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Element Use and Acquisition Strategies in Biological Soil Crusts by Kathryn Alexander Noonan A Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Approved May 2012 by the Graduate Supervisory Committee: Hilairy Hartnett, Chair Ferran Garcia-Pichel Ariel Anbar Thomas Sharp Everett Shock ARIZONA STATE UNIVERSITY May 2012 ABSTRACT Biological soil crusts (BSCs) are critical components of arid and semiarid environments and provide the primary sources of bioavailable macronutrients and increase micronutrient availability to their surrounding ecosystems. BSCs are composed of a variety of microorganisms that perform a wide range of physiological processes requiring a multitude of bioessential micronutrients, such as iron, copper, and molybdenum. This work investigated the effects of BSC activity on soil solution concentrations of bioessential elements and examined the microbial production of organic chelators, called siderophores. I found that aluminum, vanadium, copper, zinc, and molybdenum were solubilized in the action of crusts, while nickel, zinc, arsenic, and zirconium were immobilized by crust activity. Potassium and manganese displayed behavior consistent with biological removal and mobilization, whereas phosphorus and iron solubility were dominated by abiotic processes. The addition of bioavailable nitrogen altered the effects of BSCs on soil element mobilization. In addition, I found that the biogeochemical activites of BSCs were limited by molybdenum, a fact that likely contributes to co- limitation by nitrogen. I confirmed the presence of siderophore producing microbes in BSCs. Siderophores are low-molecular weight organic compounds that are released by bacteria to increase element solubility and facilitate element uptake; siderophore production is likely the mechanism by which BSCs affect the patterns I observed in soil solution i element concentrations. Siderophore producers were distributed across a range of bacterial groups and ecological niches within crusts, suggesting that siderophore production influences the availability of a variety of elements for use in many physiological processes. Four putative siderophore compounds were identified using electrospray ionization mass spectrometry; further attempts to characterize the compounds confirmed two true siderophores. Taken together, the results of my work provide information about micronutrient cycling within crusts that can be applied to BSC conservation and management. Fertilization with certain elements, particularly molybdenum, may prove to be a useful technique to promote BSC growth and development which would help prevent arid land degradation. Furthermore, understanding the effects of BSCs on soil element mobility could be used to develop useful biomarkers for the study of the existence and distribution of crust-like communities on ancient Earth, and perhaps other places, like Mars. ii TABLE OF CONTENTS Page LIST OF TABLES ..........................................................................viii LIST OF FIGURES......................................................................... ix ACKNOWLEDGEMENTS............................................................... x CHAPTER 1 OVERVIEW............................................................................. 1 References ......................................................................... 15 2 EFFECT OF NITROGEN-FIXING BIOLOGICAL SOIL CRUSTS ON SOIL SOLUTION TRACE METAL CONCENTRATIONS....................................................... 20 Abstract .............................................................................. 20 Introduction......................................................................... 21 Methods.............................................................................. 26 Field Site & Sample Collection....................................... 26 Experimental Setup ....................................................... 26 Soil Solution Processing ................................................ 30 Acetylene Reduction Assays ......................................... 31 Data Processing & Presentation .................................... 33 Results................................................................................ 35 Nitrate............................................................................ 35 Ammonium .................................................................... 37 Iron................................................................................ 41 iii CHAPTER Page Molybdenum.................................................................. 41 Vanadium ...................................................................... 41 Acetylene Reduction...................................................... 43 Discussion .......................................................................... 45 Effect of BSCs on Soil Solution Nutrient Concentrations .............................................................. 45 Influence of Nitrogen Availability on Soil Solution Trace Metal Concentrations..................................................... 51 Implications......................................................................... 55 References ......................................................................... 56 3 EVIDENCE FOR MICROBIAL UPTAKE AND SOLUBILIZATION OF BIOESSENTIAL ELEMENTS IN BIOLOGICAL SOIL CRUSTS........................................... 65 Abstract .............................................................................. 65 Introduction......................................................................... 66 Methods.............................................................................. 77 Soil Collection................................................................ 77 Experimental Design...................................................... 77 Trace Metal Analysis ..................................................... 80 Data Processing ............................................................ 81 Statistical Analysis......................................................... 83 Results................................................................................ 84 iv CHAPTER Page Week 1 Trends .............................................................. 84 Crusted Samples...................................................... 84 Killed Controls.......................................................... 91 Week 2 Trends .............................................................. 91 Crusted Samples...................................................... 91 Killed Controls.......................................................... 92 Week 1 vs Week 2......................................................... 92 Crusted Samples...................................................... 92 Killed Controls.......................................................... 93 Discussion .......................................................................... 94 Explanations for Changes in Concentration During Week 1 and Week 2 ................................................................... 94 Evidence for Biological Processes............................ 96 Evidence for Abiotic Processes .............................. 104 Effect of Nitrogen and Molybdenum Addition in Crusted Samples ...................................................................... 108 Summary & Implications ................................................... 113 References ....................................................................... 115 4 MOLYBDENUM LIMITS NITROGEN FIXATION IN BIOLOGICAL SOIL CRUSTS......................................... 126 Abstract ............................................................................ 126 Introduction....................................................................... 126 v CHAPTER Page Methods............................................................................ 133 Crust Collection and Storage ....................................... 133 Experimental Design.................................................... 133 Statistical Analysis....................................................... 136 Results.............................................................................. 136 Pre-Treatment Rate Comparison................................. 136 Water Treatment.......................................................... 137 Molybdenum Treatment............................................... 137 Discussion ........................................................................ 139 References ....................................................................... 145 5 DESERT BIOLOGICAL SOIL CRUSTS HOST NOVEL SIDEROPHORE-PRODUCING MICROORGANISMS.... 155 Abstract ............................................................................ 155 Introduction....................................................................... 156 Methods............................................................................ 160 Soil Collection.............................................................. 160 Culture Techniques and CAS Assay............................ 161 Siderophore Producer Identification............................. 163 Pyrosequencing........................................................... 164 Results.............................................................................. 165 Culturing and O-CAS................................................... 165 SIderophore Producer Identification............................
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