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Open Capasso2016dissf.Pdf The Pennsylvania State University The Graduate School College of Agricultural Sciences ANTIBIOTIC RESISTANCE IN PENNSYLVANIA STONE FRUIT ORCHARDS A Dissertation in Plant Pathology by Sarah J. Capasso © 2016 Sarah J. Capasso Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy May 2016 ii The dissertation of Sarah Capasso was reviewed and approved* by the following: María del Mar Jiménez Gasco Associate Professor of Plant Pathology Dissertation Advisor Chair of Committee Beth K. Gugino Associate Professor of Vegetable Pathology Gary W. Moorman Professor Emeritus of Plant Pathology Kari A. Peter Assistant Professor of Tree Fruit Pathology Mary Ann Victoria Bruns Associate Professor of Soil Science/Microbial Ecology Carolee T. Bull Professor of Plant Pathology and Systematic Bacteriology Head of the Department of Plant Pathology and Environmental Microbiology *Signatures are on file in the Graduate School iii ABSTRACT Bacterial spot (caused by Xanthomonas arboricola pv. pruni) is the most important bacterial disease of peach and nectarine in the eastern United States. The antibiotic oxytetracycline is used to mitigate the yield limiting symptoms of this disease. Despite that, yield loss remains high in susceptible stone fruit cultivars, raising concern among growers over the development of antibiotic resistance in the causal pathogen. Previous surveys of the stone fruit orchard bacterial community indicated the presence of oxytetracycline resistant epiphytic bacteria. This was significant because epiphytic or nontarget bacteria are thought to harbor more resistance genes and often before coexisting pathogens. Under a strong selection pressure such as repeated antibiotic applications, transfer of resistance genes from epiphytic bacteria to pathogenic bacteria is favored. Therefore, when evaluating antibiotic resistance development in pathogenic bacteria, nontarget bacteria must also be considered. The overall goal of this research was to determine the consequences of repeated oxytetracycline applications in commercial Pennsylvania stone fruit orchards, including management factors related to the incidence of bacteria carrying tetracycline resistance genes and the sensitivity of X. arboricola pv. pruni isolates to oxytetracycline. Tetracycline resistance genes, tet(A), tet(B), and tet(C), were found in epiphytic bacteria recovered from commercial stone fruit orchards and research blocks at the PSU Fruit Research and Extension Center. The most common carriers of these resistance genes were bacteria that belonged to the genera Pantoea and Pseudomonas where tet(B) was most commonly associated with the former and tet(C), the latter. Bacteria carrying these tetracycline resistance genes could grow on media amended with greater than 450 ug/ml of oxytetracycline, three times that of the rate used in the field to manage bacterial spot. While iv the incidence of tetracycline resistance genes in epiphytic bacteria significantly differed (P > 0.0001) among the sampled commercial orchards, this was not related to oxytetracycline use (P = 0.0855). When tested in the experimental stone fruit blocks, again, the distribution of bacteria positive for tetracycline resistance genes was not related to bactericide treatment (2013: P = 0.407; 2014: P = 0.520). Other management factors including tree age, cultivar, and sampling date were. Sensitivity to oxytetracycline among Xap isolates significantly differed (P > 0.0001) among those collected from commercial stone fruit orchards. While no tetracycline resistance genes were found in any of the sampled Xap isolates and overall sensitivity remained high (MIC < 25 µg/ml), oxytetracycline use was a significant factor associated with oxytetracycline sensitivity (P > 0.0001). Further research should be conducted to determine the molecular mechanism associated with the variability in sensitivity in the Xap isolates, including novel and untested resistance genes, adaptive resistance, or mutation. v TABLE OF CONTENTS LIST OF TABLES ....................................................................................................... vii LIST OF FIGURES ..................................................................................................... viii ACKNOWLEDGEMENTS ......................................................................................... x Chapter 1 Introduction ..............................................................................................1 Bacterial Spot of Stone Fruit in the Eastern United States…………………….1 Disease Significance ......................................................................................1 Symptoms and Disease Development .............................................................2 Causal Organism ...........................................................................................6 Disease Management .....................................................................................8 Use of Antibiotics in Agriculture .......................................................................10 Antibiotic Resistance ..........................................................................................11 Mechanisms of Resistance .............................................................................13 Tetracycline Resistance .................................................................................13 Bacterial Diversity of the Phyllosphere ..............................................................16 Research Goals and Objectives ..........................................................................19 Justification .........................................................................................................20 Literature Cited ...................................................................................................23 Chapter 2 Tetracycline resistance genes in epiphytic bacteria collected from Pennsylvania stone fruit orchards ..............................................................................34 Abstract ...............................................................................................................34 Introduction .........................................................................................................35 Materials and Methods .......................................................................................37 Results.................................................................................................................42 Discussion ...........................................................................................................45 Literature Cited ...................................................................................................52 Chapter 3 The effects of bactericide use on bacterial epiphytes for the management of bacterial spot in Pennsylvania stone fruit orchards ...................65 Abstract ...............................................................................................................65 Introduction .........................................................................................................66 Materials and Methods .......................................................................................70 Results.................................................................................................................76 Discussion ...........................................................................................................80 Literature Cited ...................................................................................................86 vi Chapter 4 Oxytetracycline sensitivity of Xanthomonas arboricola pv. pruni isolates collected from Pennsylvania stone fruit orchards ..................................101 Abstract ...............................................................................................................101 Introduction .........................................................................................................101 Materials and Methods .......................................................................................104 Results.................................................................................................................107 Discussion ...........................................................................................................110 Literature Cited ...................................................................................................117 Chapter 5 Discussion ................................................................................................126 Literature Cited ...................................................................................................134 Appendix ....................................................................................................................139 vii LIST OF TABLES Table 2-1: Oxytetracycline sensitivity of bacterial epiphytes with different tetracycline resistance genes ..................................................................................................58 Table 2-2: Orchard management factors associated with recovery of epiphytic bacteria from Pennsylvania orchards positive for tetracycline resistance genes ..............59 Table 3-1: 2013 evaluation of bacterial spot incidence and severity on leaves and fruit on 'Beekman' and 'Snow King' in the FREC block .............................................89 Table 3-2: 2014 evaluation of bacterial spot incidence and severity
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