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Soil Fungal Communities Associated with Plant Health As Revealed By SOIL FUNGAL COMMUNITIES ASSOCIATED WITH PLANT HEALTH AS REVEALED BY NEXT-GENERATION SEQUENCING LIHUI XU PhD THESIS • SCIENCE AND TECHNOLOGY • 2011 SOIL FUNGAL COMMUNITIES ASSOCIATED WITH PLANT HEALTH AS REVEALED BY NEXT-GENERATION SEQUENCING LIHUI XU PhD thesis • science anD technology • 2011 Department of Agroecology Science and Technology Aarhus University Forsøgsvej 1 4200 Slagelse Tryk: www.digisource.dk ISBN: 978-87-91949-99-9 Ph.d_58448_Lihui_Xu.indd 3 02/12/11 10.25 Preface This thesis is submitted to fulfill the requirements for obtaining the Ph.D. degree at the Faculty of Science and Technology, Aarhus University. The Ph.D. project was carried out at Research Centre Flakkebjerg, Department of Agroecology, Faculty of Science and Technology, Aarhus University. The present project is based on three main experimental studies resulted in three manuscripts: (i) Influence of DNA extraction and PCR amplification on amplicon sequencing-based studies of soil fungal communities; (ii) Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing; (iii) Fungal community structure in roots, rhizosphere, and bulk soil associated with plant health as examined by deep amplicon sequencing. I would like to acknowledge all the people who have been helping me in various ways. Foremost, I would like to express my sincere gratitude to my principle supervisor Dr. Mogens Nicolaisen. His enthusiasm, inspiration, and expert guidance helped me throughout all the time of my research and thesis writing. I am also greatly indebted to my co-supervisors Dr. Sabine Ravnskov and Dr. John Larsen for their thoughtful guidance, wise advice, and enormous encouragement during my Ph.D. study. It has been a great pleasure working with such a great supervising group. I am very thankful to all of the technical staff, Anne-Pia Larsen, Ellen Frederiksen, Henriette Nyskjold, Jette Them Lilholt, Steen Meier, and Tina Tønnersen for excellent technical assistance in the laboratory and in the greenhouse. My special thanks go to Kristian Kristensen, Niels Holst, and Bernd Wollenweber for their valuable advice on statistical analysis. I sincerely acknowledge Karen O´Hanlon, Stephanie Walter, and Kirsten Jensen for indispensable proofreading of the thesis and manuscripts. I would like to thank all the colleagues and friends at Research Centre Flakkebjerg for their kind assistance and for providing a pleasant working environment. i I send special thanks to Valeria Bianciotto, Erica Lumini, and Alberto Orgiazzi at University of Turin, Italy for giving great suggestions on sequence analysis. I am grateful to Professor Jo Handelsman and the entire Handelsman Lab at Yale University for their hospitality and for inspiring me in my work. It was my immense pleasure to stay in your lab. During the three months stay, I managed to generate new amplicon libraries for pyrosequencing and to learn techniques for sequence analysis. Last but not least, I would like to thank my beloved family and friends for their continuous love and tremendous support at all time. Lihui Xu October 2011 ii Contents Summary ....................................................................................................................... 1 Sammendrag ................................................................................................................. 3 1 Introduction ............................................................................................................... 5 1.1 The soil environment .......................................................................................... 5 1.1.1 Physical, chemical, and biological components ......................................... 5 1.1.2 Soil functions ................................................................................................ 6 1.1.3 Soil health ..................................................................................................... 7 1.1.4 Root and rhizosphere .................................................................................. 9 1.2 Soil fungi............................................................................................................ 10 1.2.1 Taxonomic groups of soil fungi ................................................................ 11 1.2.2 Soil fungal life cycles .................................................................................. 12 1.2.3 Role of fungi in the soil ecosystem ............................................................ 12 1.2.4 Soil fungal diversity ................................................................................... 14 1.3 Soil-borne pathogens ........................................................................................ 16 1.3.1 Pea root diseases caused by soil-borne fungal pathogens ...................... 16 1.3.2 Interactions among fungal pathogens ...................................................... 18 1.3.3 Management of soil-borne pathogens ...................................................... 19 1.4 Methods to study soil fungal diversity ............................................................ 21 1.4.1 Classical and biochemical-based techniques ........................................... 21 1.4.2 Molecular-based techniques: DNA fingerprinting and microarray ..... 23 1.4.3 Sequencing techniques .............................................................................. 28 1.5 Motivation and objectives ................................................................................ 37 2 Paper I. Influence of DNA extraction and PCR amplification on studies of soil fungal communities based on amplicon sequencing ............................................... 39 iii 3 Paper II. Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing ................................................... 51 4 Paper III. Fungal community structure in roots, rhizosphere, and bulk soil associated with plant root health as examined by deep amplicon sequencing ..... 73 5 General discussion ................................................................................................ 127 6 Conclusions and further perspectives ................................................................. 131 References ................................................................................................................. 135 iv Summary This project investigated fungal communities associated with plant root health in agricultural soils using next-generation amplicon sequencing. Initially, DNA extraction and PCR effects on the variation of read abundances of pyrosequencing generated operational taxonomic units (OTUs) were investigated using soil samples from a pea field. Results showed that species richness was consistent among replicates. Variation among dominant OTUs was low across replicates, whereas rare OTUs showed higher variation among replicates. Results further indicated that pooling of several DNA extractions and PCR amplicons will decrease variation among samples. Soil fungal communities along a soil health gradient in nine pea field soils were explored. Soil fungal communities from each soil were different and were strongly dominated by Ascomycota and Basidiomycota. Several soil-borne fungal pathogens were detected in the bulk soil. Phoma, Podospora, Pseudaleuria and Veronaea, at the genus level, correlated to the disease severity index (DSI) of pea roots; Phoma was most abundant in soils with high DSI, whereas Podospora, Pseudaleuria, and Veronaea were most abundant in soils with low DSI. Fungal communities in pea plant roots, the surrounding rhizosphere, and bulk soil from three pea fields were examined in relation to root health. Fungal diversity in terms of richness was highest in bulk soil and lowest in roots. Fungal communities in all samples were strongly dominated by Dikarya and differed significantly among the three environments. Fusarium oxysporum and Aphanomyces euteiches were the likely causes of pea root rot in the respective fields as assessed by pyrosequencing data and quantitative PCR. Glomus and Fusarium were significantly more abundant in roots, whereas Cryptococcus and Mortierella were almost exclusively found in rhizosphere and bulk soil. A clear correlation was demonstrated between health status of roots and their fungal communities. The results showed that fungal community structures are highly variable in response to the three different ecological niches, between healthy and diseased roots, and across different fields. The results presented in this project revealed a high diversity of fungal communities in agricultural soils and provided information on the different functional fungal groups, including pathogens, and their dynamics in relation to root health. This 1 knowledge will further improve the understanding of soil fungal communities with regard to plant diseases. 2 Sammendrag I dette projekt blev jordens svampesamfund undersøgt i relation til planters sundhed ved hjælp af amplicon pyrosekventering. Første blev effekten af DNA-ekstraktion og PCR på variation af mængderne af pyrosekventering genererede operationelle taksonomiske enheder (OTU) undersøgt i jordprøver fra en ærtemark. Resultaterne viste, at artsrigdommen var stabil mellem replikater. Variationen blandt dominerende OTU var lav på tværs af replikater, mens sjældne OTU viste højere variation. Resultaterne viser, at sammenlægning af flere DNA ekstraktioner og PCR produkter vil mindske variation blandt prøver.
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