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The Impact of Environmental Changes on the Microbial Community Dynamics and Abundance of Pathogenic Vibrio Species in Coastal Ecosystems

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The Impact of Environmental Changes on the Microbial Community Dynamics and Abundance of Pathogenic Vibrio Species in Coastal Ecosystems The Impact of Environmental Changes on the Microbial Community Dynamics and Abundance of Pathogenic Vibrio species in Coastal Ecosystems by Candice Amber Thorstenson a Thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Marine Microbiology Approved Dissertation Committee _____________________________________ Prof. Dr. Matthias Ullrich Jacobs University Bremen Prof. Dr. Frank Oliver Glӧckner Jacobs University Bremen Dr. Mathias Wegner Alfred Wegener Institute for Polar and Marine Research Date of Defense: 26 August 2020 Department of Life Sciences and Chemistry i Table of Contents Summary .......................................................................................................... 1 General Introduction ........................................................................................ 3 The genus Vibrio ............................................................................................................. 5 Key Vibrio Characterization and Isolation Techniques .................................................. 9 Vibrio cholerae ............................................................................................................. 10 Vibrio parahaemolyticus ............................................................................................... 12 Vibrio vulnificus ............................................................................................................ 14 Genetic Modification Technologies Applied to Marine Bacteria ................................. 16 Study Objectives and Major Aims .................................................................21 Study Outline .................................................................................................23 Results, Chapter I: Developing a Universal and Efficient Method for the Rapid Selection of Stable Fluorescent Protein-tagged Pathogenic Vibrio species ..26 Abstract ......................................................................................................................... 26 Introduction ................................................................................................................... 27 Materials and Methods .................................................................................................. 29 Results ........................................................................................................................... 39 Discussion ..................................................................................................................... 47 Acknowledgments......................................................................................................... 53 Chapter II. Ecological fitness of Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus in a Small-scale Population Dynamics Study .............54 Abstract ......................................................................................................................... 54 Introduction ................................................................................................................... 55 ii Materials and Methods .................................................................................................. 57 Results ........................................................................................................................... 62 Discussion ..................................................................................................................... 77 Acknowledgments......................................................................................................... 89 Chapter III: Pathogenic Vibrio abundance and species diversity within coastal regions of the North Atlantic and North Sea .................................................90 Summary ....................................................................................................................... 90 Introduction ................................................................................................................... 91 Materials and Methods .................................................................................................. 93 Results ........................................................................................................................... 98 Discussion ................................................................................................................... 111 Acknowledgments....................................................................................................... 116 General Discussion ......................................................................................117 Fluorescent Protein-tagging Vibrio species ................................................................ 117 The Ecological fitness of V. cholerae, V. parahaemolyticus, and V. vulnificus ......... 123 Vibrio species abundance and diversity within the North Atlantic and North Sea ..... 128 Concluding Remarks ................................................................................................... 130 Acknowledgments .......................................................................................132 References ....................................................................................................134 Supplementary Figures ................................................................................153 iii Summary Summary Coastal ecosystems are highly dynamic regions and extremely important to the livelihoods and health of the people living in coastal regions. Tourism, the aquaculture industry, and human health are all directly tied to the microbial community in these regions. Furthermore, many key aquaculture stocks, such as oysters, may serve as vectors for a variety of foodborne diseases in humans, both at the harvesting area and when imported far inland. Rising sea surface temperatures in the North Atlantic and North Sea have been heavily implicated in the spread and rising abundance of the human pathogenic Vibrio species: Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus in North America and Northern Europe. This study investigates how environmental changes may impact the growth and behavior of these key Vibrio species within the context of the surrounding microbial community. This was accomplished through the in situ fluorescent-labelling of environmental strains for live microcosm experiments with a native North Sea water community and the identification and characterization of two discrete pathogenic Vibrio populations in the North Sea off the coast of Sylt, Germany, and along the North Atlantic coast of La Tremblade, France. The genetic accessibility of these important human pathogenic Vibrios, V. cholerae, V. parahaemolyticus, and V. vulnificus, was assessed through the development of a rapid fluorescent protein-labelling system via conjugable vectors carrying fluorescent and antibiotic selection markers encoded on a transposon. This method produced transconjugants from all tested Vibrio strains with an efficiency of at least two transconjugants per 10,000 recipient cells within two days of selective growth. 1 Summary Red fluorescent protein-labelled V. cholerae, V. parahaemolyticus, and V. vulnificus clones were co-incubated with sterile sea water and non-sterile sea water containing a native microbial community under three discrete temperatures. These microcosm experiments indicated that increased temperatures alone do not confer greater competitive fitness to these Vibrio species. Finally, through environmental field sampling for pathogenic Vibrio in two discrete coastal communities, we found that temperature and salinity were the best explanatory variables for the abundance of Vibrio species in accordance with similar studies. Furthermore, through a targeted isolation campaign, we found the two Vibrio populations from each sampling site varies in species composition, allowing for future speculation on the role these species may play in their respective regions and niches. 2 General Introduction General Introduction Coastal ecosystems are valuable to human society, biodiversity, and the climate in these regions. From northern sea ice to mangrove ecosystems in the Pacific and Antarctic ice flows, the term “coastal ecosystem” refers to a dramatic range of habitats. These ecosystems are highly dynamic, representing the interchange from marine to terrestrial habitats, and are home to both specialized and adaptable flora and fauna. Approximately half of global commerce is dependent on coastal goods and services (Costanza et al., 1997), which puts coastal ecosystems under strong anthropogenic pressure and illustrates their importance to anthropological activities. The aquaculture industry has grown in the past several decades, and of concern is the spread of pathogens in fisheries and other aquaculture stocks worldwide due to anthropologic activities and environmental change (Jegatheesan et al., 2011; Naylor et al., 2000). Anthropological activities known to influence the spread of pathogens includes, but are not limited to: travel (including shipping and the transfer of ballast water), eutrophication of coastal waters influencing algal blooms, the domestication of animals and increased exposure to zoonotic diseases, the misuse of antibiotics, and contamination of water with heavy metals (Barua, 1992; R. R. Colwell, 1996; Imran et al., 2019; Lebarbenchon et al., 2008). With rising temperatures worldwide, and the warming of the
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