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The Response of Anaerobic Prokaryotic Processes And The Response of Anaerobic Prokaryotic Processes and Communities in Severn Estuary Sediments to Environmental Change Shaun Thomas A thesis submitted to Cardiff University in accordance with the regulations governing the award of Philosophiae Doctor October 2014 Cardiff University School of Earth and Ocean Sciences i DECLARATION This work has not been submitted in substance for any other degree or award at this or any other university or place of learning, nor is being submitted concurrently in candidature for any degree or other award. Signed………………………………………………………………(candidate) Date………………………….. STATEMENT 1 This thesis is being submitted in partial fulfilment of the requirements for the degree of ……………………. (insert MCh, MD, MPhil, PhD etc. as appropriate). Signed………………………………………………………………(candidate) Date………………………….. STATEMENT 2 This thesis is the result of my own independent work/investigation, except where otherwise stated. Other sources are acknowledged by explicit references. The views expressed are my own. Signed………………………………………………………………(candidate) Date………………………….. STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available online in the University’s Open Access repository and for inter-library loan, and for the title and summary to be made available to outside organisations. Signed………………………………………………………………(candidate) Date………………………….. STATEMENT 4: PREVIOUSLY APPROVED BAR ON ACCESS I hereby give consent for my thesis, if accepted, to be available online in the University’s Open Access repository and for inter-library loans after expiry of a bar on access previously approved by the Academic Standards & Quality Committee. Signed………………………………………………………………(candidate) Date………………………….. ii Acknowlegements First off I’d like to thank my parents, thank you for always believing in me and giving me the confidence I needed to get through this. Special thanks to my supervisors, John, Henrik, and Andy for putting together this project and for their assistance and helpful comments throughout. Also to Sir Martin Evans for providing the funding for the President’s Scholarship program. I’d also like to thank everyone who assisted me with lab or fieldwork: Barry Cragg, Miriam Olivier, Gordon Webster, Xiaohong Tang, Erwan Roussel, Andrew Watkins Andrea Sass, Sarah Lee, Ian Fryett, Paul Evans, Chris Wooldridge, Nick Rodgers, Luke Croudace, Angharad Williams, Jen Pinnion and Paul Biggs (and to anyone else I’ve forgotten, sorry and thank you too). Additional thanks are also due to anyone who was willing to brave a mudflat or boat trip to the always sunny and mirror-calm Severn Estuary (doubly so for those mad enough to do so more than once). Finally thanks to Kate, Loz and Tom for always being there when I needed someone to talk to, for being the best friends a guy could ask for and for always making me laugh and keeping me sane (especially during the write up). iii “And heaved and heaved, still unrestingly heaved the black sea, as if its vast tides were a conscience; and the great mundane soul were in anguish and remorse for the long sin and suffering it had bred.” Herman Melville, Moby Dick “I cannot think of the deep sea without shuddering at the nameless things that may at this very moment be crawling and floundering on its slimy bed” H. P. Lovecraft, Dagon “There is no point trying to hide from your bacteria… This is their planet, and we are only on it because they allow us to be” Bill Bryson, A Short History Of Nearly Everything iv Summary The Severn Estuary in the south-western UK is one of the most tidally dynamic environments on the planet. However, despite this the sediments of the estuary remain relatively understudied with regards to their biogeochemical potential. The aim of this project was to investigate how the constantly changing sedimentary environment in the estuary, in which millions of tonnes of sediment are eroded and deposited over the tidal cycle, affects the prokaryotes within the sediments and the processes they control, and also to determine what effect environmental changes in the estuarine system might have on these processes. The study showed that the sediments of the Severn Estuary have high rates of sediment oxygen demand (SOD) indicating a high degree of organic matter (OM) degradation. However, the sediments have low rates of the anaerobic processes that are expected to dominate in shallow marine systems (e.g. sulphate reduction and methanogenesis), suggesting that most OM degradation must be linked to processes further up the redox cascade. The sediments also showed a lack of microbial guild depth zonation, with methanogenesis occurring above or alongside sulphate reduction. Both of these unusual factors can be linked to the regular re-suspension of the estuary’s sediments by tidal action, resulting in large-scale oxidation and mixing of the sediment column and the suppression of anaerobic processes while potentially stimulating aerobic and dysaerobic activity. This same mixing would also distribute guilds of organisms throughout the sediment, creating isolated pioneer populations with a general lack of competition. Re-suspension is also likely responsible for the high cell counts that persist to significant depth around the estuary, as the mixing of sediment and entrainment of OM would produce high and homogeneous cell profiles upon deposition, which in turn can be linked to the high SOD of the estuary’s sediments. Despite this dominance of aerobic and dysaerobic processes throughout most of the estuary some isolated sites do show increased rates of anaerobic processes, particularly at locations that have undergone significant environmental change. These include fluidised mud pools in the deeper areas of the estuary, salt marsh peat deposits at St Brides Wentlooge (especially within the “activated interface”) and Cardiff Bay, an anthropogenic lake and former mudflat environment which shows significant methanogenic potential. Overall this study has shown that the dynamic conditions in the Severn Estuary promote the activity of aerobic and dysaerobic prokaryotic groups over the anaerobic groups traditionally thought to dominate in shallow marine sediments. However, this promotion is not uniform across the estuary, instead varying with topography/bathymetry and the degree of sediment disturbance. v Contents Title p. i Declaration p. ii Acknowledgements p. iii Quotations p. iv Summary p. v Contents p. vi List of Figures p. xi List of Tables p. xvi List of Abbreviations p. xvi Chapter 1. – An Introduction to Estuarine Sediment Biogeochemistry and the Severn Estuary 1.1 The Redox Cascade p. 1 1.1.1 Aerobic Respiration p. 4 1.1.2 Nitrogen Cycling - Denitrification, DNRA and Nitrification/ Ammonium Oxidation p. 5 1.1.3 Dissimilatory Manganese Reduction and Oxidation p. 7 1.1.4 Dissimilatory Iron Reduction and Oxidation p. 8 1.1.5 Dissimilatory Sulphate Reduction and Sulphide Oxidation p. 9 1.1.6 Methanogenesis, Fermentation and AOM p. 14 1.2 Environmental Factors influencing Prokaryotic Growth p. 20 1.2.1 Salinity p. 20 1.2.2 Temperature p. 23 1.3 An Introduction to the Severn Estuary 1.3.1 Geographical Setting p. 26 1.3.2 Geological History and Formation p. 30 1.3.3 Tidal Range p. 30 1.3.4 Biogeochemistry of the Severn Estuary p. 34 1.3.5 Benthic Macrofauna of the Severn Estuary p. 37 1.3.6 Sediments of the Severn Estuary p. 39 vi 1.3.7 Hydrology and Water Chemistry of the Severn Estuary p. 47 1.3.8 Research Objectives and Site Selection p. 50 Chapter 2. – Methodology 2.1 Sediment Coring p. 53 2.2 Oxygen Uptake Measurements p. 55 2.3 Sectioning of Sediment Cores p. 58 2.4 Pore Water Analysis p. 58 2.5 Sediment Gas Content p. 60 2.6 Total Cell Counts p. 61 2.7 Rates of Anaerobic Processes p. 64 3.7.1 Active Sulphate Reduction Rate Measurements p. 64 3.7.2 Active Methanogenesis Rate Measurements p. 70 2.8 Sediment Porosity p. 73 Chapter 3. – The Severn Estuary Transect: Cores ST1, ST2 and ST3 3.1 Site Locations and Lithology p. 74 3.2 The Severn Estuary Transect – Results p. 76 3.2.1 Biogeochemistry of Core ST1 p. 76 3.2.2 Biogeochemistry of Core ST2 p. 81 3.2.3 Biogeochemistry of Core ST3 p. 85 3.3 The Severn Estuary Transect – Discussion p. 90 3.3.1 Sedimentology p. 90 3.3.2 Organic Acids – Acetate, Lactate and Formate p. 91 3.3.3 Nitrate and Ammonium p. 93 3.3.4 Chloride and the Alkali Metals p. 95 3.3.5 Sulphate p. 99 3.3.6 Methane p. 100 3.3.7 Total Cell Counts p. 102 3.4 The Severn Estuary Transect – Conclusions p. 104 vii Chapter 4. – Severn Estuary Tidal Flats, Part 1: Cores ST4 and ST5 4.1 Site Locations and Lithology p. 106 4.2 Severn Estuary Tidal Flats, Part 1 – Results p. 111 4.2.1 Biogeochemistry of Core ST4 p. 111 4.2.2 Biogeochemistry of Core ST5 p. 119 4.3 Severn Estuary Tidal Flats, Part 1 – Discussion p. 126 4.4 Severn Estuary Tidal Flats, Part 1 – Conclusions p. 130 Chapter 5. – Severn Estuary Tidal Flats, Part 2: Core ST6 5.1 Site Location and Lithology p. 131 5.2 Severn Estuary Tidal Flats, Part 2 – Results p. 133 5.2.1 Biogeochemistry of ST6 p. 133 5.3 Severn Estuary Tidal Flats, Part 2 – Discussion p. 142 5.3.1 Comparison with Core ST4 p. 142 5.3.2 Comparison with Core ST5 p. 145 5.4 Severn Estuary Tidal Flats, Part 2 – Conclusions p. 147 Chapter 6. – Bridgwater Bay: Cores ST7 and ST8 6.1 Site Locations and Lithology p. 148 6.2 Bridgwater Bay – Results p. 150 6.2.1 Biogeochemistry of Core ST7 p. 150 6.2.2 Biogeochemistry of Core ST8 p. 156 6.3 Bridgwater Bay – Discussion p.
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