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Research Collection Research Collection Doctoral Thesis Development and application of molecular tools to investigate microbial alkaline phosphatase genes in soil Author(s): Ragot, Sabine A. Publication Date: 2016 Permanent Link: https://doi.org/10.3929/ethz-a-010630685 Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library DISS. ETH NO.23284 DEVELOPMENT AND APPLICATION OF MOLECULAR TOOLS TO INVESTIGATE MICROBIAL ALKALINE PHOSPHATASE GENES IN SOIL A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) presented by SABINE ANNE RAGOT Master of Science UZH in Biology born on 25.02.1987 citizen of Fribourg, FR accepted on the recommendation of Prof. Dr. Emmanuel Frossard, examiner PD Dr. Else Katrin Bünemann-König, co-examiner Prof. Dr. Michael Kertesz, co-examiner Dr. Claude Plassard, co-examiner 2016 Sabine Anne Ragot: Development and application of molecular tools to investigate microbial alkaline phosphatase genes in soil, c 2016 ⃝ ABSTRACT Phosphatase enzymes play an important role in soil phosphorus cycling by hydrolyzing organic phosphorus to orthophosphate, which can be taken up by plants and microorgan- isms. PhoD and PhoX alkaline phosphatases and AcpA acid phosphatase are produced by microorganisms in response to phosphorus limitation in the environment. In this thesis, the current knowledge of the prevalence of phoD and phoX in the environment and of their taxonomic distribution was assessed, and new molecular tools were developed to target the phoD and phoX alkaline phosphatase genes in soil microorganisms. The newly- designed primers were then used to identify phoD- and phoX-harboring microorganisms and to explore the relationships between selected environmental factors and the phoD- and phoX-harboring community composition and structure in thirty sites across three land-uses and six soil types in Australia and Switzerland. Additionally, the total and active phoD-harboring community composition and structure as affected by phosphate depletion and pH were studied in a long-term fertilization trial in grassland characterized by a natural pH gradient on the site. The newly-designed primers amplified phoD and phoX in soil microorganisms with a good coverage and specificity. The phoD gene was found in 1 archaeal, 13 bacterial and 2 fungal phyla, and the phoX gene in 1 archaeal and 16 bacterial phyla. Dominant phoD- harboring phyla were Actinobacteria, Cyanobacteria, Deinococcus-Thermus, Firmicutes, Gemmatimonadetes, Planctomycetes and Proteobacteria, while abundant phoX-harboring phyla were Acidobacteria, Actinobacteria, Chloroflexi, Planctomycetes, Proteobacteria and Verrucomicrobia. The composition and structure of phoD- and phoX-harboring communities were significantly correlated with climate, soil group, land-use, pH and soil nutrient concentrations. However, the significance of these correlations differed in iii ABSTRACT intensity between the phoD- and the phoX-harboring community. Additionally, our case study in the long-term fertilization trial showed that the total and active phoD-harboring communities were on the whole composed of similar phyla with, however, different relative abundances. Furthermore, phosphate depletion affected the composition and structure of the active phoD-harboring community only, while soil pH impacted the composition and structure of both the total and active phoD-harboring community. Additionally, primers targeting the acpA acid phosphatase gene were designed and pre- liminary work was conducted on the same thirty sites used to study phoD and phoX. Our results suggest that acpA is not as widespread in bacteria as phoD and phoX. Dominant acpA-harboring orders included Burkholderiales, Methylococcales, Pseudomonadales and Rhizobiales. The primers designed in this thesis revealed a large diversity of phoD and phoX in soil and represent valuable tools to study phoD- and phoX-harboring communities in environmental samples. Despite differences in environmental factors, dominant phoD- harboring phyla were generally similar in all samples, while dominant phoX-harboring phyla differed substantially between the samples. Nonetheless, our results suggest that the composition and structure of the phoD- and the phoX-harboring communities are affected by the same environmental factors. iv RÉSUMÉ Les phosphatases jouent un rôle capital dans le cycle du phosphore dans le sol. En tant qu’enzymes, elles catalysent l’hydrolyse des composés organiques phosphatés en orthophosphate, l’unique forme de phosphore disponible pour les plantes et les microor- ganismes du sol. Les phosphatases alcalines PhoD et PhoX et la phosphatase acidique AcpA sont sécrétées par des microorganismes. Elles hydrolysent essentiellement les phosphomonoesters qui représentent souvent le type de phosphore organique le plus abondant dans le sol. Dans ce travail de thèse, de nouveaux outils moléculaires ciblant les gènes des phosphatases alcalines phoD et phoX dans les microorganismes du sol ont été développés. Ces outils ont par la suite été utilisés dans trente sols classés en cinq groupes différent et incluant trois types d’utilisation du sol en Australie et en Suisse, afin d’identifier les microorganismes clés ayant les gènes phoD et phoX et d’explorer les liens entre la structure et la composition de la communauté possédant ces genes et les éléments environnementaux. De plus, un essai de fertilisation phosphatée de longue durée dans une prairie caractérisée par un gradient de pH naturel a permis l’étude des effets du l’appauvrissement en phosphate et du pH sur la composition et la structure des communautés active et totale ayant le gène phoD. Ces nouvelles amorces ont permis d’amplifier les gènes phoD et phoX chez les micro- organismes du sol avec une bonne spécificité et une bonne couverture de la diversité. Dans notre étude, le gène phoD était présent dans un phylum archéal, treize phyla bac- tériens et deux phyla fongiques, tandis que le gène phoX était présent dans un phylum archéal et seize phyla bactériens. Les phyla clés ayant le gène phoD incluaient des Actinobacteria, Cyanobacteria, Deinococcus-Thermus, Firmicutes, Gemmatimonadetes, Planctomycetes et Proteobacteria, tandis que les phyla clés ayant le gène phoX incluaient des Acidobacteria, Actinobacteria, Chloroflexi, Planctomycetes, Proteobacteria et Verru- v ABSTRACT comicrobia. La composition et la structure des communautés ayant les gènes phoD et phoX étaient significativement corrélées au climat, groupe de sol, type d’utilisation du sol, pH et concentrations de nutriments du sol. L’étude de cas dans l’essai de fertilisation phosphatée a montré que les communautés active et totale ayant le gène phoD étaient composées des mêmes phyla. De plus, alors que le pH influençait la composition et la structure des communautés active et totale possédant le gène phoD, l’appauvrissement en phosphate affectait uniquement la communauté active. De plus, des amorces amplifiant le gène acpA ont été développées et des étude prélim- inaires sur la prévalence et la composition du gène acpA dans les trente sols utilisés pour étudier les gènes phoD et phoX ont été menées. Nos résultats suggèrent que le gène acpA n’est pas aussi répandu dans les bactéries que les gènes phoD et phoX. Les ordres clés comprenant le gène acpA incluaient les Burkholderiales, Methylococcales, Pseudomonadales and les Rhizobiales. Les amorces développées dans cette thèse révèlent la grande diversité des micro- organismes du sol ayant les gènes phoD et phoX. En dépit des différences des éléments environnementaux, les phyla ayant le gène phoD étaient similaires, tandis que les phyla ayant le gène phoX variaient considérablement. Toutefois, nos résultats suggèrent que la composition et la structure des communautés ayant les gènes phoD et phoX sont influencées par les mêmes éléments environnementaux. Les nouvelles amorces présentées de ce travail sont de précieux outils pour étudier les communautés possédant les gènes phoD et phoX dans l’environment. vi ABBREVIATIONS ADONIS Analysis of Variance Using Distance Matrices ANOSIM Analysis of Dissimilarity ANOVA Analysis of Variance AMP Adenosine Monophosphate ATP Adenosine Triphosphate cAMP Cyclic Adenosine Monophosphate BLAST Basic Local Alignment Search Tool C Carbon CaCO3 Carbonate CD database Conserved Domain Database Cmic Microbial Carbon COG Clusters of Orthologous Groups DNA Deoxyribonucleic Acid ENA European Nucleotide Archive IMG/M database Integrative Microbial Genomes and Metagenomes Database MUSCLE MUltiple Sequence Comparison by Log-Expectation N Nitrogen NCBI National Center for Biotechnology Information NGS Next Generation Sequencing NMDS Non-Metric Dimensional Scaling Nmic Microbial Nitrogen P Phosphorus PCR Polymerase Chain Reaction Pres Resin-extractable Phosphorus Porg Organic Phosphorus qPCR Quantitative Real-Time PCR RDA Redundancy Analysis RNA Ribonucleic Acid SFF Standard Flowgram Format Sest Estimated Species Richness Sobs Observed Species Richness TAT Twin Arginine Translocation TC Total Carbon TOC Total Organic Carbon TP Total Phosphorus TN Total Nitrogen T-RFLP Terminal-Restriction Fragment Length Polymorphism vii CONTENTS ABSTRACT iii ABBREVIATIONS vii 1 GENERAL INTRODUCTION 1 1.1 Phosphorus in soil . 2 1.2 Phosphatases . 5 1.2.1 Phosphatase classes . 5 1.2.2 Alkaline and acid phosphatases . 6 1.2.3 Phosphatase gene regulation . 10 1.2.4 Reaction mechanisms of phosphatases
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