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Molecular Factors and Genetic Differences Defining Symbiotic Phenotypes of Galega Spp

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Molecular Factors and Genetic Differences Defining Symbiotic Phenotypes of Galega Spp Department of Food and Environmental Sciences University of Helsinki Helsinki Molecular factors and genetic differences defining symbiotic phenotypes of Galega spp. and Neorhizobium galegae strains Janina Österman ACADEMIC DISSERTATION To be presented, with the permission of the Faculty of Agriculture and Forestry of the University of Helsinki, for public examination in lecture hall 2, Viikki building B, Latokartanonkaari 7, on the 26th of June 2015, at 12 noon. Helsinki 2015 Supervisor: Professor Kristina Lindström Department of Environmental Sciences University of Helsinki, Finland Co-supervisors: Professor J. Peter W. Young Department of Biology University of York, England Docent David Fewer Department of Food and Environmental Sciences University of Helsinki, Finland Pre-examiners: Professor Katharina Pawlowski Department of Ecology, Environment and Plant Sciences Stockholm University, Sweden Docent Minna Pirhonen Department of Agricultural Sciences University of Helsinki, Finland Opponent: Senior Lecturer, Doctor Xavier Perret Department of Botany and Plant Biology Laboratory of Microbial Genetics University of Geneva, Switzerland Dissertationes Schola Doctoralis Scientiae Circumiectalis, Alimentarie, Biologicae ISSN 2342-5423 (print) ISSN 2342-5431 (online) ISBN 978-951-51-1191-3 (paperback) ISBN 978-951-51-1192-0 (PDF) Electronic version available at http://ethesis.helsinki.fi/ Hansaprint Vantaa 2015 Abstract Nitrogen is an indispensable element for plants and animals to be able to synthesise essential biological compounds such as amino acids and nucleotides. Although there is plenty of nitrogen in the form of nitrogen gas (N2) in the Earth’s atmosphere, it is not readily available to plants but needs to be converted (fixed) into ammonia before it can be utilised. Nitrogen-fixing bacteria living freely in the soil or in symbiotic association with legume plants, fix N2 into ammonia used by the plants. This is known as biological nitrogen fixation (BNF). In contrast to industrial nitrogen fixation, an energy-demanding process using high temperature and pressure to produce chemical fertilizers, BNF makes use of solar energy alone to complete the same reaction. However, the requirements on compatibility of plants and nitrogen- fixing micro-organism, the rate of conversion and the ability of the micro-organisms to survive in stressful environments are limiting factors of this system. The current demand for more sustainable food production makes BNF an attractive alternative. However, optimization of existing BNF systems as well as development of new highly productive ones is necessary, to be able to replace the use of chemical fertilisers. In order to develop new alternatives, we need to gain more knowledge on the requirements set by both plants and micro-organisms for successful and efficient nitrogen fixation to occur. In this thesis, the nitrogen-fixing legume host Galega (goat’s rue) and its symbiotic microbial partner Neorhizobium galegae were used as a model system to investigate the features defining good symbiotic nitrogen fixation. Studies of genetic diversity within the host plant showed that there are genetic traits making a distinction between the two species G. orientalis and G. officinalis, both at a whole-genome level and at the level of specific symbiosis-related genes. Genome sequencing of ten strains of N. galegae provided a useful dataset for studying i) the genomic features separating N. galegae from related nitrogen-fixing bacteria (rhizobia) and ii) the genetically encoded characteristics that divide strains of N. galegae into two separate symbiovars (symbiotic variants that show different phenotypes on the two different Galega host plant species). These studies provided new information on genes possibly involved in determining host specificity and efficiency of nitrogen fixation. In addition, previously unrecognised genetic contents provided insight into the ecology of N. galegae. Most importantly, genome sequencing enabled identification of the noeT gene, responsible for acetylation of the N. galegae Nod factor (signal molecule required for symbiosis). Although the noeT gene did not turn out to be the crucial determinant enabling nodulation of Galega spp. as previously anticipated, these results are important for future studies on mechanisms behind the selectiveness (host specificity) observed in nitogen-fixing symbioses between Galega and N. galegae. 3 Sammanfattning Växter och djur är beroende av kväve för att kunna syntetisera nödvändiga biologiska föreningar så som aminosyror och nukleotider. Även om det finns ett överflöd av kvävgas i atmosfären, kan växter inte använda sig av kvävgasen som sådan, utan den måste först omvandlas (fixeras) till ammoniak. Kvävefixerande bakterier har en naturlig förmåga att fixera kvävgas till fördel för växterna. Det här fenomenet kallas biologisk kvävefixering. Bakterierna kan antingen vara frilevande eller leva i symbios med baljväxter. I motsats till industriell kvävefixering, en energikrävande process som är beroende av hög temperatur och högt tryck för att binda kväve i kvävegödsel, utnyttjar biologisk kvävefixering enbart solenergi för samma reaktion. Biologisk kvävefixering begränsas å andra sidan av krav på kompatibilitet mellan värdväxter och kvävefixerande mikroorganismer, effektiviteten av kvävefixeringen samt mikroorganismernas förmåga att överleva under krävande förhållanden. Den rådande efterfrågan på mer hållbara sätt att producera mat för jordens befolkning gör biologisk kvävefixering ett attraktivt alternativ. För att kunna ersätta använding av industriellt kvävegödsel krävs ändå att existerande biologiska kvävefixeringssystem optimeras och att nya högproduktiva system utvecklas. Detta å sin sida förutsätter förbättrad kunskap om de krav som både växter och mikroorganismer ställer för att en lyckad, effektiv kvävefixering ska vara möjlig. I denna avhandling användes som modellsystem växt – bakterie paret Galega (getärt) och Neorhizobium galegae, som ingår kvävefixerande symbios med varandra, för att studera särdrag som är kännetecknande för en lyckad symbiotisk kvävefixering. Studier av den genetiska diversiteten inom värdväxten visade att genetiska drag skiljer de två arterna G. orientalis och G. officinalis åt, både då hela genomet beaktas och på ett plan av specifika symbiosrelaterade gener. Genomsekvensering av tio stammar av N. galegae tillhandahöll ett användbart dataset för att studera genetiska drag som dels skiljer N. galegae från närbesläktade kvävefixerande bakterier (rhizobier), dels delar in stammar av N. galegae i två symbiovarer (d.v.s. varianter av bakterien som uttrycker sig olika på de två olika värdväxtarterna av Galega). Dessa studier resulterade i ny information om gener som kan vara involverade i att bestämma värdväxtspecificiteten och effektivitetsgraden för kvävefixeringen. Dessutom identifierades genetiskt innehåll som ger ny information om bakteriens ekologi. Av största vikt var att genomsekvenseringen ledde till identifiering av genen noeT, som modifierar den så kallade Nod faktorn (en signalmolekyl som behövs för initiering av en fungerande symbios) hos N. galegae. Även om det visade sig att noeT inte spelar den avgörande rollen som möjliggör symbios med arter av Galega som tidigare antogs, så utgör dessa resultat en viktig grund för kommande studier av mekanismerna som bidrar till den selektivitet (värdväxtspecificitet) som präglar den kvävefixerande symbiosen mellan Galega och N. galegae. 4 Acknowledgements This work was mostly carried out at the excellent working facilities of the Department of Food and Environmental Sciences, University of Helsinki. The Department of Environmental Sciences, University of Helsinki, is acknowledged for providing office space during the final stage. Financial support was provided by the Academy of Finland (project 132544) and the Swedish Cultural Foundation in Finland (grant 13/7440-1304). I wish to thank my supervisors for supporting me through this work. My main supervisor Prof. Kristina Lindström always kept the door open, making it easy to discuss problems and choices to be made. Stina’s support and her faith in me have been important for my scientific development. During the seven weeks I spent in Prof. Peter Young’s group at the Univeristy of York I got a good introduction to the world of bioinformatics and genomics, and I am grateful for the discussions we had - the huge amount of information on rhizobia that Peter possesses is incredible. I also want to thank Doc. David Fewer for helping me with tricky bioinformatics and English editing especially at the beginning of my PhD studies. In addition to my official supervisors I am truly grateful for all the time and effort that Lars Paulin at the DNA Sequencing and Genomics lab has put into guiding me through genome sequencing and bioinformatics related to this. You were like a supervisor to me! Lasse also put me in contact with a number of persons without whom I could not have made it: Pia Laine and Juhana Kammonen from the sequencing lab and Per Johansson from the Department of Food Hygiene and Environmental Health. Pia did a great job with assembly of the two complete N. galegae genomes, but also managed to make work more fun with her sense of humor , so thank you - I really appreciated our little chats! Juhana deserves special thanks for patiently explaining every detail of genome assembly but also for always taking the time to help me out and provide nice detailed descriptions. I also greatly appreciate the guidance to
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