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Routes to Food Spoilage — Salt Fungi and a New Apple Disease, Paecilomyces Rot

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Routes to Food Spoilage — Salt Fungi and a New Apple Disease, Paecilomyces Rot ROUTES TO FOOD SPOILAGE — SALT FUNGI AND A NEW APPLE DISEASE, PAECILOMYCES ROT A Dissertation Presented to the Faculty of the Graduate School of Cornell University In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by Megan Nicole Biango-Daniels May 2018 © 2018 Megan Nicole Biango-Daniels ROUTES TO FOOD SPOILAGE — SALT FUNGI AND A NEW APPLE DISEASE, PAECILOMYCES ROT Megan Nicole Biango-Daniels, Ph. D. Cornell University 2018 Extremophilic fungi have surprising powers, surviving and growing under inhospitable conditions including high salinity and high temperatures. These abilities make them formidable enemies in food and agricultural environments. Considering these fungi as a continuum in both environments offers a novel way to examine problems that can arise in the field and end on the shelf. Challenging long-held notions about where spoilage fungi can originate, sea salts were examined as potential sources of low water activity spoilage fungi and were found to contain spoilage-species of Aspergillus, Penicillium, and Cladosporium. Exploring another group of extreme fungi, the farm-to-food transmission route of the heat-resistant spoilage mold, Paecilomyces niveus (Byssochlamys nivea) was elucidated. It was found in a third of New York orchard soils sampled. Experimental inoculations demonstrated its ability to cause a postharvest disease of apples in accordance with Koch’s postulates. The disease was later demonstrated on developing fruit in apple orchards. The newly described disease, Paecilomyces rot, caused by P. niveus presents with symptoms including circular, concentrically-ringed, brown lesions. Its firm, U-shaped internal rot resembles other fungal apple diseases. Importantly, Paecilomyces niveus was observed to produce its heat-resistant ascospores inside apples. When infected apples were used to make juice concentrate using common industry protocols, with stringent thermal processing, some ascospores survived in the finished product. The results suggest that when lesser-quality apples, infected with P. niveus, are used to make concentrate they may introduce spoilage inoculum as well as patulin, the most significant apple mycotoxin. To evaluate control methods for this new disease in the field, the efficacy of EC50 concentrations of difenoconazole, fludioxonil, and pyrimethanil, three active ingredients in fungicides, were tested on thirty P. niveus isolates. Cultures from agricultural environments, likely to have been previously exposed to fungicides, were found to be less sensitive than cultures from environments, such as food, where prior exposure was unlikely. Although resistance does not appear to be widespread, the exposed isolates were significantly less sensitive to fludioxonil. Future research should explore the spoilage implications of this apple disease, its incidence and etiology, and its control before and after harvest. BIOGRAPHICAL SKETCH A native of the Ithaca area, Megan N. Biango-Daniels received her B.S. in Biology with a concentration in Ecology, Evolution, and Behavior from Binghamton University before coming to Cornell. In her free time, she likes to write haikus. Cold rain, hot coffee. Warm autoclave hisses “Good morning” heat and pressure waiting. Plastic pipette tips, their clear, blue, or yellow tips filtered and empty. Microscope light glows, glass coverslip pressed over. Clipped in place on stage. v To Christopher & To all the people who inspire me but will never read this. vi ACKNOWLEDGMENTS I am grateful for the support of all my family and friends. I would like to thank my advisor Kathie Hodge for showing me what it means to be an excellent scientist, teacher, and mentor. I am grateful to my entire committee: Randy Worobo, Eric Nelson, and Kerik Cox for their constant encouragement, advice, and support. I would like to thank the Royall T. Moore fund and Plant Pathology and Plant-microbe Biology department for supporting my work. I love this department and consider myself privileged to have worked alongside its faculty, who constantly inspire me. One person, who I want to recognize for always making time to talk with and mentor me is George Hudler; reading his book inspired me to study fungi and I never imagined that I’d be lucky enough to pick his brain. I am grateful to Cornell Cooperative Extension agents, apple consultants, and orchard owners for their help in soil sampling. I would like to thank Cornell University Orchards for their support of this work, and Erika Mudrak of the Cornell Statistical Consulting Unit for her assistance with data analysis. My work was supported by the USDA National Institute of Food and Agriculture, Hatch project 1002546, and by the Cornell CALS Arthur Boller Apple Research Grant. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the National Institute of Food and Agriculture (NIFA) or the United States Department of vii Agriculture (USDA). viii TABLE OF CONTENTS BIOGRAPHICAL SKETCH v DEDICATION vi ACKNOWLEDGMENTS vii LIST OF TABLES xi LIST OF FIGURES xii LIST OF ILLUSTRATIONS xiv Chapter 1: SEA SALTS AS A POTENTIAL SOURCE OF FOOD SPOILAGE FUNGI INTRODUCTION 1 MATERIALS AND METHODS 2 RESULTS 7 DISCUSSION 15 ACKNOWLEDGMENTS 19 REFERENCES 20 CHAPTER 2: PAECILOMYCES ROT: A NEW APPLE DISEASE INTRODUCTION 28 MATERIALS AND METHODS 30 RESULTS 42 DISCUSSION 50 ACKNOWLEDGMENTS 55 REFERENCES 56 CHAPTER 3: SURVIVAL OF PAECILOMYCES NIVEUS IN APPLE JUICE CONCENTRATE MADE FROM FRUIT WITH PAECILOMYCES ROT INTRODUCTION 63 MATERIALS AND METHODS 67 RESULTS 73 DISCUSSION 75 ACKNOWLEDGMENTS 78 REFERENCES 79 ix CHAPTER 4: PAECILOMYCES NIVEUS: PATHOGENICITY IN THE ORCHARD AND SENSITIVITY TO THREE FUNGICIDES INTRODUCTION 86 MATERIALS AND METHODS 89 RESULTS 97 DISCUSSION 103 ACKNOWLEDGMENTS 107 REFERENCES 108 x LIST OF TABLES Table 1.1: Identities of fungi isolated from seven commercially available 8 salts. Table 2.1: Isolates and accession numbers used in phylogenetic analyses. 33 Table 2.2: Origin information for P. niveus isolates from soil in New York 45 orchards. Table 4.1: Origin information for exposed and baseline P. niveus isolates 90 used to characterize fungicide sensitivity with the NCBI accession numbers for their BenA region sequence. xi LIST OF FIGURES Figure 1.1: The number of fungi in each of the seven salts, organized by 13 ocean of origin. Figure 1.2: The total number of fungal isolates from the combined 14 subsamples of each salt, with colors representing the different taxa. Figure 1.3: The global distribution of fungi across subsamples grouped by 15 ocean of origin of salts (Atlantic or Pacific). Figure 2.1: Phylogenetic tree of concatenated partial β-tubulin and ITS 43 sequences of 31 taxa, including Paecilomyces niveus (Byssochlamys nivea) isolate CO7, rooted with Thermoascus crustaceus as an outgroup. Figure 2.2: Phylogenetic tree of partial β-tubulin sequences of 47 taxa, 44 including Paecilomyces niveus (Byssochlamys nivea) isolates from New York orchards, rooted with Thermoascus crustaceus as an outgroup. Figure 2.3: Increase in the mean diameter of lesions inoculated with 50 Paecilomyces niveus (Byssochlamys nivea) compared to the mean diameter of mock-inoculated control wounds on ‘Gala’ and ‘Golden Delicious’ apples. Figure 3.1: The mean colony forming units per liter of P. niveus from 74 samples taken throughout the apple juice concentrate process. Figure 3.2: Representative images of P. niveus spore and the concentration 74 of ascospores observed throughout the apple juice concentrate process. Figure 3.3: The patulin concentration in single strength cider made from 75 mock-inoculated apples and throughout the apple juice concentrate process of concentrate made from apples with Paecilomyces rot. Figure 4.1: Phylogenetic relationships of P. niveus isolates from this study 98 to related species, rooted with Thermoascus crustaceus as an outgroup. Figure 4.2: The diameter of inoculated and mock-inoculated lesions on 99 orchard inoculated ‘Gala’ apples at harvest. Figure 4.3: Boxplot showing the median percent relative growth after one 100 week of baseline and exposed P. niveus isolates at adjusted mean EC50 concentrations of fungicides. xii Figure 4.4: Heatmap of relationships among exposed and baseline P. 102 niveus isolates based on percent relative growth at EC50 concentrations of difenoconazole, fludioxonil, and pyrimethanil. xiii LIST OF ILLUSTRATIONS Illustration 2.1: Representative images of post-harvest disease symptoms 47 caused by Paecilomyces niveus (Byssochlamys nivea) on ‘Gala’ and ‘Golden Delicious’ apples. Illustration 2.2: Representative image of Paecilomyces niveus 48 (Byssochlamys nivea) asci containing ascospores, observed in the cores of infected apples. Illustration 3.1: Representative images of a ‘Gala’ apple with post-harvest 68 Paecilomyces rot. Illustration 3.2: Diagram of the apple juice concentrate process used to 69 make concentrate from apples with Paecilomyces rot. Illustration 4.1: Representative image of an inoculated ‘Gala’ apple, 94 showing how roundness was measured. Illustration 4.2: Representative image of symptoms of Paecilomyces Rot on 99 ‘Gala’ inoculated in the orchard. Illustration 4.3: Representative images of the mesocarp of inoculated ‘Gala’ 100 apples showing unique symptoms of Paecilomyces rot in the orchard. xiv CHAPTER 1 SEA SALTS AS A POTENTIAL SOURCE OF FOOD SPOILAGE FUNGI1 INTRODUCTION Valued for their nuanced taste and texture and their often artisanal origins,
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