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Temperature Limitations to Enzyme-Catalyzed Arctic Soil

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Temperature Limitations to Enzyme-Catalyzed Arctic Soil A Thesis entitled What’s the Holdup? Temperature Limitations to Enzyme-Catalyzed Arctic Soil Decomposition by Ruth Whittington Submitted to the Graduate Faculty as partial fulfillment of the requirements for the Master of Science Degree in Biology ___________________________________________ Michael Weintraub, PhD, Committee Chair ___________________________________________ Daryl Moorhead, PhD, Committee Member ___________________________________________ Patrick Sullivan, PhD, Committee Member ___________________________________________ Cyndee Gruden, PhD, Dean College of Graduate Studies The University of Toledo August 2019 Copyright 2019, Ruth Whittington This document is copyrighted material. Under copyright law, no parts of this document may be reproduced without the expressed permission of the author. An Abstract of What’s the Holdup? Temperature Limitations to Enzyme-Catalyzed Arctic Soil Decomposition by Ruth Whittington Submitted to the Graduate Faculty as partial fulfillment of the requirements for the Master of Science Degree in Biology The University of Toledo August 2019 Arctic ecosystems contain globally important terrestrial carbon stocks, and their temperatures are rising at twice global rates. While increasing temperatures lead to faster decomposition and carbon mineralization rates, predicting the magnitude and future patterns of soil respiration is difficult due to multiple interacting direct and indirect effects. In particular, we lack mechanistic data on how low temperatures impact extracellular enzyme activities and thereby determine carbon supply rates to respiration. For this research, I performed two laboratory soil incubations designed to measure the temperature responses of enzymes catalyzing the terminal steps in Arctic tundra soil organic matter depolymerization. These experiments were designed to first characterize microbial activity responses to temperature based on cumulative carbon loss, and then to identify how substrate and nutrient availability mediate indirect temperature responses. In the first experiment, tundra soils were incubated across a temperature gradient from 4 - 20 °C and subsequently harvested at four time points at comparable levels of cumulative carbon loss. Comparing temperature effects on respiration rates as they changed with greater substrate depletion, respiration temperature sensitivity declined over iii time, likely due to declining substrate availability at higher temperatures. In contrast, enzyme temperature sensitivity increased over time, an apparent consequence of increased enzyme production at higher temperatures. These results indicate that carbon flow from depolymerization may not be high enough to sustain microbial activity below 10 °C and may explain observations of unexpectedly high increases in soil respiration with temperature in this range. In a second experiment, labile carbon was added with and without nutrients to tundra soils incubated at 8 and 16 °C and subsequently harvested at three points based on cumulative carbon loss from control soils. Respiration temperature sensitivity increased following labile carbon addition, indicating low substrate availability suppressed temperature responses from control soils. Temperature limitations to enzyme production persisted across all treatments, suggesting limitations to enzyme production may be due to lower microbial demand at low temperatures. Overall, results from this research demonstrate a number of indirect temperature effects on enzyme production and carbon availability that are currently unaccounted for in predictive Earth system models. Furthermore, they suggest that both enzyme production and activity are likely to increase as Arctic soils warm, two mechanisms by which temperature rise may increase carbon transfer from tundra soils to the atmosphere. iv Acknowledgements Thank you to my advisor, Michael Weintraub as well as my committee members, Daryl Moorhead and Patrick Sullivan for challenging me and supporting all my work at the University of Toledo. Thank you also to the past and present members of the Ecosystem and Soil Ecology Lab including Cameron McMillan, Jessica R. Susser, Kristie Bowersox, Jason Broadwater, Michala Burke, Ami Fofana, Somier Martin, and Jessica Swedik without whom, this work would not be possible. For their support in the field, thank you to Madeline Stokes, Jocelyn Cramer, and Maryann Ramos. Finally, I would like to acknowledge the National Science Foundation for funding this research through the Office of Polar Programs grant #1503939. v Table of Contents Abstract .............................................................................................................................. iii Acknowledgements ..............................................................................................................v Table of Contents ............................................................................................................... vi List of Tables ................................................................................................................... ix List of Figures ......................................................................................................................x List of Abbreviations ........................................................................................................ xii List of Symbols ................................................................................................................ xiii 1 Diverging Temperature Responses of Enzyme Production Allowing for Greater Carbon Release at High Temperature ......................................................................1 1.1 Introduction .......................................................................................................1 1.2 Methods ........................................................................................................17 1.2.1 Study Area .......................................................................................17 1.2.2 Soil Sampling and Processing ..........................................................17 1.2.3 Lab Incubations ................................................................................18 1.2.4 Microbial Respiration ......................................................................20 1.2.5 Destructive Harvests and Extractions ..............................................21 1.2.6 Nutrient Assays ................................................................................23 1.2.7 Extracellular Enzyme Assays ..........................................................24 1.2.8 Statistical Analysis ...........................................................................26 vi 1.3 Results ........................................................................................................28 1.3.1 Respiration and Cumulative C Loss ................................................28 1.3.2 Nutrient Concentrations and Microbial Biomass .............................30 1.3.3 Enzyme Activities ............................................................................32 1.4 Discussion .......................................................................................................46 1.4.1 Temperature Sensitivity of Enzyme Activities ................................46 1.4.2 Temperature Sensitivity of Respiration ...........................................52 1.4.3 Conclusions ......................................................................................54 2 Substrate and Nutrient Availability Mediat Microbial Activity Temperature Responses ........................................................................................................56 2.1 Introduction .....................................................................................................56 2.2 Methods ........................................................................................................72 2.2.1 Study Area .......................................................................................72 2.2.2 Soil Sampling and Processing ..........................................................72 2.2.3 Lab Incubations ................................................................................73 2.2.4 Microbial Respiration ......................................................................75 2.2.5 Destructive Harvests and Extractions ..............................................75 2.2.6 Nutrient Assays ................................................................................78 2.2.7 Extracellular Enzyme Assays ..........................................................79 2.2.8 Data Analysis ...................................................................................82 2.3 Results ........................................................................................................85 2.3.1 Respiration and Cumulative C Loss ................................................85 2.3.2 Microbial Biomass C, N, and Phosphate .........................................90 vii 2.3.3 Nutrient Concentrations ...................................................................92 2.3.4 Enzyme Activities ............................................................................96 2.4 Discussion .....................................................................................................105 2.4.1 Substrate-Limited Temperature Responses ...................................105 2.4.2 Potential for Nutrient Limitation ...................................................109
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