Long-Term Experimental Warming Increases the Efficiency of the Methane Cycle
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Long-term experimental warming increases the efficiency of the methane cycle School of Biological and Chemical Sciences Queen Mary University of London Submitted in partial fulfilment of the requirements of the Degree of Doctor of Philosophy I, Yizhu Zhu, confirm that the research included within this thesis is my own work or that where it has been carried out in collaboration with, or supported by others, that this is duly acknowledged below and my contribution indicated. Previously published material is also acknowledged below. I attest that I have exercised reasonable care to ensure that the work is original, and does not to the best of my knowledge break any UK law, infringe any third party’s copyright or other Intellectual Property Right, or contain any confidential material. I accept that the College has the right to use plagiarism detection software to check the electronic version of the thesis. I confirm that this thesis has not been previously submitted for the award of a degree by this or any other university. The copyright of this thesis rests with the author and no quotation from it or information derived from it may be published without the prior written consent of the author. Signature: Date: 27th September 2019 This research project was supervised by Professor Mark Trimmer and Dr. Kevin Purdy and was supported by Queen Mary Principal’s research studentship. Abstract Methane is a potent greenhouse gas whose net emission from ecosystems represents the balance between microbial methane production (methanogenesis) and oxidation (methanotrophy), each with different sensitivities to temperature. How this balance will be altered by global warming over the long-term, and especially in freshwaters that are major methane sources, remains unknown. Here I demonstrate, using a well-replicated (n=20), long- term (for 11 years) freshwater warming experiment (+4 °C above ambient), that experimental warming of freshwater ecosystems drives a disproportionate increase in methanogenesis over methanotrophy that increases the warming potential of the gases they emit. After 11 years of warming, an ongoing divergence in methane emission between the warmed and ambient ponds was revealed and the annual methane emissions are now 2.4-fold higher under warming, in far excess of predictions based on temperature alone. Such increase in methane emissions was augmented by shifts in the methanogen community as warming makes hydrogenotrophic methanogenesis more energetically favourable. In contrast, the methanotroph community was conserved. Methanotrophy was able to respond physiologically to higher temperatures and methane, though the overall capacity to oxidise methane was limited to < 95 % of the methane produced but not the 98 % required to prevent methane emission from increasing. This long-term warming experiment provides a mechanistic understanding of a potential positive feedback, where climate warming induces changes at microbial level that stimulate increases in whole-ecosystem methane emissions. Further, the experimentally induced changes to the methane cycle are borne out at global scale as a disproportionate increase in the capacity of naturally warmer ecosystems to emit methane. Together, the findings in this thesis strongly indicate that as Earth continues to warm, natural 1 ecosystems will emit disproportionately more methane to the atmosphere in a positive feedback warming loop. 2 Acknowledgements I would like to express my very great appreciation to my supervisor, Prof. Mark Trimmer, for giving me the opportunity to work on this project and for your guidance during the planning and development of this research work. Thank you for all the time you have been generously given for teaching me statistics, critical thinking and scientific writing. I would also like to thank Dr. Kevin Purdy, my co-supervisor, for useful suggestions and for patient instructions on molecular work and paper writing. Thanks to Dr. Ozge Eyice-Broadbent for teaching the molecular work and for sharing your experience in academia. Thanks to Dr. Liao Ouyang for introducing me the laboratory during my very first days in Queen Mary and to Dr. Lidong Shen and Dr. Sarah Harpenslager for very useful discussions on science. Thanks to Dr. Ian Sander, Dr. Felicity Shelley and Paul Fletcher for offering technical and fieldwork assistance. A big thank to Tian Du for your encouragement in the difficult times and for suggestions about surviving a PhD. And to my parents for your unconditional support throughout my study. 3 Table of Contents Abstract 1 Acknowledgements 3 Chapter 1 General Introduction ........................................................................... 8 1.1 Feedback through greater methane emissions in a warmer world ........................................ 8 1.1.1 Disproportionate emissions from freshwaters ..................................................................... 8 1.1.2 Temperature sensitivity of methane fluxes ......................................................................... 9 1.1.3 Methane emissions are not a simple response to temperature alone ................................. 10 1.2 Net CH4 emission: the balance between production (methanogenesis) and oxidation (methanotrophy) ............................................................................................................................................... 11 1.2.1 Methanogenesis and its response to warming ................................................................... 12 1.2.2 Methanotrophy responses to temperature and greater methane availability ..................... 13 1.2.3 Coupled processes between methane production and oxidation ....................................... 14 1.2.4 Long-term effects: can methanotrophy counterbalance methanogenesis in a warmer world? 15 1.3 Linking microbial communities to ecosystem-level processes .............................................. 16 1.3.1 Limitation in microbial community ecology ..................................................................... 17 1.3.2 Archaeal methanogens and bacterial methanotrophs ........................................................ 18 1.3.3 Temporal scales in linking microbial community to ecosystem-level processes .............. 19 1.3.4 A long-term warming mesocosm experiment ................................................................... 20 1.4 Goals and structural outline of the thesis ............................................................................... 21 Chapter 2 Long-term warming continuously amplifies methane emissions .. 23 2.1 Abstract ..................................................................................................................................... 23 2.2 Introduction .............................................................................................................................. 24 2.3 Materials and Methods ............................................................................................................ 26 2.3.1 Mesocosm pond facility .................................................................................................... 26 4 2.3.2 Sediment characteristics .................................................................................................... 26 2.3.3 Dissolved methane concentrations .................................................................................... 27 2.3.4 Methane and carbon dioxide fluxes measurements via high-frequency chambers ........... 28 2.3.5 Characterization of ebullition in methane emission measurements .................................. 29 2.3.6 Calculation of methane and carbon dioxide fluxes ........................................................... 31 2.3.7 Ratio of methane emission to net carbon dioxide exchange ............................................. 32 2.3.8 Net global warming potential of carbon gases emitted ..................................................... 33 2.3.9 Statistical analysis ............................................................................................................. 34 2.3.10 Prediction of methane emission from the apparent activation energy .............................. 39 2.4 Results........................................................................................................................................ 41 2.4.1 Sediment characteristics and comparison of CH4 emission from experimental ponds to natural ecosystems ......................................................................................................................................... 41 2.4.2 Net carbon dioxide exchange ............................................................................................ 42 2.4.3 Annual methane emissions ................................................................................................ 44 2.4.4 Ratio of methane emission to net carbon dioxide exchange ............................................. 46 2.4.5 Temperature dependence of methane and carbon dioxide emissions and rates of methane and carbon dioxide emissions at 15 °C .......................................................................................................... 50 2.4.6 Meta-analysis of global data on CH4 and CO2 emission at 15 °C ..................................... 53 2.4.7 Ratio of CH4 to CO2 emission ........................................................................................... 54 2.5 Discussion .................................................................................................................................