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The Application of Culture-Independent Methods in Microbial Assessment of Quality and Safety Risk Factors in Swiss Cheese and Oysters Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Qianying Yao, B.S. Graduate Program in Food Science and Technology The Ohio State University 2016 Dissertation Committee: Dr. Hua Wang, advisor Dr. Lynn Knipe Dr. Melvin Pascall Dr. Zhongtang Yu Copyright by Qianying Yao 2016 Abstract Unwanted microorganisms greatly affect the quality and safety of the final food products. For instance, besides foodborne pathogens, quality defects in Swiss cheese ranging from unusual eyes, splits, off-flavors, to off-odors result in an estimated $24 million economic loss annually to the industry. Ohio has the largest Swiss cheese industry in the U.S., and to reveal microbial causative agents in Swiss cheese with quality defects has become a critical need to solve the problem for the industry. While conventional approaches were insufficient to identify the risk factors promptly and accurately, recent advancements in molecular techniques enabled in-depth investigation of potential causative agents and the development of rapid detection method for safety and quality control. To properly assess the split defect associated bacteria in Swiss cheese, a rapid detection platform for propionibacteria in dairy matrices was developed, and the microbial profiles of Swiss cheese with and without split defect were successfully evaluated. Results of these studies contributed to a comprehensive understanding of the microbial cause of split defect in Swiss cheese, enabled culture-independent methods in ii microbial assessment for dairy products, and illustrated the power of 16S metagenomics in improving fundamental understanding of the microbiology in Swiss cheese. In Chapter 1, an extensive literature review was conducted in terms of cheese quality and safety issues. With high nutritional values, Swiss cheese is a popular cheese type in the United States. The Swiss cheese microbiota consist of starter cultures and environmental microorganisms. The major safety risk in cheese is the contamination of pathogenic bacteria from raw milk or post-pasteurization handling. Non-pathogenic bacteria usually cause quality issues in cheese. Quite a few studies have been conducted on microbial identification and profiling in cheese using metagenomics. However, there is no study applying metagenomics to assessment of Swiss cheese safety and quality risks. In Chapter 2, a rapid detection system for Propionibacterium in food matrices were successfully developed. In this study, one pair of genus-specific primers targeting the 16S ribosomal RNA of the genus Propionibacterium, and four pairs of species- specific primers targeting different protein coding genes of P. freudenreichii, P. acidipropionici, P. acnes, P. avidum, were designed and evaluated. This detection system showed no cross-reactivity with other dairy-related bacteria, indicating its utility in dairy industry. In Chapter 3, the starter cultures and non-starter microbiota from split Swiss cheese blocks made by two different factories were analyzed. Result showed no significant difference in the relative abundance of starter cultures among split and non- split cheese, and the relative abundance of Enterobacteriaceae was significantly higher in iii split Swiss cheese than that of non-split samples, providing evidence that Enterobacteriaceae could be a microbial causing candidate for split defects. The difference in relative abundance of starter cultures in Swiss cheese made by two factories was observed, which could be due to different recipe in production. A comprehensive assessment of the bacterial profiles potentially associated with Swiss cheese quality made by one factory was conducted in this study. The microbial profile of retail cheese with eyes, factory-made Swiss cheese with and without split defects, pasteurized milk, and starter cultures were extensively analyzed by 16S metagenomics. The microbiota of Swiss cheese made in a local cheese factory showed consistency in both richness and diversity when compared to retail eye-forming cheese. The starter cultures were dominated by Streptococcus, Lactobacillus and Propionibacterium, and these genera were also dominant in Swiss cheese microbiota, while common commensal microbiota represented a very low proportion of the cheese microbiota. Using Principal Component Analysis and a heat map with dendrograms, it was demonstrated that the split areas in Swiss cheese were microbiologically different from eye areas, which could be due to inhomogeneous distribution of starter cultures. In Chapter 4, retail oysters as a potential channel disseminating antibiotic resistance was assessed. A total of nine oysters belong to three types were collected. High prevalence of culturable bacteria resistant to tetracycline, cefotaxime, lincomycin, gentamicin, ciprofloxacin and ceftazidime were investigated using Brain Heart Infusion, MacConkey and Phenylethyl Alcohol media. Meanwhile, shotgun metagenomics on iv oyster microbiota was conducted by extracting genomic DNA and high throughput sequencing using Hiseq platform. The microbial profile, functional metabolic groups, and antibiotic resistome were analyzed from the sequencing data using MG-RAST platform. High prevalence of multidrug-resistant and acriflavin-resistant genes were identified in oyster microbiota. Result from this study provided critical information on the application of culture- independent molecular techniques to identifying and addressing important food safety and quality challenges. v Dedication Dedicated to my parents, Guoqiang Yao and Ying Zhang for being a constant source of support throughout my lifetime. Dedicated to my husband Peipei Tang, for his endless love and unconditional support in every aspect of my life. vi Acknowledgement I would like to express my sincere gratitude to my advisor Dr. Hua Wang, who is the mentor throughout my graduate study. She provides me with insightful suggestions towards my research, as well as valuable advice towards my career path. I would also like to thank Drs. Lynn Knipe, Melvin Pascall, and Zhongtang Yu for their service on my candidacy and dissertation committee. The valuable suggestions from my committee were of great value to my research. Besides my committee members, I would also like to thank Dr. W James Harper. The project is impossible without him. I would also extend my gratitude to the former and present members of Dr. Wang’s Lab: Lu Zhang, Ying Huang, Yu Li, Yang Zhou, and Wenfei Wang, for sharing their professional knowledge as well as experience with me. I really enjoyed the happy days we spent together. I am grateful to China Scholarship Council for funding my stipend during my 4- year graduate study. Center for Innovative Food Technology, OARDC SEED for graduate students. vii Vita 2012…………………………………………B.S. Biological Sciences, Fudan University, Shanghai, China 2012 to present……………………………...PhD student, Graduate Research Associate, Department of Food Science and Technology, The Ohio State University Publications Presentations at conferences: Yao, Q and Wang, HH. (April 2016). Microbial Profiling Using 16S rDNA Metagenomics for Quality Assessment in Swiss Cheese. Poster presented at 2016 Ohio Agricultural Research and Development Center (OARDC) Annual Meeting. Wooster, OH Yao, Q and Wang, HH. (July 2015). Swiss cheese microbial quality assessment by 16S rDNA metagenomics. Poster presented at Institute of Food Technologists (IFT) 2015 Annual Meeting & Food Expo. Chicago, IL Yao, Q and Wang, HH. (April 2015). Microbial Profiling Using 16S rDNA Metagenomic Analysis for Swiss Cheese Assessment. Poster presented at 2015 Ohio Valley Institute of Food Technologists (OVIFT) Supplier’s Expo. West Chester, OH viii Yao, Q and Wang, HH. (June 2014). Rapid detection of Propionibacterium by 16S rDNA-targeted genus-specific PCR. Poster presented at 5th Ohio Valley Institute of Food Technologists (OVIFT) Symposium. Columbus, OH; and at Institute of Food Technologists (IFT) 2014 Annual Meeting & Food Expo. New Orleans, LA Fields of Study Major Field: Food Science and Technology ix Table of Contents Abstract…………………………………………………………………………………ii Dedication………………………………………………………………………………v Acknowledgement……………………………………………………………………….vi Vita………………………………………………………………………………………vii List of Tables…………………………………………………………………………...xiii List of Figures………………………………………………………………………xiv Chapter 1 Literature Background and Rationale of the Study 1.1 Introduction……………………………………………………………………...1 1.1.1 Bacteria in Swiss cheese production………………………………………3 1.1.2 Safety and quality challenges in Swiss cheese……………………………5 1.1.3 Microbial assessment 1.1.3.1 Research in propionibacteria identification in cheese matrices……..10 1.1.3.2 Culture-independent molecular techniques in studying bacterial community…………………………………………………………...11 x 1.1.3.2.1 Denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE)…...11 1.1.3.2.2 Terminal-restriction fragment length polymorphism (T- RFLP) ………………………………………………..12 1.1.3.2.3 Automated ribosomal intergenic spacer analysis (ARISA)……………………………………………...13 1.1.3.3 High-throughput sequencing and metagenomics in food microbial ecology…………………………………………….14 1.2 Seafood………………………………………………………………………16 1.2.1 Antibiotic resistance in the ecosystem…………………………...18 1.2.2 Culture-independent molecular techniques to study the
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