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Role of Exopolymeric Substances in Biofilm Formation on Dairy Separation Membranes Nuria Garcia-Fernandez South Dakota State University

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Role of Exopolymeric Substances in Biofilm Formation on Dairy Separation Membranes Nuria Garcia-Fernandez South Dakota State University South Dakota State University Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange Theses and Dissertations 2016 Role of Exopolymeric Substances in Biofilm Formation on Dairy Separation Membranes Nuria Garcia-Fernandez South Dakota State University Follow this and additional works at: https://openprairie.sdstate.edu/etd Part of the Dairy Science Commons Recommended Citation Garcia-Fernandez, Nuria, "Role of Exopolymeric Substances in Biofilm Formation on Dairy Separation Membranes" (2016). Theses and Dissertations. 958. https://openprairie.sdstate.edu/etd/958 This Dissertation - Open Access is brought to you for free and open access by Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange. For more information, please contact [email protected]. ROLE OF EXOPOLYMERIC SUBSTANCES IN BIOFILM FORMATION ON DAIRY SEPARATION MEMBRANES BY NURIA GARCIA-FERNANDEZ A dissertation submitted in partial fulfillment of the requirements for the Doctor of Philosophy Major in Biological Sciences Specialization in Dairy Science South Dakota State University 2016 iii To my family. iv ACKNOWLEDGEMENTS This investigation was completed at the Department of Dairy Science of South Dakota State University under the co-guidance of Drs. Ashraf Hassan and Sanjeev Anand. I want to acknowledge the Midwest Dairy Research Center and the Agricultural experiment station of SDSU for sponsoring my assistantship and for funding this project. I would like to gratefully and sincerely thank Dr. Ashraf Hassan, for giving me the opportunity to join his group and starting this investigation, his teaching about biofilms and exopolysaccharides was generous, always providing stimulating challenges, and inspiring me to chase original paths without fear to fail or make mistakes. I also want to express my appreciation to Dr. Sanjeev Anand, for always having his door open for my questions, and his guidance during my beginning stages providing new ideas and thoughts on my biofilm research work, and during final stages of compilation, and writing this dissertation. I thank Dr. Lloyd Metzger and Dr. Vikram Mistry for participating in my Advisory Committee, challenging me with technical and philosophical questions and interpretations that enhanced my critical thinking. I am also grateful for the advice received by Dr. Fathi Halaweish on analytical methods for characterization of exopolymeric material, and protein purification. I thank my lab mates for making lab work very enjoyable. It sure was fun to get to know so many international cultures and traditions. v Lastly but by no means least, I thank my dear husband, Fernando, for his unconditional support and encouragement throughout this time without which this research would not have been completed. vi CONTENTS ABSTRACT xi CHAPTER 1. INTRODUCTION AND BACKGROUND INFORMATION 1 1. Dairy processing membranes 1 2. The problem of biofilms on filtration membranes 3 3. Mechanisms of bacterial adhesion 5 3.1 Cell / substrate surface characteristics 5 3.2 Biopolymers as adhesives 7 4. EPS producing cultures in the dairy industry 8 5. Slime-producing endospore forming bacilli in the dairy industry 9 6. Characterization of microbial exopolymeric substances (EPS) 12 6.1 Methods of isolation and purification of bacterial EPS 12 6.2 Methods of analysis of bacterial EPS 14 6.2.1 Analysis of total carbohydrate content and total protein content of EPS 14 6.2.2 Monosaccharide analysis 15 6.2.3 Amino acid analysis 18 7. Control strategies for biofilm formation of RO membranes 19 7.1. Cleaning-in-place procedures (CIP) 19 7.2. Antimicrobial approach to inactivate the embedded cells 21 7.3. Enzymatic degradation of the biofilm matrix 22 CHAPTER 2. ROLE OF EXOPOLYSACCHARIDES PRODUCED BY DAIRY STARTER CULTURES IN FORMATION OF WHEY CONCENTRATION MEMBRANE BIOFILMS 24 Abstract 24 Introduction 25 Materials and methods 27 Source of EPS producing bacteria and other cultures 27 Selection of the EPS(−) mutants 27 vii Preparation of RO membranes for in vitro biofilm studies 28 Study of attachment and biofilm formation 29 Microscopic observations 29 Transmission Electron Microscopy (TEM) observation of bacterial cell surface structures. 30 Confocal Laser Scanning Microscopy (CLSM) observation of bacterial capsules 30 Scanning Electron Microscopy (SEM) observations of biofilms on RO membranes. 31 Cell surface hydrophobicity 31 Zeta-potential of bacterial cells 32 Influence of EPS producing cultures on biofilm formation by potential food pathogens 33 Effects of surfactants on cell attachment and biofilm formation 33 Statistical analysis 34 Results 35 Study of attachment and biofilm formation 35 Cell surface hydrophobicity and charge 35 Microscopic observations 36 Influence of EPS producing cultures on biofilm formation by potential food pathogens 37 Effects of surfactants on cell attachment and biofilm formation 37 Discussion 38 Evaluation of attachment and biofilm formation as affected by EPS production 38 Influence of EPS on biofilm formation by potential food pathogens 39 Role of hydrophobicity on cell attachment and biofilm formation by EPS producing bacteria 40 Conclusions 42 Tables and Figures 43 viii CHAPTER 3. INFLUENCE OF SLIME PRODUCED BY BACILLUS SPP. ON MEMBRANE BIOFILM FORMATION 54 Abstract 54 Introduction 55 Materials and methods 56 Source of bacterial cultures 56 Selection of slime-negative mutants 57 Attachment and biofilm development on RO membranes 58 Evaluation of biofilm formation 58 Study of the role of slime production on biofilm formation 59 Modification of cell surface hydrophobicity by surfactants 60 Characterization of the slime of Bacillus strains 61 Statistical analysis 63 Results 63 Attachment and biofilm formation by slime-producing Bacillus strains 63 Hydrophobicity and surface charge 63 Microscopic observations 65 Bacillus slime composition 65 Discussion 67 Conclusions 73 Tables and Figures 75 CHAPTER 4. A NOVEL APPLICATION OF A FUNGAL CATALASE PREPARATION TO CONTROL SPORE-FORMING BACTERIA IN THE DAIRY INDUSTRY 84 Abstract 84 Introduction 85 Materials and methods 87 Bacterial strains 87 Enzymes 87 Spore preparation 88 ix Inhibition of spores in milk 88 Agar diffusion test on vegetative cells 89 Determination of MIC by microdilution testing 90 Effect of catalase on biofilm formed by slime-producing Bacillus 90 Characterization of the antimicrobial activity 92 Effect of heat on the antimicrobial properties of catalase 92 Sporostatic test 93 Identification of the major proteins of Cat preparations 93 Results 94 Inhibition of spores in milk 94 Determination of the MIC of Cat 95 Effect of catalase on biofilm formed by slime-producing Bacillus 96 Characterization of the antimicrobial activity 96 Discussion 97 Conclusions 101 Tables and Figures 102 CHAPTER 5. EVALUATION OF NATURAL DEPOLYMERASES ISOLATED FROM BACTERIOPHAGES AND BACTERIA ON DISRUPTING THE BIOFILM MATRIX – A PROOF OF CONCEPT 116 Abstract 116 Introduction 118 Materials and methods 120 Isolation of bacteriophages infecting EPS degrading bacteria 120 Partial purification of EPS degrading enzymes from bacteriophages 121 Application of crude enzymes from bacteriophages 122 Application of crude enzymes from EPS producing culture after long fermentation 124 Application of crude enzymes from amylolytic bacteria to biofilms formed on RO membranes 125 Statistical analysis 127 x Results and discussion 127 Bacteriophage crude-enzymes 127 Depolymerases from EPS producing culture that degrades its own EPS 129 Application of crude enzymes from amylolytic Bacillus strain to biofilms formed on RO membranes 132 Conclusions 133 Tables and Figures 135 CHAPTER 6. SUMMARY AND CONCLUSIONS 141 BIBLIOGRAPHY 147 xi ABSTRACT ROLE OF EXOPOLYMERIC SUBSTANCES IN BIOFILM FORMATION ON DAIRY SEPARATION MEMBRANES NURIA GARCIA-FERNANDEZ 2016 In the concentration of cheese whey by membrane filtration processes, fouling is a major limiting factor that leads to flux decline and affects product quality. The growth of biofilms on membranes contributes to biofouling. Biofilms are very difficult to eliminate, and will serve as the seed for additional biofilm development and product contamination. The biofilm matrix is composed mainly of microbial exopolymeric substances (EPS), and therefore EPS is thought to help bacteria to adhere and form biofilms by acting as a cementing agent. The first research project under this study was conducted with the aim of elucidating the role of the EPS produced by lactic acid starter cultures on reverse osmosis (RO) membranes. A second study was designed to investigate the role of EPS produced by spore forming bacteria on RO membrane biofilms. A third study was conducted to evaluate the application of Catalase (Cat) on spores and biofilms formed by spore forming bacteria that produce EPS. Finally, the fourth study evaluated the application of natural depolymerases from bacteriophages and bacteria to disrupt biofilms. In the first research project we observed that the EPS of Streptococcus thermophilus strain 3534 enhanced biofilm formation but the EPS of Lactococcus lactis ssp. cremoris strain JFR inhibited the attachment and biofilm formation to RO membranes. This was associated to the cell-surface hydrophobicity of the strains, which xii was affected by the EPS production. In the second study a greater biofilm
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