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Microbiota of Dominant Atlantic Copepods: Pleuromamma Sp. As a Host to a Betaproteobacterial Symbiont

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Microbiota of Dominant Atlantic Copepods: Pleuromamma Sp. As a Host to a Betaproteobacterial Symbiont UNIVERSITY OF SOUTHAMPTON Faculty Of Natural And Environmental Sciences School of Ocean and Earth Science Microbiota of dominant Atlantic copepods: Pleuromamma sp. as a host to a betaproteobacterial symbiont by Sara Joan Javornik Cregeen Thesis for the degree of Doctor of Philosophy March 2016 UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Sciences Thesis for the degree of Doctor of Philosophy MICROBIOTA OF DOMINANT ATLANTIC COPEPODS: PLEUROMAMMA SP. AS A HOST TO A BETAPROTEOBACTERIAL SYMBIONT by Sara Joan Javornik Cregeen Copepods are the most abundant zooplankton group in the ocean and play a pivotal role as grazers of microorganisms and prey for larger animals. Furthermore, they are major contributors to the pool of dissolved organic material in the pelagic and therefore play an important role in the microbial loop. Although biology of copepods has been under investigation for more than a century, few studies have looked at the relationship between copepods and their associated bacteria. Could copepods be perceived as distinctive microbial hotspots in nutrient poor pelagic environment? The microbiota of three Pleuromamma species, an abundant genus of copepods that migrate vertically from surface waters to several hundred meters water depth and back on a daily basis was investigated using various molecular and morphological techniques. The focus was on the differences in the bacterial community composition of these copepods along the Atlantic Meridional Transect, which traverses major oceanic biomes such as the subtropical gyres and the equatorial convergence region. Additionally, the community structure and stable isotope composition of the likely microplankton food source as well as the Pleuromamma copepods was assessed along the same cruise transect. Sequencing of 16S rRNA tag libraries derived from individual Pleruromamma copepods showed a broad diversity of Bacteria associated with these copepods. These bacterial communities were uniform across the oceanic provinces and Pleuromamma species. These results were reflected in the uniformity of the prey community composition, however there was an indication that Pleuromamma copepods from different regions in the Atlantic rely on different food sources. Fluorescence in situ hybridisation and electron microscopy showed the presence of bacteria in the midgut region of the copepod guts and more specifically a high abundance of Betaproteobacteria. The bacterial community of a dominant copepod species in the Atlantic has previously not been studied on such a large spatial scale and sample size. This study shows that the same bacterial taxa were associated with Pleuromamma copepods inhabiting distinct oceanic regions. Moreover, a betaproteobacterial genus not present in the water-column appears to be closely associated with Pleuromamma. “I may not have gone where I intended to go, but I think I have ended up where I needed to be.” - Douglas Adams Where Earth's tears flow, Ubiquitous crustaceans Paddle their oar-feet - by Dr. Matthew Humphreys Table of Contents Table of Contents Table of Contents .................................................................................................................................... i List of Tables ........................................................................................................................................... v List of Figures ...................................................................................................................................... vii List of Appendices ............................................................................................................................... ix DECLARATION OF AUTHORSHIP ................................................................................................... xi Acknowledgements .......................................................................................................................... xiii Abbreviations ...................................................................................................................................... xv Chapter 1 Introduction ...................................................................................................................... 1 1.1 Copepods – pivotal players in the pelagic food web ............................................................ 2 1.2 Pelagic trophic web ............................................................................................................................ 3 1.3 Animal-microbe associations ......................................................................................................... 6 1.3.1 Types of symbioses ......................................................................................................... 7 1.3.2 Symbiont role .................................................................................................................... 8 1.3.3 Symbiont transmission .................................................................................................. 9 1.4 Methodology used to study animal-bacteria interactions .............................................. 11 1.4.1 Next generation sequencing technologies .......................................................... 12 1.4.2 Partitioning of sequences into meaningful units ............................................. 14 1.4.3 Quantitative and visualisation methods .............................................................. 15 1.5 Thesis rationale ................................................................................................................................ 16 1.5.1 Aims and objectives ..................................................................................................... 16 Chapter 2 Atlantic Meridional Transect – description of the study site and sampling procedures ........................................................................................................................ 19 2.1 Atlantic Meridional Transect Programme ............................................................................. 19 2.2 Physical and biological structuring of the Atlantic Ocean .............................................. 20 2.2.1 Defining Atlantic Ocean regions along AMT22 and AMT24 ........................ 21 2.3 AMT – sample collection ............................................................................................................... 24 2.3.1 AMT22 ............................................................................................................................... 26 2.3.2 AMT24 ............................................................................................................................... 27 Chapter 3 Molecular characterisation and morphological description of Pleuromamma copepods ............................................................................................. 33 3.1 Introduction ....................................................................................................................................... 33 3.2 Methods ............................................................................................................................................... 34 3.2.1 Sample selection ............................................................................................................ 34 3.2.2 COI amplification and phylogenetic analysis ..................................................... 35 i Table of Contents 3.2.3 Copepod condition measurements and elemental composition ............... 36 3.2.4 Electron microscopy and histology ....................................................................... 36 3.2.5 Supplementary information – Appendix A ......................................................... 37 3.3 Results .................................................................................................................................................. 37 3.3.1 Phylogenetic relationship of P. gracilis, P. piseki and P. borealis ............... 38 3.3.2 Body size and condition of animals along the AMT24 cruise track ......... 42 3.3.3 Morphological description ........................................................................................ 43 3.4 Discussion ........................................................................................................................................... 47 Chapter 4 Microplankton and Pleuromamma copepod elemental and stable isotope analysis along AMT24 .................................................................................................. 51 4.1 Introduction ....................................................................................................................................... 51 4.2 Materials and Methods .................................................................................................................. 53 4.2.1 Sample collection .......................................................................................................... 53 4.2.2 FlowCam image processing ...................................................................................... 55 4.2.3 Stable isotope and elemental C and N measurements ................................... 55 4.2.4 Data analysis ................................................................................................................... 56 4.3 Results .................................................................................................................................................
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