The Response of Anaerobic Prokaryotic Processes and Communities in Severn Estuary Sediments ...

388 Pages·2015·14.93 MB·English

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. 164
6.4 Bridgwater Bay – Conclusions p. 171

Chapter 7. – St Brides Wentlooge: Cores StB1 and StB2
7.1 Core Descriptions and Lithology p. 173
7.2 St Brides Wentlooge – Results p. 175
7.2.1 Biogeochemistry of Core StB1 p. 175
7.2.2 Biogeochemistry of Core StB2 p. 188
7.3 St Brides Wentlooge – Discussion p. 203
viii
7.4 St Brides Wentlooge - Glycolate Slurry Experiment p. 210
7.4.1 Methodology p. 210
7.4.2 Results and Discussion p. 211
7.5 St Brides Wentlooge – Conclusions p. 215

Chapter 8. – Cardiff Bay: Cores CB2-CB8
8.1 Site Locations and Lithology p. 218
8.2 Cardiff Bay – Results p. 221
8.2.1 Biogeochemistry of Site 1 – Cores CB2, CB5 and CB8 p. 221
8.2.2 Biogeochemistry of Site 2 – Cores CB3 and CB6 p. 233
8.2.3 Biogeochemistry of Site 3 – Cores CB4 and CB7 p. 243
8.3 Cardiff Bay – Discussion p. 252
8.3.1 Core Lithology p. 252
8.3.2 Sediment Oxygen Demand and Organic Acids p. 255
8.3.3 Chloride, Bromide and Sodium p. 256
8.3.4 Nitrate, Nitrite and Ammonium p. 258
8.3.5 Sulphate and Thiosulphate p. 260
8.3.6 Methane p. 262
8.3.7 Total Cell Counts p. 267
8.4 Cardiff Bay – Conclusions p. 267

Chapter 9. – General Discussion
9.1 Biogeochemical Processes in the Severn Estuary p.269
9.1.1 Sulphate reduction in the Severn Estuary p.269
9.1.2 Methanogenesis in the Severn Estuary p. 275
9.1.3 Oxygen Uptake and Organic Matter Degradation in the Severn
Estuary p. 283
9.1.4 Prokaryotic Cell Numbers in the Severn Estuary p. 288
9.2 Statistical Analyses p. 297
9.3 Unusual Microbial Habitats of the Severn Estuary p. 312
9.3.1 Fluidised Muds p. 312
9.3.2 Buried Salt Marshes p. 313
9.3.3 Submarine Groundwater Discharge p. 314
ix
9.4 The Role of Sedimentary Prokaryotes in Future
Environmental Change p. 315
9.4.1 The Effects of Climate Change in the Severn Estuary p. 315
9.4.2 The Effects of Tidal Barrages in the Severn Estuary p. 319
9.4.3 The Role of Severn Estuary Microbiota in Effecting the Environment
and Climate p. 322
9.5 Future Investigations p. 325
9.5.1 Simulating respiration rates in fluidised mud beds p. 325
9.5.2 Examining the effects of varying temperatures on microbial
processes in Severn Estuary sediments p. 327
9.5.3 Studying the inhibition of prokaryotic processes by peat-derived
compounds p. 328
9.5.4 Measuring NO -, Fe3+ and Mn3+ reduction in Severn Estuary
3
sediments p. 328
9.5.5 Measuring the effusive methane flux of the sediments of Cardiff Bay p. 328
9.5.6 Examining the biogeochemistry of other hypertidal estuaries p. 329
9.6 Conclusions on the Biogeochemistry of the Severn Estuary p. 330

References p. 334
x