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THE ACTINORHIZAL SYMBIOSIS of the EARLIEST DIVERGENT FRANKIA CLUSTER Nguyen Thi Thanh Van

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THE ACTINORHIZAL SYMBIOSIS of the EARLIEST DIVERGENT FRANKIA CLUSTER Nguyen Thi Thanh Van THE ACTINORHIZAL SYMBIOSIS OF THE EARLIEST DIVERGENT FRANKIA CLUSTER Nguyen Thi Thanh Van The actinorhizal symbiosis of the earliest divergent Frankia cluster Nguyen Thi Thanh Van ©Nguyen Thi Thanh Van, Stockholm University 2017 ISBN print 978-91-7649-716-6 ISBN PDF 978-91-7649-717-3 Printed in Sweden by US-AB, Stockholm 2017 Distributor: Department of Ecology, Environment and Plant Sciences Stockholm University, Stockholm, Sweden Con kính tặng Ba Sammanfattning Under de senaste åren har allt större tonvikt lagts vid vikten av att utveckla en världsomspännande utvecklingsmässigt ekologiskt hållbar jordbruksnäring. Nödvändigheten av att minska beroendet av syntetiska kvävebaserade gödningsmedel har lett till ett alltmer växande forskningsfält baserat på vikten av biologisk kvävefixering, med emfas på rotknölsymbios. Mina studier har fokuserat på mekanismerna i och med actinorhizalsymbios, i.e den symbiotiska interaktionen mellan olika kvävefixerande actinobacteria -genus Frankia. i förhållande till en mycket skiftande grupp av växter från åtta olika växtfamiljer, som sammantaget kallas actinorhizalväxter. Frankia kluster II har visats vara en systerklad i förhållande till alla andra kluster, vilket gör att denna speciella gren kan ge insikt i hur Frankia kluster II kan tillföra värdefull information om den evolutionära bakgrunden i och med actinorhizalsymbios. Det första fullt sekvenserade genomet av en medlem från detta kluster, Candidatus Frankia datiscae Dg1 med ursprung från Pakistan, visar att genomet infattar nod generna nodABC som svarar för framställandet av lipochitooligosaccharid Nod-faktorer, vilket särskiljer denna medlem från andra grupper av Frankia som saknar dessa gener. Arbetet i och med denna avhandling är grundat på gDNA isolerat från sex inokula, tre från Nordamerika (USA; två från Kalifornien och ett från Alaska), ett från Europa (Frankrike), ett från Asien (Japan) och ett från Oceanien (Papua Nya Guinea). gDNA isolerades från rotknölar från Datisca glomerata (Datiscaceae), Ceanothus thyrsiflorus (Rhamnaceae), Coriaria myrtifolia och Coriaria arborea (Coriariaceae). Sammantaget sekvenserades tretton metagenom. Denna avhandling visar att de olika medlemarna i Frankia kluster II agerar som en grupp, vilket kan förklara förmågan att just kluster II kan nodulera en ovanligt stor och divers grupp av värdväxter, vilka innefattar fyra familjer från två ordningar. Det inokulum som isolerades från Papua Nya Guinea (den enda art från södra halvklotet som hittills sekvenserats), visade sig härbärgera en hittills okänd Frankia-art, som namngavs Candidatus Frankia meridionalis. Alla kluster II-arter studerade i detta arbete bär nod-generna nodABC i sitt genom, med undantag för den art som isolerats från Papua Nya Guinea vars genom enbart innehar nodB’C. Alla tre metagenom isolerade från USA innefattade dessutom en sulfotransferas-gen, nodH. Denna gen har visat sig vara uttryckt värdväxtspecifikt, då proteinet kunde spåras i rotknölar från värdväxten C. thyrsiflorus men inte i de knölar som isolerats från D. glomerata. Fylogenetiska analyser sammantagna med transposasfrekvensdata i våra analyserade genom ger starkt stöd till hypotesen att den utökade värdkretsen från Coriaria till Datisca för Frankia-arter i kluster II skedde i Euroasien samt att kluster II-arter kom till nordamerika via Berings sund. För att erhålla mer information om och hur värdväxten påverkar mikrosymbiontens molekylära reaktioner jämfördes metabolismen i rotknölar från D. glomerata (Cucurbitales) och C. thyrsiflorus (Rosales) på transkriptionsnivå. Det system som skyddar nitrogenas från de negativa effekterna av syre verkar vara mer effektivt i rotknölar från Ceanothus i jämförelse med hur systemet verkar i knölar från Datisca, enär bakteriernas kvävemetabolism sannolikt är likställd i samröret med båda växtarterna. Aminosyraextrakten från rotknölarna från D. glomerata visar att profilen utifrån kvävehaltiga aminosyror domineras av glutamat and arginin, vilket stöder hypotesen att Frankia utsöndrar kväve, troligen i form av arginin, speciellt anpassat för symbiosen med D. glomerata. Således visar våra data att arter från Frankia II särskiljer sig från andra Frankia-arter i hänseendet att deras repertoar av nod-gener och deras kvävemetabolism i symbios med sin värdväxt är specifikt annorlunda. List of publication This thesis is based on the following publications and manuscripts: I. Nguyen TV, Wibberg D, Battenberg K, Blom J, Vanden Heuvel B, Berry AM, Kalinowski J, Pawlowski K (2016) An assemblage of Frankia Cluster II strains from California con- tains the canonical nod genes and also the sulfotransferase gene nodH. BMC Genomics 17: 796. II. Nguyen TV, Wibberg D, Vigil-Stenman T, Battenberg K, Demchenko KN, Blom J, Fernandez MP, Yamanaka T, Berry AM, Kalinowski J, Brachmann A, Pawlowski K. Meta- genomes from the earliest divergent Frankia cluster: They come in teams. Manuscript III. Nguyen TV, Hilker R, Wibberg D, Battenberg K, Berry AM, Kalinowski J, Pawlowski K. Cucurbitales vs. Rosales: Anal- ysis of bacterial metabolism based on candidate gene expres- sion profiling in root nodules of Datisca glomerata and Cea- nothus thyrsiflorus. Manuscript IV. Persson T, Nguyen TV, Alloisio N, Pujic P, Berry AM, Nor- mand P, Pawlowski K (2016) The N-metabolites of roots and actinorhizal nodules from Alnus glutinosa and Datisca glom- erata: can D. glomerata change N-transport forms when nod- ulated? Symbiosis 70: 149-157 My contributions to these papers/manuscripts were as follows: I: Obtained the inoculum, grew and infected the plants, isolated the DNA, participated in the evaluation of the genome data, conducted and evaluated the RT-qPCR experiments, partici- pated in writing the manuscript II: Grew the plants and maintained the inocula, isolated the DNA, participated in the evaluation of the genome data, conducted and evaluated the RT-qPCR experiments, participated in writ- ing the manuscript III: Grew the D. glomerata plants, performed all RNA isolations, conducted and evaluated the RT-qPCR experiments, wrote the manuscript IV: Grew the plants and extracted the metabolites for D. glomer- ata, participated in the evaluation of the data and the writing of the manuscript Also partially written by the author but not included in this thesis: V. Nguyen TV, Pawlowski K (2017). Frankia and actinorhizal plants: symbiotic nitrogen fixation. In: Mehnaz S (ed). Mi- crobes for sustainability - Rhizotrophs, Springer, New York. In press. VI. Normand P, Nguyen TV, Battenberg K, Berry AM, Vanden Heuvel B, Fernandez MP, Pawlowski K. Proposal of Candi- datus Frankia californiensis, the uncultured nitrogen-fixing symbiont associated with a phylogenetically broad group of hosts endemic to California. Int J Syst Evol Microbiol, in preparation. Contents 1. Introduction ......................................................................................... 13 1.1 Nitrogen-fixing symbiosis in root nodules ......................................... 13 1.2 Actinorhizal symbiosis ....................................................................... 14 1.3 Actinorhizal nodules .......................................................................... 19 1.3.1 Nodule induction ........................................................................ 19 1.3.2 Nodule structure ......................................................................... 21 1.3.3 Nodule metabolism ..................................................................... 23 1.4 Signal exchange between microsymbiont and host plant ................... 24 1.4.1 Signal exchange in the legume-rhizobia symbiosis .................... 24 1.4.2 Signal exchange in actinorhizal symbiosis ................................. 26 1.5 Evolution of actinorhizal symbiosis ................................................... 27 2. Aim of this thesis ................................................................................. 29 3. Comments on methodology ................................................................. 30 3.1 Frankia gDNA isolation for genome sequencing ........................... 30 3.2 Candidate gene expression profiling of bacteria in nodules of Datisca glomerata and Ceanothus thyrsiflorus ..................................................... 30 3.3 Amino acid profiling of roots and nodules from Datisca glomerata . 32 4. Results and Discussion ........................................................................ 33 4.1 Genome sequencing of Frankia cluster II strains............................... 33 4.1.1 Frankia cluster II inocula represent strain assemblages ............. 33 4.1.2 Eurasian cluster II Frankia (meta-)genomes contain the canonical nod genes nodABC and North American strains also contain the sulfotransferase gene nodH.................................................................. 37 4.1.3 Cluster II genome (in-)stability: transposase frequencies in the different strains .................................................................................... 38 4.1.4 Evolution of the symbiosis between actinorhizal plants and Frankia cluster II strains ...................................................................... 39 4.2 Candidate gene expression profiling of bacterial metabolism in root nodules of D. glomerata (Cucurbitales) and C. thyrsiflorus (Rosales) .... 40 4.2.1 Frankia nodABC genes are expressed in both types of nodules, and nodH genes are expressed in nodules of C. thyrsiflorus ...................... 41 4.2.2 The expression levels of genes encoding bacterial truncated
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