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The Greater Unseen: on the Identities, Distributions, and Impacts of Foliar Bacteria on Tropical Arboreal Species

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The Greater Unseen: on the Identities, Distributions, and Impacts of Foliar Bacteria on Tropical Arboreal Species THE GREATER UNSEEN: ON THE IDENTITIES, DISTRIBUTIONS, AND IMPACTS OF FOLIAR BACTERIA ON TROPICAL ARBOREAL SPECIES by Eric Anthony Griffin B.S., Berry College, 2008 Submitted to the Graduate Faculty of the Kenneth P. Dietrrich School of Arts and Sciences in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Pittsburgh 2016 UNIVERSITY OF PITTSBURGH Kenneth P. Dietrich School of Arts and Sciences This dissertation was presented by Eric Anthony Griffin It was defended on April 20, 2016 and approved by Dr. Nathan Morehouse, Dpt. of Biological Sciences, University of Pittsburgh Dr. Jonathan Pruitt, Dpt. of Ecology, Evolution, and Marine Biology, University of California at Santa Barbara Dr. Mark Rebeiz, Dpt. of Biological Sciences, University of Pittsburgh Dr. Elizabeth Arnold, Dpt. Ecology and Evolutionary Biology, University of Arizona Dissertation Advisor: Dr. Walter Carson, Dpt. Of Biological Sciences, University of Pittsburgh ii Copyright © by Eric Griffin 2016 iii THE GREATER UNSEEN: ON THE IDENTITIES, DISTRIBUTIONS, AND IMPACTS OF FOLIAR BACTERIA ON TROPICAL ARBOREAL SPECIES Eric Griffin, Ph.D. University of Pittsburgh, 2016 Bacteria have been called the “unseen majority” in nature. Leaves of higher plants comprise perhaps the largest bacterial substrate on earth, yet we know surprisingly little about the bacteria that occupy these spaces. The shaded understory of tropical forests is likely a “hotspot” for bacteria because water availability and humidity are high and UV radiation is low. Ultimately, these communities may be critical mediators of plant performance among co-occurring woody species and ultimately contribute to plant species distributions at the community level. In this dissertation, I (Chapter 2) review the ecology and behavior of bacteria that reside on the phyllosphere (on and inside leaves) and outline testable hypotheses to empirically evaluate the potential ecological implications of foliar bacteria. Moreover, I conducted a major effort to test interrelated hypotheses regarding the distribution, impact, and identity of foliar bacteria with replicated manipulations of N, P, and K in large experimental forest plots in Panama. To determine the net effect of foliar bacteria, I experimentally reduced bacterial in situ via the application of standard antibiotics for nearly three years. Specifically, I (Chapter 3) evaluated the degree to which soil nutrients and foliar bacteria impacted seedling growth among co- iv occurring woody species. Additionally, I (Chapter 4) evaluated the degree to which soil nutrients and foliar bacteria mediated leaf traits and enemy impacts among species and soil nutrient additions. Finally, I (Chapter 5) conducted a major sequencing effort to determine the degree to which host species, soil nutrients, and commercial antibiotics caused variation in bacterial endophyte community structure. Overall, my results demonstrate that there are frequent interactions between soil nutrient and foliar bacteria on plant performance and enemy impacts, which differ among host species. Further, metagenomic sequencing revealed that host species, soil nutrient additions, and antibiotics caused significant variations in bacterial community composition. For every metric, plant-bacterial interactions are largely dependent on host species and soil resource supply, a classic niche axis for species coexistence. Ultimately, my work provides evidence that foliar bacteria are an entirely independent plant functional trait that can cause critical species-specific performance outcomes, which may have important implications for plant diversity maintenance. v TABLE OF CONTENTS PREFACE ............................................................................................................................. XVIII 1.0 INTRODUCTION ................................................................................................................ 1 1.1 CHAPTER 2: ECOLOGY AND NATURAL HISTORY OF FOLIAR BACTERIA ............................................................................................................................ 2 1.2 CHAPTER 3: SOIL NUTRIENTS MEDIATE PLANT-MICROBE INTERACTIONS .................................................................................................................. 3 1.3 CHAPTER 4: IMPACTS OF SOIL NUTRIENTS AND BACTERIA ON LEAF TRAITS AND ENEMIES ..................................................................................................... 4 1.4 CHAPTER 5: ENDOPHYTE COMMUNITY ASSEMBLAGES ........................... 5 2.0 THE ECOLOGY AND NATURAL HISTORY OF FOLIAR BACTERIA WITH A FOCUS ON TROPICAL FORESTS AND AGROECOSYSTEMS ......................................... 7 2.1 INTRODUCTION ........................................................................................................ 7 2.1.1 Definitions .......................................................................................................... 9 2.2 BACTERIAL COLONIZATION AND RECRUITMENT TO THE PHYLLOSPHERE .............................................................................................................. 10 2.2.1 From soil to seed to seedling .......................................................................... 10 2.2.2 Mechanical chauffeuring ................................................................................ 11 2.2.3 Wind and rain ................................................................................................. 12 vi 2.2.4 Animal vectors ................................................................................................ 13 2.2.5 Vertical transmission ...................................................................................... 14 2.2.6 The core microbiome ...................................................................................... 15 2.3 FROM THE CANOPY TO THE FOREST FLOOR: TEMPERATURE, HUMIDITY, AND RADIATION STRUCTURE PHYLLOBACTERIAL COMMUNITIES ................................................................................................................. 17 2.3.1 Temperature and humidity ............................................................................ 17 2.3.2 UV radiation .................................................................................................... 18 2.4 TROPICAL LEAF ARCHITECTURE LIKELY SUPPORTS GREATER PHYLLOBACTERIAL COLONIZATION AND ABUNDANCE COMPARED TO TEMPERATE LEAVES .................................................................................................... 19 2.5 INTERACTIONS AMONG BACTERIA ON THE LEAF SURFACE ................ 21 2.5.1 Competition and niche partitioning .............................................................. 21 2.5.2 Bacterial aggregation ...................................................................................... 23 2.6 BACTERIAL-FUNGAL INTERACTIONS ON THE PHYLLOSPHERE ......... 24 2.7 BACTERIA IN THE INTERIOR PORTIONS OF LEAVES ............................... 26 2.7.1 Gaining access to the interior of the leaf ...................................................... 26 2.7.2 Bacterial endophytes significantly promote plant growth: lessons from root endophytes ........................................................................................................... 27 2.8 FOLIAR PATHOGENS: WHO THEY ARE, HOW THEY OVERCOME PLANT DEFENSES, AND THEIR DELETERIOUS POTENTIAL TO TROPICAL PLANTS ............................................................................................................................... 28 2.8.1 The main players ............................................................................................. 28 vii 2.8.2 How they overcome plant defenses ............................................................... 30 2.8.3 Bacterial pathogens in tropical systems ........................................................ 31 2.9 FOLIAR BACTERIA IN THE TROPICS .............................................................. 31 2.9.1 Phyllobacteria in tropical habitats ................................................................ 31 2.9.2 Bacterial endophytes in tropical habitats ..................................................... 33 2.10 WHAT ARE THE IMPACTS OF BACTERIAL PATHOGENS FOR PLANT COMMUNITIES IN TROPICAL HABITATS: TWO PERSPECTIVES .................... 35 2.11 CONCLUSIONS AND FUTURE DIRECTIONS ................................................. 37 2.12 ACKNOWLEDGMENTS ....................................................................................... 39 2.13 BIBLIOGRAPHY .................................................................................................... 40 2.14 TABLES .................................................................................................................... 87 3.0 SOIL FERTILITY MEDIATES SEEDLINGS RESPONSES TO FOLIAR BACTERIA IN A TROPICL FOREST: EXPERIMENTAL EVIDENCE AND ECOLOGICAL IMPLICATIONS .......................................................................................... 101 3.1 INTRODUCTION .................................................................................................... 101 3.2 METHODS ............................................................................................................... 105 3.2.1 Study site and species ................................................................................... 105 3.2.2 Design of the fertilization experiment ......................................................... 106 3.2.3 Seedling measurements and antibiotics .....................................................
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