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The Hydrocarbon Biodegradation Potential of Faroe-Shetland Channel Bacterioplankton

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THE HYDROCARBON BIODEGRADATION POTENTIAL OF FAROE-SHETLAND CHANNEL BACTERIOPLANKTON Angelina G. Angelova Submitted for the degree of Doctor of Philosophy Heriot Watt University School of Engineering and Physical Sciences July 2017 The copyright in this thesis is owned by the author. Any quotation from the thesis or use of any of the information contained in it must acknowledge this thesis as the source of the quotation or information. ABSTRACT The Faroe-Shetland Channel (FSC) is an important gateway for dynamic water exchange between the North Atlantic Ocean and the Nordic Seas. In recent years it has also become a frontier for deep-water oil exploration and petroleum production, which has raised the risk of oil pollution to local ecosystems and adjacent waterways. In order to better understand the factors that influence the biodegradation of spilled petroleum, a prerequisite has been recognized to elucidate the complex dynamics of microbial communities and their relationships to their ecosystem. This research project was a pioneering attempt to investigate the FSC’s microbial community composition, its response and potential to degrade crude oil hydrocarbons under the prevailing regional temperature conditions. Three strategies were used to investigate this. Firstly, high throughput sequencing and 16S rRNA gene-based community profiling techniques were utilized to explore the spatiotemporal patterns of the FSC bacterioplankton. Monitoring proceeded over a period of 2 years and interrogated the multiple water masses flowing through the region producing 2 contrasting water cores: Atlantic (surface) and Nordic (subsurface). Results revealed microbial profiles more distinguishable based on water cores (rather than individual water masses) and seasonal variability patterns within each core. Secondly, the response of the microbial communities to crude oil was investigated in laboratory-based microcosms. Microbial communities from all water masses exhibited hydrocarbon biodegradation activity at average FSC temperatures (4°C), albeit with markedly delayed and potentially slower response in comparison to those exposed to moderate control temperatures (20°C). A collection of bacterial isolates, comprising of 230 FSC strains with putative hydrocarbonoclastic activity was created, which included psychrotolerant members belonging to the genera Marinobacter, Pseudoalteromonas, Cycloclasticus, Halomonas, Thalassolituus and Glaciecola. Lastly, a sophisticated molecular technique called DNA-based stable isotope probing (DNA-SIP) was used to directly target and identify hydrocarbon-degrading taxa that may not be easily amenable to cultivation. Using DNA-SIP, hydrocarbonoclastic FSC strains affiliated with the genera Phaeobacter and Lentibacter were identified, along with strains affiliated with known hydrocarbon-degraders from the genera Thalassolituus, Alcanivorax, Oleispira, Glaciecola, Marinobacter and Cycloclasticus. Correlating the findings from all three experiments, revealed that ~41% of the baseline FSC microbial community constituted bacteria affiliated to genera with hydrocarbon-degrading capacities. Their response to the presence of hydrocarbons, however, appeared to be largely influenced by temperature. This work is the first to establish a microbial baseline for the FSC and to investigate the microbial repose to crude oil in the water column of the region. Results are expected to contribute to the development of biotechnologies and oil-spill mitigation strategies tailored for the FSC region in the event of an oil spill. ACKNOWLEDGEMENTS Firstly, I would like to express my gratitude to my supervisor Dr Tony Gutierrez for giving me this amazing opportunity and supporting me throughout this project. Next a very special thank you is due to Dr Stephen Summers and Dr Ted Henry who endured my inquiries and always took the time to teach me, guide me and help me advance in this PhD. Thank you to Dr Andrew Free and his wonderful team for teaching me the secrets of DGGE, to the scientific crew of MRV Scotia for helping me with sampling, understanding the hydrography of the Faroe-Shetland Channel, guiding me during the cruises and especially for not loosing me at sea. Furthermore, I send my sincerest gratitude to Dr Nina Domrowski and Dr Brett Baker from the Marine Science Institute at the University of Texas, for providing special attention and training in metagenomic data analysis and metabolic prospecting. It was a privilege to be taught by you. This work would also not have been possible without my dearest friends and colleagues from Heriot-Watt University, who made me feel like a part of a community, provided sanity, moral support, wisdom and scientific expertise as needed. A very special thank you to my family who stepped up to make this endeavour of mine possible. Last but not least, I would like to thank my doggie Rockie who patiently waited for me while I chased my dreams. DEDICATION This thesis is dedicated to my grandmother Radka Yanakieva, who has always been my inspiration, motivation and strength. DECLARATION STATEMENT ACADEMIC REGISTRY Research Thesis Submission Name: Angelina Angelova School: School of Engineering and Physical Sciences Version: (i.e. First, First Degree Sought: Doctor of Philosophy Resubmission, Final) Declaration In accordance with the appropriate regulations I hereby submit my thesis and I declare that: 1) the thesis embodies the results of my own work and has been composed by myself 2) where appropriate, I have made acknowledgement of the work of others and have made reference to work carried out in collaboration with other persons 3) the thesis is the correct version of the thesis for submission and is the same version as any electronic versions submitted*. 4) my thesis for the award referred to, deposited in the Heriot-Watt University Library, should be made available for loan or photocopying and be available via the Institutional Repository, subject to such conditions as the Librarian may require 5) I understand that as a student of the University I am required to abide by the Regulations of the University and to conform to its discipline. 6) I confirm that the thesis has been verified against plagiarism via an approved plagiarism detection application e.g. Turnitin. * Please note that it is the responsibility of the candidate to ensure that the correct version of the thesis is submitted. Signature of Date: 11/07/2017 Candidate: Submission Submitted By (name in capitals): ANGELINA ANGELOVA Signature of Individual Submitting: Date Submitted: 17/07/2017 For Completion in the Student Service Centre (SSC) Received in the SSC by (name in capitals): Method of Submission (Handed in to SSC; posted through internal/external mail): E-thesis Submitted (mandatory for final theses) Signature: Date: TABLE OF CONTENTS ABSTRACT ............................................................................................................................. 0 TABLE OF CONTENTS ........................................................................................................ 0 Glossary .................................................................................................................................... 1 Chapter 1: Introduction ...................................................................................................... 2 1.1 Oceanography of the Faroe-Shetland Channel .......................................................... 2 1.2 Crude oil in the marine environment .......................................................................... 4 1.2.1 Natural oil seeps ................................................................................................................... 4 1.2.2 Anthropogenic oil sources .................................................................................................... 5 1.3 Composition of crude oil ............................................................................................... 7 1.3.1 Aliphatics ......................................................................................................................................... 8 1.3.2 Aromatics ........................................................................................................................................ 9 1.3.3 Resins .............................................................................................................................................. 9 1.3.4 Asphaltenes .................................................................................................................................... 10 1.3.5 General properties of crude oils .................................................................................................... 10 1.4 Fate of crude oil upon its entry into the marine environment ................................ 11 1.5 Microbial degradation of hydrocarbons in the ocean .............................................. 13 1.5.1 Factors influencing microbial degradation ......................................................................... 13 1.5.1.1 Temperature ................................................................................................................................ 14 1.5.1.2 Nutrients ..................................................................................................................................... 14 1.5.1.3 Oxygen ....................................................................................................................................... 15 1.5.2 Strategies used
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