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Impact of Plant Species, N Fertilization and Ecosystem Engineers on the Structure and Function of Soil Microbial Communities

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Impact of Plant Species, N Fertilization and Ecosystem Engineers on the Structure and Function of Soil Microbial Communities IMPACT OF PLANT SPECIES, N FERTILIZATION AND ECOSYSTEM ENGINEERS ON THE STRUCTURE AND FUNCTION OF SOIL MICROBIAL COMMUNITIES Dissertation zur Erlangung des mathematisch-naturwissenschaftlichen Doktorgrades "Doctor rerum naturalium" der Georg-August-Universität Göttingen im Promotionsprogramm Biologie der Georg-August University School of Science (GAUSS) vorgelegt von Birgit Pfeiffer aus Forst/ Lausitz Göttingen 2013 Betreuungsausschuss Prof. Dr. Rolf Daniel, Genomische und angewandte Mikrobiologie, Institut für Mikrobiologie und Genetik; Georg-August-Universität Göttingen PD Dr. Michael Hoppert, Allgemeine Mikrobiologie, Institut für Mikrobiologie und Genetik; Georg-August-Universität Göttingen Mitglieder der Prüfungskommission Referent/in: Prof. Dr. Rolf Daniel, Genomische und angewandte Mikrobiologie, Institut für Mikrobiologie und Genetik; Georg-August-Universität Göttingen Korreferent/in: PD Dr. Michael Hoppert, Allgemeine Mikrobiologie, Institut für Mikrobiologie und Genetik; Georg-August-Universität Göttingen Weitere Mitglieder der Prüfungskommission: Prof. Dr. Hermann F. Jungkunst, Geoökologie / Physische Geographie, Institut für Umweltwissenschaften, Universität Koblenz-Landau Prof. Dr. Stefanie Pöggeler, Genetik eukaryotischer Mikroorganismen, Institut für Mikrobiologie und Genetik, Georg-August-Universität Göttingen Prof. Dr. Stefan Irniger, Molekulare Mikrobiologie und Genetik, Institut für Mikrobiologie und Genetik, Georg-August-Universität Göttingen Jun.-Prof. Dr. Kai Heimel, Molekulare Mikrobiologie und Genetik, Institut für Mikrobiologie und Genetik, Georg-August-Universität Göttingen Tag der mündlichen Prüfung: 20.12.2013 Two things are necessary for our work: unresting patience and the willingness to abandon something in which a lot of time and effort has been put. Albert Einstein, (Free translation from German to English) Dedicated to my family. Table of contents Table of contents Table of contents I List of publications III A. GENERAL INTRODUCTION 1 1. BIODIVERSITY AND ECOSYSTEM FUNCTIONING AS IMPORTANT GLOBAL ISSUES 1 2. THE ROLE OF FOREST SOILS AS ECOSYSTEM AND MICROBIAL HABITAT 2 3. PARAMETERS INFLUENCING SOIL MICROBIAL COMMUNITY COMPOSITION AND ACTIVITY 4 3.1. EFFECT OF PLANT SPECIES IDENTITY AND DIVERSITY ON SOIL MICROBIAL COMMUNITIES 6 3.2. IMPACT OF ANTS ON SOIL MICROBIAL COMMUNITY COMPOSITION 7 4. 16S RRNA AND 16S RRNA GENES AS MOLECULAR MARKERS IN MICROBIAL ECOLOGY STUDIES 8 5. OBJECTIVES OF THIS THESIS 9 6. REFERENCES 11 B. PUBLICATIONS 22 B.I EFFECT OF TREE SPECIES IDENTITY, TREE SPECIES DIVERSITY, LEAF LITTER PRESENCE, AND SAMPLING TIME ON SOIL MICROBIAL COMMUNITIES 23 1. LEAF LITTER IS THE MAIN DRIVER FOR CHANGES IN BACTERIAL COMMUNITY STRUCTURES IN THE RHIZOSPHERE OF ASH AND BEECH 24 1.1. Supplementary data 36 2. ROOTS FROM BEECH (FAGUS SYLVATICA L.) AND ASH (FRAXINUS EXCELSIOR L.) DIFFERENTIALLY AFFECT SOIL MICROORGANISMS AND CARBON DYNAMICS 55 2.1. Supplementary data 66 3. TREE EFFECTS ON DIVERSITY AND STRUCTURE OF SOIL BACTERIAL AND FUNGAL COMMUNITIES 71 B.II IMPACT OF N FERTILIZATION ON SOIL MICROBIAL COMMUNITIES AND GREENHOUSE GAS FLUXES 86 I Table of contents 1. THE INHIBITING EFFECT OF NITRATE FERTILIZATION ON METHANE UPTAKE OF A TEMPERATE FOREST SOIL IS INFLUENCED BY LABILE CARBON 87 2. N FERTILIZATION SHAPES THE COMPOSITION AND DIVERSITY OF ACTIVE SOIL BACTERIAL COMMUNITIES 99 3. COMBINED EFFECTS OF NITRATE AND LABILE C ON THE N2O EMISSIONS OF A TEMPERATE FOREST SOIL 138 B.III INFLUENCE OF LASIUS ANTS ACTING AS ECOSYSTEM ENGINEERS 168 1. NUTRIENT FLOW FROM ABOVEGROUND TO BELOWGROUND SYSTEMS AND CHANGES IN SOIL MICROBIAL COMMUNITY DRIVEN BY ANTS AND HOMOPTERAN HONEYDEW 169 1.1. Supplementary data 195 2. INFLUENCE OF LASIUS ANTS ON SOIL MICROBIAL COMMUNITIES IN GRASSLANDS – A FUNCTIONAL AND MOLECULAR APPROACH 200 B.IV MICROBIAL COMMUNITIES INHABITING BIOLOGICAL SOIL CRUSTS 218 1. BACTERIAL DIVERSITY IN BIOLOGICAL SOIL CRUSTS FROM EXTRAZONAL MOUNTAIN DRY STEPPES IN NORTHERN MONGOLIA 219 C. DISCUSSION 233 1. EFFECT OF TREE SPECIES IDENTITY, TREE SPECIES DIVERSITY, LEAF LITTER PRESENCE, AND SAMPLING TIME EFFECTS ON SOIL MICROBIAL COMMUNITIES 234 2. IMPACT OF RISING NITROGEN DEPOSITION INTO FOREST SOILS ON BACTERIAL ACTIVITY AND COMMUNITY COMPOSITION 238 3. INFLUENCE OF LASIUS ANTS ACTING AS ECOSYSTEM ENGINEERS 243 4. CONCLUSION 244 5. REFERENCES 246 D. SUMMARY 253 Acknowledgments 255 Curriculum vitae 257 II List of publications List of publications Fender, AC., Pfeiffer, B., Gansert, D., Leuschner, C., Daniel, R. and Jungkunst, HF. The inhibiting effect of nitrate fertilisation on methane uptake of a temperate forest soil is influenced by labile carbon. Biology and Fertility of Soils, 2012, Volume 48, Number 6, Pages 621-631 Kemmling, A., Pfeiffer, B., Daniel, R. and Hoppert, M. Bacterial diversity in biological soil crusts from extrazonal mountain dry steppes in northern Mongolia. Erforschung biologischer Ressourcen der Mongolei, 2012, Volume 12, Pages 437-449 Cesarz, S., Fender, AC., Beyer, F., Valtanen, K., Pfeiffer, B., Gansert, D., Hertel, D., Polle, A., Daniel, R., Leuschner C. and Scheu, S. Roots from beech (Fagus sylvatica L.) and ash (Fraxinus excelsior L.) differentially affect soil microorganisms and carbon dynamics. Soil Biology and Biochemistry, 2013, Volume 61, Pages 23-32 Pfeiffer, B., Fender, AC., Lasota, S., Jungkunst, HF., and Daniel, R. Leaf litter is the main driver for changes in bacterial community structures in the rhizosphere of ash and beech. Applied Soil Ecology, 2013, Volume 72, Pages 150-160 III A. General introduction “On any possible, reasonable or fair criterion, bacteria are – and always have been – the dominant forms of life on Earth. “ S. J. Gould (1941–2002) (paleontologist and evolutionary biologist) A. General introduction 1. Biodiversity and ecosystem functioning as important global issues Biodiversity was defined within the third Global Biodiversity Outlook (2010) as the variability among living organisms from all sources including, inter alia, terrestrial, marine and other aquatic ecosystems and the ecological complexes of which they are part. This includes diversity within species, between species and of ecosystems. Biodiversity can be measured as richness, evenness and heterogeneity. Richness is a measure of the number of unique life forms, evenness is a measure of the equitability among life forms, and heterogeneity is the measure of the dissimilarity among life forms (Cardinale et al. 2012). Biodiversity and ecosystem functioning are closely related. Ecosystem functions are processes that control energy, nutrient and organic matter fluxes such as the decomposition of dead plant material and the recycling of essential nutrients within an environment (Cardinale et al. 2012). Consequences of changes in biodiversity, especially loss in biodiversity, were mainly studied with respect to plant and animal diversity (Chapin et al. 2000; Loreau et al. 2001; Petchey and Gaston 2002; Ives and Carpenter 2007; Hooper et al. 2012). Species diversity affects the function of ecosystems as well as the resilience and resistance of ecosystems to environmental changes (Chapin et al. 2000). Furthermore, biodiversity buffering environmental variations such as climate changes, increasing nitrogen depositions and carbon dioxide emissions enhances the efficiency and stability of ecosystem processes with time (Cardinale et al. 2012). A decrease in species diversity might force populations to a point where they become more and more vulnerable until they finally collapse. As a consequence, ecosystem functions could also collapse, when lost activities of particular organisms cannot be buffered, recovered or replaced by other species. Balvanera et al. (2006) found in a meta-analysis of 103 publications biodiversity effects to be weaker at the ecosystem than the community level and further to be negative at the population level. Within numerous experiments on effects of biodiversity loss, artificial gradients with respect to grassland plant diversity were 1 A. General introduction analyzed (Tilman et al. 1996; Palmborg et al. 2005; Spehn et al. 2005; Tilman et al. 2006), but so far only a few studies explored artificial or natural gradients in forest tree diversity (Hooper et al. 2005; Leuschner et al. 2009; Jacob et al. 2010a). Furthermore, investigations on the relationship between biodiversity and ecosystem functions mainly focused on aboveground systems. Significant effects of biodiversity on the decomposer fauna were found by analyzing aboveground and belowground systems in grasslands (Scherber et al. 2010; Eisenhauer et al. 2012). The linkage between aboveground and belowground systems was rarely studied, especially with respect to forests and forest soils. 2. The role of forest soils as ecosystem and microbial habitat The habitat soil, the so called pedosphere, is known as probably the most complex habitat on earth. It represents an enormously diverse, multifunctional and multicomponent system. Soils differ in organic and inorganic compounds, pore size, texture, and pH. They are composed of mineral particles differing in size, shape and chemical composition, various stages of decomposed soil organic matter (SOM), soil gases and water, as well as dissolved minerals and dissolved organic matter (DOM) (Brady and Weil 2002). Soils are inhabited by plant roots, soil fauna and microbiota. Furthermore, soils are important contributors to the global nutrient cycle, and represent sources as well as sinks of methane (CH4), nitrous oxide (N2O) and carbon dioxide (CO2). Especially
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