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ANTIMICROBIAL ACTIVITY OF GOAT MILK CASEIN GENERATED BY LACTIC ACID BACTERIA USED AGAINST Cronobacter sakazakii IBRAHIM MUSTAFA ELSHAAFI UNIVERSITI SAINS ISLAM MALAYSIA
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  • ANTIMICROBIAL ACTIVITY OF GOAT MILK CASEIN GENERATED BY LACTIC ACID BACTERIA USED AGAINST

    Cronobacter sakazakii

    IBRAHIM MUSTAFA ELSHAAFI

    UNIVERSITI SAINS ISLAM MALAYSIA

  • ANTIMICROBIAL ACTIVITY OF GOAT MILK CASEIN GENERATED BY LACTIC ACID BACTERIA USED AGAINST

    Cronobacter sakazakii

    Ibrahim Mustafa Elshaafi (Matric. No. 3090103)

    Thesis submitted in fulfillment for the degree of master of science

    Faculty of Science and Technology UNIVERSITI SAINS ISLAM MALAYSIA

    NILAI

    January 2015

  • i

    APPROVAL

    The thesis entitled ANTIMICROBIAL ACTIVITY OF GOAT MILK CASEIN GENERATED BY LACTIC ACID BACTERIA USED AGAINST Cronobacter sakazakiisubmitted by Mr. Ibrahim Mustafa Elshaafi (Matric. No. 3090103) for the Degree of Master in Science was duly approved by the following academic authorities:

    ZAITON HASSAN, Ph.D, Faculty of Science and Technology, Universiti Sains Islam Malaysia Date: January 2015

  • ii

    AUTHORS DECLARATION

    I hereby declare that the work in this thesis entitled ANTIMICROBIAL ACTIVITY OF GOAT MILK CASEIN GENERATED BY LACTIC ACID BACTERIA USED AGAINST Cronobacter sakazakii and submitted for the Degree of Master in Science and Technologyis my own except for quotations and summaries which have been duly acknowledged.

    Date: Signature: Name: IBRAHIM MUSTAFA ELSHAAFI Matric No: 3090103 Address: Faculty of Science & Technology Universiti Sains Islam Malaysia (USIM) 71 800 Nilai, Negeri Sembilan, Malaysia

  • iii

    BIODATA OF AUTHOR

    Ibrahim Mustafa Elshaafi (3090103) was born on the 8th February 1987 in Misurata, Libya (828398). He completed his primary and secondary education in Misurata, a city located in the north west of Libya. He is holder of the degree in Microbiology, after a 3-year program at the Faculty of Sciences of the University of Misurata (7th October), Misurata, from 2005 to 2008. He is at present master student majoring in food microbiology.

  • iv

    ACKNOWLEDGEMENTS

    Grateful to Allah SWT and His Messenger Muhammad SAW. I would like first and foremost to extend my deepest gratitude to Assoc. Prof Dr. Zaiton Hassan who accepted to supervise this thesis work and for the provision of all needed supports despite her various other duties. Dear Assoc. Prof. Dr. Zaiton Hassan, I have learned from you more than I can humanly acknowledge here. I extend my heartfelt thanks to you for your patience, guidance and inspirational skills. I express my sincere gratitude to Dr. Hanina Mohd Noor for her commendable advices and guidance in her capacity of co-supervisor. Your advices and teachings have been instrumental in the implementation of my study program. My special acknowledgement and appreciation to Dr. Norakkiah Abdullah Sani from UKM who co-supervise this thesis and share her invaluable experience in Microbiology particularly in Cronobacter sakazakii. My deepest appreciations go to my colleagues Sharifah, Shahidah. Emdakim, Saadu Lawal, Dahimi, Belal, Honor and Aween for their help and friendship during my studies at USIM. Special regards are extended to my beloved elder brothers Ahmed, Mohammad and Abdullah, I thank my father, Mr. Mustafa Ali Elshaafi, and mother, Mrs Turkeyah Elttomi, for all the sacrifices consented for my education.

  • v

    ABSTRACT

    ANTIMICROBIAL ACTIVITY OF GOAT MILK CASEIN GENERATED BY LACTIC ACID BACTERIA USED AGAINST

    Cronobacter sakazakii

    Cronobacter sakazakii is a foodborne pathogen that has been implicated to be the main cause of neonates infections from reconstituted powdered infant formula and powdered milk. Attention is being focused on production of physiologically active compounds derived from milk proteins with antimicrobial property that are effective against the foodborne pathogens are increasing. This study was carried out to investigate the capabilities of 30 lactic acid bacteria (LAB) isolates obtained from different sources to hydrolyse goats milk casein (GMC) and produce peptides with antimicrobial activity that can inhibit the growth C. sakazakii and other pathogens. Eight isolates showed good proteolytic activity with clear zones ranging from 7 to 12 mm on skim milk-MRS agar. Initial screening of GMC fermented with these LAB isolates showed that three of them produced hydrolysates that showed antimicrobial activity against the target pathogens C. sakazakii ATCC 25944, C. sakazakii E4 and C. sakazakii O531G and other pathogens. The three LAB were identified as Lactobacillus casei CF2, Enterococcus faecium F.F.B, and Lactobacillus plantarum S by bio-chemical tests, API CHL50, and 16s DNA sequencing. The inhibitory activity of goat milk casein hydrolysate (GMCH) against multi antibiotic resistant pathogens were significantly (P

  • vi

    ABSTRAK

    Cronobacter sakazakii adalah pathogen bawaan makanan yang telah dibabitkan sebagai punca utama penyebab infeksi bayi daripada serbuk isian semula formula bayi dan susu tepung. Perhatian keatas penghasilan kompoun aktif fisiologi daripada protein susu yang mempunyai ciri antimikrob berkesan ke atas patogen bawaan makanan adalha meningkat. Kajian ini telah dijalankan untuk menyiasat kebolehan 30 bakteria asid laktik (LAB) yang dipencilkan daripada pelbagai sumber untuk menghidrolisis casein susu kambing (GMC) dan menghasilkan peptida yang mempunyai aktiviti antimikrob dan mampu merencat pertumbuhan C. sakazaki dan patogen lain. Lapan pencilan telah menunjukkan aktiviti proteolitik yang baik dengan zon cerah antara 7 ke 12 mm pada agar MRS-susu rendah lemak. Saringan awal ke atas GMC yang telah ditapai dengan pencilan LAB menunjukkan tiga daripadanya menghasilkan hidrolisat yang menunjukkan aktiviti antimikrob ke atas patogen sasaran C. sakazakii ATCC 25944, C. sakazakii E4 and C. sakazakii O531G dan patogen lain. Ketiga tiga LAB telah dikenalpasti sebagai Lactobacillus casei CF2, Enterococcus faecium F.F.B, dan Lactobacillus plantarum S menggunakan ujian bio-kimia, API CHL50, susunan 16s rDNA. Aktiviti perencatan kasein susu kambing hidrolisat (GMCH) keatas patogen pelbagai rintangan antibiotik adalah signifikan (p

  • vii

    . Cronobacter sakazakii .

    30 - 7 .

    . MRS 12 C. sakazakii 3

    ATCC 25944, C. sakazakii E4 and C. sakazakii O531G. . Lactobacillus casei CF2, Enterococcus faecium F.F.B, and Lactobacillus plantarum S API CHL 50

    . DNA . (p

  • viii

    CONTENTS

    CONTENTS Page APPROVAL i AUTHOR DECLARATION ii BIODATA OF AUTHOR iii ACKNOWLEDGEMENTS iv ABSTRACT v ABSTRAK vi vii CONTENT vii LIST OF TABLES xii LIST OF FIGURES xiv LIST OF APPENDICES xvi LIST OF ABBREVIATION AND SYMBOLS xvii CHAPTER 1: INTRODUCTION 1 CHAPTER 2: LITTERATURE REVIEW 4

    2.1 Cronobacter and Its Significance for Safety 4

    2.1.1 Taxonomy of Enterobacter sakazakii 4 2.1.2 Health hazards of Cronobacter in Infants 6 2.1.3 Characteristics of Cronobacter Species 8 2.1.4 Susceptibility of Cronobacter spp. to Antibiotics 10 2.1.5 Characteristics of Cronobacter Infections 10 2.1.6 Presence of Cronobacter in Infant Formula Milk 11 2.1.7 Inactivation and Inhibition of Cronobacter in Infant Formula Milk 13

    2.2 Antimicrobial Compounds Produced by Lactic Acid Bacteria 14 2.3 Occurrence of Bioactive Peptides in Various Milk and Milk Products 18

    2.3.1 Health Aspects 182.3.2 Antimicrobial Agents 20

    2.4 Production and Functionality of Bioactive Peptides 21

    2.4.1 Enzymatic Hydrolysis 22 2.4.2 Microbial Fermentation 23

    2.5 Milk as a Source of Antimicrobial Peptides 24 2.6 Lactose 25

  • ix

    CHAPTER 3: ISOLATION, CHARACTERIZATION AND IDENTIFICATION OF LACTIC ACID BACTERIA FROM DIFFERENT SOURCES

    26

    3.1 INTRODUCTION 26 3.2 MATERIALS AND METHODS 29

    3.2.1 Isolation of LAB from Different Sources 29 3.2.2 Proteolytic ActivityDetection 30 3.2.3 Acid and Bile Tolerance of LAB Isolates 30

    3.2.3.1 Bile Tolerance 30 3.2.3.2 Tolerance to Different Acidic pH Values 31

    3.2.4 Sodium Chloride Tolerance 31 3.2.5 Phenotypic Identification of LAB Using API 50 CHL Assay 32 3.2.6 Genotypic Characterization 32

    3.2.6.1 DNA Extraction 323.2.6.2 PCR Amplification of LAB 34 3.2.6.3 PCR Product Clean Up 35 3.2.6.4 Gel Extraction 36 3.2.6.5 PCR Product Sequencing 37

    3.3 RESULTS 37

    3.3.1 Proteolytic Activity of LAB Isolated from Different Sources 37 3.3.2 Bile salt, Acid and Sodium Chloride Tolerance of LAB Isolates 39 3.3.3 Phenotypic Identification of LAB Using API 50 CHL Assay 43 3.3.4 Molecular Characterization for LAB Isolates 45

    3.3.5 PCR of Lactic Acid Bacteria 46

    3.4 DISCUSSION 47 3.5 CONCLUSION 49

    CHAPTER 4: ANTIMICROBIAL ACTIVITY OF GOAT MILK CASEIN HYDROLYSATE AGAINST MULTI ANTIBIOTIC RESISTANT Cronobacter sakazakii AND SELECTED PATHOGENIC BACTERIA

    50

    4.1 INTRODUCTION 50 4.2 MATERIALS AND METHODS 53

    4.2.1 LAB Cultures 53 4.2.2 Goat and Bovine Milk Casein Preparation 53 4.2.3 Generation of Protein Hydrolysate 54 4.2.4 Protease Activity Assay (PA) 54 4.2.5 Antibiotic Resistant Test of Target Bacteria 56

  • x

    4.2.6 Antibacterial Activity of GMC and BMC Hydrolysate 56

    4.3 RESULTS 57 4.3.1 Protease Activity Assay (PA) 57 4.3.2 Multiple Antibiotic Resistant (MAR) Patterns of Tested Pathogens 57

    4.3.3 Antimicrobial Activity of GMC and BMC Hydrolysates against Selected Pathogens

    61

    4.4 DISCUSSION 62 4.5 CONCLUSION 64

    CHAPTER 5: ANTIMICROBIAL ACTIVITY OF GOAT MILK CASEIN HYDROLYSATE DERIVED FROM FERMENTATION OF GOAT MILK CASEIN WITH LACTIC ACID BACTERIA

    65

    5.1 INTRODUCTION 65 5.2 MATERIALS AND METHODS 67

    5.2.1 Microorganisms and Culture Conditions 67 5.2.2 Lactose Content 67 5.2.3 Detection of Proteolytic Activity by O-Phthalaldehyde (OPA) Spectrophotometric Assay

    68

    5.2.4 Protein Content of GMCH 69 5.2.5 Determination of pH of GMC Hydrolysates 70 5.2.6 Antimicrobial Kinetics of AMP 70 5.2.7 Amino Acid Composition 71 5.2.8 Statistical Analyses 72

    5.3 RESULTS 72

    5.3.1 Effect of Lactose Concentration and Fermentation Time on Proteolytic Activity (Pa) and pH of GMCH

    72

    5.3.2 Time-Kill Assay of GMCH 77 5.3.3 Amino Acid Composition of GMCH 84

    5.4 DISCUSSION 86 5.5 CONCLUSION 88

    CHAPTER 6: CONCLUSION AND RECOMMENDATIONS 89

    6.1 CONCLUSION 89 6.2 RECOMMENDATIONS 90

    REFERENCES 91

  • xi

    APPENDICES 134 LIST OF PUBLICATONS 147

  • i

    LIST OF TABLES

    Page

    TABLE 1: Characteristic of LAB Isolated from Different Sources 38

    TABLE 2: Growth of Selected LAB in MRS Broth with 0.3% of Bile Salt Incubated at 37oC Measured at OD560 nm

    40

    TABLE 3: Survival of pH-Stressed LAB-CF2 in MRS Broth Incubated at 37oc for 24h Measured at OD560 nm

    41

    TABLE 4: Survival of pH-Stressed LAB-F.F.B in MRS Broth Incubated at 37oC for 24 h Measured at OD560 nm

    41

    TABLE 5: Survival of pH-Stressed LAB-S in MRS Broth Incubated at 37oC for 24 h Measured at OD560 nm

    42

    TABLE 6: Survival of Selected LAB in MRS Broth with Different NaCl Concentrations Incubated at 37oC

    42

    TABLE 7: Carbohydrates Fermentation by Lactic Acid Bacteria Isolates Using API 50 CHL Identification System

    43

    TABLE 8: Quantification of Purified DNA Extracts 45

    TABLE 9: Protease Activity of Selected LAB on Hammersten Casein Incubated at 45oC for 30 min

    57

    TABLE 10: Antibacterial Activity of Selected Antibiotics Against Pathogenic Bacteria Measured by Diameter of Inhibition Zone around the Discs

    59

    TABLE 11: Antibacterial Activity of Selected Antibiotics Against Target C. sakazakii spp. Measured by Diameter of Inhibition Zone around the Discs

    60

    TABLE 12: Antimicrobial Activity of GMCH Against Selected Pathogens Incubated at 30oC for 24 h

    61

    TABLE 13: CFU Reduction of C. sakazakii ATCC 25944, C. sakazakii E4, andC.sakazakii O531G using different LAB-GMCH Concentrations Evaluated at Different Time Intervals

    82

  • ii

    TABLE 14: Initial Number of Target Pathogens at Different LAB-GMCH Concentrations

    83

    TABLE 15: Amino Acid Composition of GMCH Fermented by Selected LAB at 37oC for 48 h Incubation

    85

  • i

    LIST OF FIGURES

    Page

    FIGURE 1: Growth of LAB on MRS Agar with CaCO3 Showing Clear Zones around the Colonies

    37

    FIGURE 2: LAB Isolates as Seen Under the Microscope Showing the Shape and Gram Reaction

    38

    FIGURE 3: Clear Zones around LAB Colonies Indicating Proteolytic Activity on MRS Skim Milk Agar

    39

    FIGURE 4: DNA Bands of LABs on the 1.0% Agarose Gel 46

    FIGURE 5: The Effect of Lactose Concentration on PA and pH of Fermentation after 24 h at 37oC with L. casei-CF2

    74

    FIGURE 6: The Effect of Lactose Concentration on PA and pH of Fermentation after 48 h at 37oC with L. casei-CF2

    74

    FIGURE 7: The Effect of Lactose Concentration on PA and pH of Fermentation after 24 h at 37oC with E. faecium-FFB

    75

    FIGURE 8: The Effect of lactose Concentration on PA and pH of Fermentation after 48 h at 37oC with E. faecium-FFB

    75

    FIGURE 9: The Effect of Lactose Concentration on PA and the pH of Fermentation after 24 h at 37oC with L. plantarum-S

    76

    FIGURE 10: The Effect of Lactose Concentration on PA and the pH of Fermentation after 48 h at 37oC with L. plantarum-S

    76

    FIGURE 11: Time-kill Curve of GMCH-L. casei CF2 on Survival of (A) C. sakazakii ATCC 25944, (B) C. sakazakii O531G and (C) C. sakazakii E4 after 24 h Fermentation at 30oC

    78

    FIGURE 12: Time-kill Curve of GMCH-L. casei CF2 on Survival of (A) C. sakazakii ATCC 25944, (B) C. sakazakii O531G and (C) C. sakazakii E4 after 48 h Fermentation at 30oC

    79

    FIGURE 13: Time-kill Curve of GMCH-E. faecium F.F.B on Survival of (A) C. sakazakii ATCC 25944, (B) C. sakazakii O531G and (C) C. sakazakii E4 after 48 h Fermentation at 30oC

    80

  • ii

    FIGURE 14: Time-kill Curve of GMCH-L. plantarum S on Survival of (A) C. sakazakii ATCC 25944, (B) C. sakazakii O531G and (C) C. sakazakii E4 after 48 h Fermentation at 30oC

    81

  • iii

    LIST OF APPENDICES

    Page

    APPENDIX A Partial sequence of LAB isolates DNA (A): L. casei CF2, (B): E. faecium F.F.B and (C): L. plantarum S.

    137

    APPENDIX B Figure 1: Amino acid composition profile of GMCH fermented by LAB at 37oC (A): standard amino acids, (B): Control GMC, (C): L. casei CF2 and (D): E. faecium F.F.B, E: L. plantarum S.

    140

    APPENDIX C ANOVA Output for the Effect of LAB, Fermentation Time and Lactose Concentration on Proteolytic Activity

    143

    APPENDIX D Least mean Square Comparison for pH and Antimicrobial Activity of GMCH

    144

    APPENDIX E ANOVA Output for the Effect of GMCH, GMCH Concentration and Time on the Inhibitory Activity Against Cronobacter spp.

    145

    APPENDIX F Least Mean Square Comparison for pH and Antimicrobial Activity of GMCH

    146

    APPENDIX G ANOVA Output for the Effect of GMCH, GMCHC and Kill-Time on the Inhibitory Activity Against Cronobacter spp.

    147

  • iv

    LIST OF ABBREVIATIONS AND SYMBOLS

    C degree celsius

    l microliter

    m micrometer

    ACE angiotensin-I converting enzyme

    AMPs antimicrobial peptides

    BMC bovines milk caseinate

    bp base pair

    CaCO3 Calcium carbonate

    CCl3COOH trichloroacetic acid

    CEP cell envelop-associated proteinase

    CFU colony-forming unit

    CH3COONa sodium acetate

    CH3COONa.3H2O sodium acetate trihydrate

    cm centimeter

    CPPs calcium-binding phosphopeptides

    dH2O distilled water

    ddH2O double-distilled water

    DNA deoxyribonucleic acid

    FeSO4.7H2O iron (II) sulfate heptahydrate

    FT fermentation time

    g gram

    GABA - aminobutyric acid

    GI gastrointestinal

    GMC goats milk casein

    GMCH goats milk casein hydrolysate

    GMCHs goats milk casein hydrolysates

    GMP glycomacropeptide

  • v

    h hour

    H2O water

    HCl hydrochloric acid

    IFM Infant formula milk

    LAB lactic acid bacteria

    LC lactose concentration

    M mole

    mg milligram

    MgSO4.7H2O magnesium sulfate

    min minute

    ml milliliter

    mm millimeter

    mM millimole

    MnSO4.H2O manganese (II) sulfate monohydrate

    MRS Man, Rogosa and Sharpes

    Na2CO3 sodium carbonate NaCl sodium chloride

    NaOH sodium hydroxide

    ng nanogram

    nm nano meter

    OPA O-phthalaldehyde

    PA Protease activity assay

    PBS phosphate-buffer saline

    PCR polymerase chain reaction

    pmole picomole

    RC regenerated cellulose

    RNA ribonucleic acid

    sec second

    TCA trichloroacetic acid

    u unit

    UV ultraviolet

  • vi

    v/v volume/volume

    w/v weight/volume

    -la -lactalbumin

    -lg -lactoglobulin

    g microgram

  • 93

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