypertensive peptides in Spanish dry-cured ham. J. Proteomics 78 (2013), 499–507.
54. [54] Nongonierma, A.B., Mooney, C., Shields, D.C., FitzGerald, R.J., In silico approaches to predict the potential of milk protein-derivedpeptides as dipeptidyl peptidase IV (DPP-IV) inhibitors. Peptides 57 (2014), 43–51.
55. [55] Meisel, H., Casokinins as bioactive peptides in the primary strucure of casein. Schwenke, K.D., Mothes, R., (eds.) Food Proteins, Structure and Functionality, 1993, VCh, Weinheim, New York, Basel, Cambridge, Tokyo, 67–75.
56. [56] Maruyama, S., Miyoshi, S., Tanaka, H., Angiotensin I-converting enzyme inhibitors derived from ficus carica. Agric. Biol. Chem. 53 (1989), 2763–2767.
57. [57] Rival, S.G., Fornaroli, S., Boeriu, C.G., Wichers, H.J., Caseins and casein hydrolysates: 1. Lipoxygenase inhibitory properties. J. Agric. Food Chem. 49 (2001), 287–294.
58. [58] Du, D.G., Yao, S.Y., Rojas, M., Lin, Y.Z., Conformational and topological requirements of cell-permeable peptide function. J. Peptide Res. 51 (1998), 235–243.
59. [59] Suetsuna, K., Separation and identification of antioxidant peptides from proteolytic digest of dried bonito. Nippon Suisan Gakkaishi 65 (1999), 92–96 (Japanese Edition).
60. [60] Harwig, S.S.L., Kokryakov, V.N., Swiderek, K.M., Aleshina, G.M., Zhao, C., Lehrer, R.I., Prophenin-1, an exceptionally proline-rich antimicrobial peptide from porcine leukocytes. FEBS Lett. 362 (1995), 65–69.
61. [61] Casteels-Josson, K., Zhang, W., Capaci, T., Casteels, P., Tempst, P., Acute transcriptional response of the honeybee peptide-antibiotics gene repertoire and required post-translational conversion of the precursor structures. J. Biol. Chem. 269 (1994), 28569–28575.
62. [62] Liu, R., Zheng, W., Li, J., Wang, L., Wu, H., Wang, X., et al. Rapid identification of bioactive peptides with antioxidant activity from the enzymatic hydrolysate of Mactra veneriformis by UHPLC–Q-TOF mass spectrometry. Food Chem. 167 (2015), 484–489.
63. [63] Mayo, K.H., Haseman, J., Ilyina, E., Gray, B., Designed b-sheet-forming peptide 33mers with potent human bactericidal/permeability increasing protein-like bactericidal and endotoxin neutralizing activities. Biochem. Biophys. Acta 1425 (1998), 81–92.
64. [64] Kohama, Y., Nagase, Y., Oka, H., Nakagawa, T., Teramoto, T., Murayama, N., et al. Production of angiotensin-converting enzyme inhibitors from baker's yeasts Glyceraldehyde-3-phosphate Dehydrogenase. J. Pharmacobio-Dyn 13 (1990), 766–771.
65. [65] Ferrer-Miralles, N., Vazquez, E., Villaverde, A., Membrane-active peptides fro non-viral gene therapy: making the safest easier. Trends Biotechnol. 26 (2008), 267–275.
66. [66] De Gobba, C., Tompa, G., Otte, J., Bioactive peptides from caseins released by cold active proteolytic enzymes from Arsukibacterium ikkense. Food Chem. 165 (2014), 205–215.
67. [67] Larrick, J.W., Lee, J., Ma, S., Li, X., Francke, U., Wright, S.C., et al. Structural, functional analysis and localization of the human CAP18 gene. FEBS Lett. 398 (1996), 74–80.
68. [68] Rozek, T., Waugh, R.J., Steinborner, S.T., Bowie, J.H., Tyler, M.J., Wallace, J.C., The maculatin peptides from the skin glands of the tree frog Litoria genimaculata: a comparison of the structures and antibacterial activities of maculatin 1.1 and caerin 1.1. J. Pept. Sci. 4 (1998), 111–115.
69. [69] Gallego, M., Aristoy, M.C., Toldrá, F., Dipeptidyl peptidase IV inhibitory peptides generated in Spanish dry-cured ham. Meat Sci 96 (2014), 757–761.
70. [70] Pellegrini, A., Thomas, U., Bramaz, N., Hunziker, P., Von Fellenberg, R., Isolation and identification of three bactericidal domains in the bovine alpha-lactalbumin molecule. Biochim. Biophys. Acta 1426 (1999), 439–448.
71. [71] Bougatef, A., Nedjar-Arroume, N., Manni, L., Ravallec, R., Barkia, A., Guillochon, D., et al. Purification and identification of novel antioxidant peptides from enzymatic hydrolysates of sardinelle (Sardinella aurita) by-products proteins. Food Chem. 118 (2010), 559–565.
72. [72] Shen, G., Chahal, B., Majumder, K., You, S.J., Wu, J., Identification of novel antioxidative peptides derived from a thermolytic hydrolysate of ovotransferrin by LC-MS/MS. J. Agric. Food Chem. 58 (2010), 7664–7672.
73. [73] Tichaczek, P.S., Nissen-Meyer, J., Nes, I.F., Vogel, R.F., Hammes, W.P., Characterization of the bacteriocins curvacin A from Lactobacillus curvatus LTH1174 and sakacin P from L. sake LTH673. Syst. Appl. Microbiol. 15 (1992), 460–465.
74. [74] Mukhija, S., Germeroth, L., Schneider-Mergener, J., Erni, B., Identification of peptides inhibiting enzyme I of the bacterial phosphotransferase system using combinatorial cellulose-bound peptide libraries. Eur. J. Biochem. 254 (1998), 433–438.