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Denitrification, Dissimilatory Nitrate Reduction, and Methanogenesis in the Gut of Earthworms (Oligochaeta): Assessment of Greenhouse Gases and Genetic Markers

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Denitrification, Dissimilatory Nitrate Reduction, and Methanogenesis in the Gut of Earthworms (Oligochaeta): Assessment of Greenhouse Gases and Genetic Markers Denitrification, Dissimilatory Nitrate Reduction, and Methanogenesis in the Gut of Earthworms (Oligochaeta): Assessment of Greenhouse Gases and Genetic Markers Dissertation To obtain the Academic Degree Doctor rerum naturalium (Dr. rer. nat.) Submitted to the Faculty of Biology, Chemistry, and Earth Sciences of the University of Bayreuth by Peter Stefan Depkat-Jakob Bayreuth, July 2013 This doctoral thesis was prepared at the Department of Ecological Microbiology, University of Bayreuth, from April 2009 until July 2013 supervised by Prof. PhD Harold Drake and co-supervised by PD Dr. Marcus Horn. This is a full reprint of the dissertation submitted to obtain the academic degree of Doctor of Natural Sciences (Dr. rer. nat.) and approved by the Faculty of Biology, Chemistry and Geosciences of the University of Bayreuth. Acting dean: Prof. Dr. Rhett Kempe Date of submission: 02. July 2013 Date of defence (disputation): 15. November 2013 Doctoral Committee: Prof. PhD H. Drake 1st reviewer Prof. Dr. O. Meyer 2nd reviewer Prof. Dr. G. Gebauer Chairman Prof. Dr. H. Feldhaar Prof. Dr. G. Rambold CONTENTS I CONTENTS FIGURES ......................................................................................................X TABLES ................................................................................................... XIII APPENDIX TABLES .................................................................................... XV EQUATIONS.............................................................................................. XVI ABBREVIATIONS, CHEMICAL FORMULAS, AND ENZYMES ........................... XVII 1. INTRODUCTION ....................................................................................... 1 1.1. Nitrous oxide and methane as potent greenhouse gases ...................................1 1.2. Microbial processes involved in the formation of N2O ........................................2 1.2.1. Denitrification.....................................................................................................4 1.2.1.1. Denitrification pathway and associated enzymes ........................................4 1.2.1.2. Organisms and regulation of denitrification ..................................................8 1.2.2. Dissimilatory reduction of nitrate to ammonium ...........................................10 1.2.3. Molecular analysis of denitrifiers and dissimilatory nitrate reducers ..........11 1.2.4. Nitrification .......................................................................................................12 1.3. Methanogenesis as the main biotic source of CH4 ............................................13 1.4. Earthworms ..........................................................................................................16 1.4.1. Diversity, habitats and feeding guilds of earthworms ..................................16 1.4.2. Ecological relevance of earthworms ..............................................................17 1.4.3. Digestive system of earthworms and microorganisms as part of their nutrition ............................................................................................................19 1.4.4. Microorganisms associated with the earthworm digestive system .............21 1.4.5. Emission of N2O and CH4 by earthworms ......................................................23 1.5. Hypotheses and Objectives .................................................................................25 2. MATERIALS AND METHODS ................................................................... 26 2.1. Location and sampling of earthworms and their soils and other substrates ............................................................................................................26 2.1.1. Brazil .................................................................................................................26 2.1.1.1. Earthworms ...............................................................................................26 2.1.1.2. Millipedes ..................................................................................................27 2.1.2. Germany ...........................................................................................................30 II CONTENTS 2.1.3. New Zealand .....................................................................................................31 2.2. Experiments with living earthworms, their soils and substrates, dissected earthworm guts, and gut contents ....................................................32 2.2.1. Incubation experiments with living earthworms............................................32 2.2.1.1. Additional N2O emission experiments........................................................32 2.2.1.2. Additional CH4 emission experiments ........................................................33 2.2.2. Incubation experiments with dissected earthworm guts ..............................33 2.2.3. Incubation experiments with earthworm gut contents..................................34 2.2.3.1. Brazil .........................................................................................................34 2.2.3.1.1. Denitrification experiments ...................................................................34 2.2.3.1.2. Methanogenesis experiments ..............................................................34 2.2.4. Preparation of earthworm gut contents for other experiments ....................35 2.2.4.1. Brazil .........................................................................................................35 2.2.4.2. Germany ...................................................................................................35 2.2.4.3. New Zealand .............................................................................................36 2.2.5. Millipedes .........................................................................................................36 2.3. Microbiological methods .....................................................................................36 2.3.1. Growth media and plates for cultivation and cloning ...................................36 2.3.1.1. Solutions ...................................................................................................36 2.3.1.1.1. Anoxic water ........................................................................................36 2.3.1.1.2. Phosphate buffer ..................................................................................36 2.3.1.1.3. Mineral salts DE-A ...............................................................................37 2.3.1.1.4. Mineral salts DE-B ...............................................................................37 2.3.1.1.5. Mineral salts ME ..................................................................................37 2.3.1.1.6. Trace elements DE ..............................................................................38 2.3.1.1.7. Trace elements ME ..............................................................................38 2.3.1.1.8. Vitamins DE .........................................................................................39 2.3.1.1.9. Vitamins ME-A .....................................................................................39 2.3.1.1.10. Vitamins ME-B .....................................................................................40 2.3.1.1.11. Carbon sources ....................................................................................40 2.3.1.1.12. Nitrite ...................................................................................................40 2.3.1.1.13. Nitrate ..................................................................................................41 CONTENTS III 2.3.1.1.14. Combined C-sources and vitamins .......................................................41 2.3.1.1.15. Combined C-sources, vitamins, and nitrate ..........................................41 2.3.1.1.16. Soil extract ...........................................................................................42 2.3.1.1.17. Earthworm extract ................................................................................42 2.3.1.2. Liquid media and media plates ..................................................................42 2.3.1.2.1. DE/NO2 medium used for the isolation of denitrifiers ...........................42 2.3.1.2.2. DE/N2O-medium used for the isolation of denitrifiers ...........................43 2.3.1.2.3. DE-plates to maintain isolates under oxic conditions ............................43 2.3.1.2.4. DE/ISO-medium for growth experiments with isolates ..........................44 2.3.1.2.5. DE/ISO/NO3-medium for growth experiments with isolates ..................45 2.3.1.2.6. RUP-medium for the enrichment and isolation of methanogens ...........45 2.3.1.2.7. SOC medium .......................................................................................46 2.3.1.2.8. LB (lysogeny broth) plates ....................................................................46 2.3.1.2.9. LB plates with ampicillin/IPTG/X-Gal ....................................................47 2.3.2. Cultivation and growth experiments ..............................................................47 2.3.2.1. Isolation of denitrifiers ...............................................................................47 2.3.2.2. Growth experiments under oxic and anoxic condition with Isolate 201 and Isolate 208..........................................................................................48
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