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Role of Epiphytic Bacteria in the Colonization of Fruits And

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Role of Epiphytic Bacteria in the Colonization of Fruits And ROLE OF EPIPHYTIC BACTERIA IN THE COLONIZATION OF FRUITS AND LEAFY GREENS BY FOODBORNE BACTERIAL PATHOGENS A Dissertation by MARIANA VILLARREAL SILVA Submitted to the Office of Graduate and Professional Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Chair of Committee, Alejandro Castillo Committee Members, Gary R. Acuff Elsa A. Murano Leon H. Russell Head of Department, Boon Chew August 2016 Major Subject: Food Science and Technology Copyright 2016 Mariana Villarreal Silva ABSTRACT The epiphytic bacteria content in fruits and leafy greens and their effect toward the colonization of foodborne bacterial pathogens was studied. Populations of mesophilic, lactic acid, coliform, and psychrotrophic bacteria were recovered from cantaloupe, tomato, pepper, spinach, endives, and parsley, and the effect of environmental and agricultural conditions toward epiphytic bacteria content was evaluated. The epiphytic bacteria content was variable by commodity, with cantaloupes and spinach being the most populated commodities. The environmental temperature and the irrigation method also affected the epiphytic bacteria content. To determine the inhibitory effect of epiphytic bacteria toward Escherichia coli O157:H7 and Salmonella enterica serovar Saintpaul, 9,307 isolates were evaluated in vitro. In total, 2.6, 0.7 and 6.4% of the isolates were antagonistic toward E. coli O157:H7, S. Saintpaul, or both pathogens, respectively. Most antagonistic isolates were psychrotrophs and lactic acid bacteria. Overall, more antagonistic isolates from fruits were found in samples collected in the fall than the summer. Further biochemical identification revealed that most of the antagonistic psychrotrophs were Alcaligenes faecalis sbsp. faecalis. In fruits, most of the antagonistic isolates were Leuconostoc, Enterococcus, and Streptococcus species. Furthermore, the effect of epiphytic bacteria toward S. Saintpaul growth in fruits and toward E. coli O157:H7growth in leafy green leaves was studied in the plant surface. Enterococcus kobei and Enterococcus casseliflavus from cantaloupe, and of Staphylococcus hominis subsp. hominis from tomato inhibited S. Saintpaul on cantaloupe rind, and tomato skin, respectively. Similarly, ii Enterococcus faecalis affected S. Saintpaul on peppers and Gemella morbillorum, Enterococcus gallinarum, and Bacillus mycoides affected E. coli O157:H7 growth on parsley. The effect of Streptococcus alactolyticus, Bacillus licheniformis, Gemella bergeri, Staphylococcus sciuri, and Enterococcus gallinarum toward E. coli O157:H7 growth and stomata invasion in endives was observed using confocal microscopy. After 24 h, E. coli O157:H7 growth was moderately inhibited by all epiphytic isolates tested. However, after three days, treated and control samples presented similar pathogen growth. The results from this study demonstrated that some epiphytic bacteria from fruits and leafy greens are potential biocontrol agents, able to reduce the proliferation of E. coli O157:H7 and S. enterica in fruits and vegetables. iii DEDICATION To my husband and best friend, Jorge, I am forever thankful for your love, patience, and support throughout these years. To Jacobo, my son, and my motivation, full of smiles. For him, I hope curiosity will lead his path, open his mind, brighten his spirit, and amuse him with every discovery he finds. To my mom, Belia, and my dad, César, who taught me to reach for better things, to work hard, to give everything I have, and to never give up. To Marcela and Paulina, my sisters and best friends, and to my handsome nephews, whose hearts are close and endlessly connected to mine despite the long distance. iv ACKNOWLEDGEMENTS I want to extent my gratitude to my advisor, and committee chair, Dr. Alejandro Castillo, for the opportunity to pursue a doctoral degree and for his advice and support during my graduate studies, and to my committee members, Dr. Elsa Murano, Dr. Gary Acuff, and Dr. Leon Russell, for their willingness to help me throughout my research. I also want to thank to Dr. Elisa Cabrera, and Mrs. Lisa Lucia for their support and expertise advice, but most importantly for their friendship. I also want to thank to Ana M., Alexandra, Keila, Mary Pía, Grihalakshmi, and Verónica, for always being there, during uncountable hours in the laboratory, and for all the moments shared. I want to express my gratitude to all my friends, especially to Alana, Amie Marie, Andrea, Andrés, Ayoola, Fanny, Jennifer, Jessie, Katie, Kathy Jo, Marco, Matt, Megha, Noo, Noushin, Sara, Sofía, Tanita, Tamra, Wendy, and Zahra, for their support, solidarity, and technical assistance. I also want to thank to Dr. Juan Anciso and Ashley Gregory for the samples, to Dr. Joseph Sturino for the LAB control strains, to Dr. Roula Barhoumi for her assistance with the confocal microscope, to Ana Mercado for the S. Saintpaul growth curve data, and to Veronica Arias for the growth curve analyses. Finally, I want to thank to the National Council in Science and Technology (CONACyT) of Mexico for the academic financial support and to the National Institute of Food and Agriculture, NIFA-USDA, for funding the present research. v NOMENCLATURE AMP Ampicillin APT All-purpose media containing Tween 80 CL Coliform GFP Green fluorescent protein IA Inhibition area(s) IPTG Isopropyl β-D-1 thyogalactoside ivAEB in-vitro antagonistic, epiphytic bacteria LAB Lactic Acid Bacteria MRS De Man, Rogosa, and Sharpe medium MS Mesophile PBS Phosphate buffer solution PW Peptone water PY Psychrotroph RIF Rifampicin STEC Shiga-toxin producing Escherichia coli TSA Tryptic soy agar medium TSB Tryptic soy broth medium VRBA Violet red bile agar medium. vi TABLE OF CONTENTS Page ABSTRACT .......................................................................................................................ii DEDICATION .................................................................................................................. iv ACKNOWLEDGEMENTS ............................................................................................... v NOMENCLATURE .......................................................................................................... vi TABLE OF CONTENTS .................................................................................................vii LIST OF FIGURES ............................................................................................................ x LIST OF TABLES ...........................................................................................................xii INTRODUCTION .............................................................................................................. 1 REVIEW OF LITERATURE ............................................................................................. 4 Leafy green production .................................................................................................. 4 Spinach (Spinacia oleracea) ....................................................................................... 4 Curly endive (Cichorium endivia) .............................................................................. 7 Parsley (Petroselinum crispum) .................................................................................. 8 Fruit production .............................................................................................................. 9 Cantaloupe (Cucumis melo var. cantaloupensis) ...................................................... 10 Tomato (Solanum lycopersicum) .............................................................................. 11 Pepper (Capsicum annuum) ...................................................................................... 13 Contributing factors during the contamination with foodborne pathogens in fruits and vegetables .............................................................................................................. 15 Pre-harvest contamination ........................................................................................ 15 Post-harvest contamination ....................................................................................... 19 Prevention of produce contamination .......................................................................... 22 Worldwide impact of fruit and vegetable foodborne pathogen contamination ............ 24 Current surge of foodborne disease outbreaks related to fruits and vegetables ........... 27 Important foodborne outbreaks related to leafy greens ............................................ 28 Important foodborne outbreaks related to fruits ....................................................... 29 Pathogens linked to foodborne outbreaks in fruits and vegetables .............................. 31 Escherichia coli O157:H7 ........................................................................................ 32 Salmonella enterica .................................................................................................. 37 Factors involved in the pathogen colonization of produce .......................................... 43 Electrostatic forces and hydrophobicity ................................................................... 43 vii Plant-associated microbiota ...................................................................................... 45 Environmental factors ............................................................................................... 46 Pathogen-inherent factors
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