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The actinorhizal symbiosis of the earliest divergent Frankia cluster
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

In recent years, the need to reduce reliance on synthetic nitrogen fertilizer has led to extensive research on biological nitrogen fixation, especially on root nodule symbioses. My study focuses on actinorhizal symbioses, the symbiotic interactions between members of nitrogen-fixing soil actinobacteria from the genus Frankia and a diverse group of plants from eight families, collectively called actinorhizal plants. Frankia cluster II has been shown to be sister to all other clusters. Thus, one of my aims was to gain insight into this cluster to get more information about the evolution of actinorhizal symbioses. The first sequenced genome of a member from this cluster Candidatus Frankia datiscae Dg1 originated from Pakistan. This strain contains the canonical nod genes nodABC responsible for the synthesis of lipochitooligosaccharide Nod factors. In this thesis, we obtained three Frankia inocula from North America (USA), one from Europe (France), one from Asia (Japan) and one from Oceania (Papua New Guinea). Thirteen metagenomes were sequenced based on gDNA isolated from root nodules of Datisca glomerata (Datiscaceae), Ceanothus thyrsiflorus (Rhamnaceae), Coriaria myrtifolia and Coriaria arborea (Coriariaceae). This study shows that members of Frankia cluster II come in teams, helping to explain the ability of cluster II to nodulate a wide host range, four families from two orders. The inoculum from Papua New Guinea, the only sequenced strain from the Southern Hemisphere so far, contains a new Frankia species, which was proposed as Candidatus Frankia meridionalis. All cluster II strains in this study contain the canonical nod genes nodABC, with the exception of the strain from Papua New Guinea which contains only nodB’C. All North American metagenomes also contain the sulfotransferase gene nodH. This gene shows host plant-specific expression in that it was expressed in nodules of C. thyrsiflorus but not in D. glomerata. Phylogenetic analysis and transposase frequencies of the new genomes strongly support the hypothesis that the extension of the cluster II host range from Coriaria to Datisca occurred in Eurasia and that cluster II strains came to North America via the Bering Strait. To acquire more information of the influence of the host plant on the behavior of the microsymbionts, the bacterial metabolism in nodules of D. glomerata (Cucurbitales) and C. thyrsiflorus (Rosales) were compared at the level of transcription. The system to protect nitrogenase from oxygen in Ceanothus nodules seems to be more efficient than in Datisca nodules, whereas the bacterial nitrogen metabolism is likely to be similar in both host plants. The amino acid profile of D. glomerata nodules shows that the nitrogenous solutes are dominated by glutamate and arginine, supporting the suggestion that Frankia in D. glomerata nodules exports an assimilated form of nitrogen, most likely arginine. Thus, our data show that cluster II Frankia strains differ from all other Frankia clusters with regard to the presence of the canonical nod genes and their nitrogen metabolism in symbiosis. 

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University , 2017. , p. 63
National Category
Other Biological Topics
Research subject
Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-139969ISBN: 978-91-7649-716-6 (print)ISBN: 978-91-7649-717-3 (electronic)OAI: oai:DiVA.org:su-139969DiVA, id: diva2:1076320
Public defence
2017-04-06, Vivi Täckholmssalen (Q211), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 13:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 2: Manuscript. Paper 3: Manuscript.

Available from: 2017-03-14 Created: 2017-02-22 Last updated: 2017-03-29Bibliographically approved
List of papers
1. An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH
Open this publication in new window or tab >>An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH
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2016 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 17, article id 796Article in journal (Refereed) Published
Abstract [en]

Background: The ability to establish root nodule symbioses is restricted to four different plant orders. Soil actinobacteria of the genus Frankia can establish a symbiotic relationship with a diverse group of plants within eight different families from three different orders, the Cucurbitales, Fagales and Rosales. Phylogenetically, Frankia strains can be divided into four clusters, three of which (I, II, III) contain symbiotic strains. Members of Cluster II nodulate the broadest range of host plants with species from four families from two different orders, growing on six continents. Two Cluster II genomes were sequenced thus far, both from Asia.

Results: In this paper we present the first Frankia cluster II genome from North America (California), Dg2, which represents a metagenome of two major and one minor strains. A phylogenetic analysis of the core genomes of 16 Frankia strains shows that Cluster II the ancestral group in the genus, also ancestral to the non-symbiotic Cluster IV. Dg2 contains the canonical nod genes nodABC for the production of lipochitooligosaccharide Nod factors, but also two copies of the sulfotransferase gene nodH. In rhizobial systems, sulfation of Nod factors affects their host specificity and their stability.

Conclusions: A comparison with the nod gene region of the previously sequenced Dg1 genome from a Cluster II strain from Pakistan shows that the common ancestor of both strains should have contained nodABC and nodH. Phylogenetically, Dg2 NodH proteins are sister to rhizobial NodH proteins. A glnA-based phylogenetic analysis of all Cluster II strains sampled thus far supports the hypothesis that Cluster II Frankia strains came to North America with Datisca glomerata following the Madrean-Tethyan pattern.

Keywords
Frankia, Uncultured, Datisca glomerata, nodABC, nodH, mce
National Category
Environmental Biotechnology Biological Sciences
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-136065 (URN)10.1186/s12864-016-3140-1 (DOI)000385510400004 ()27729005 (PubMedID)
Available from: 2017-01-03 Created: 2016-11-29 Last updated: 2017-11-29Bibliographically approved
2. Metagenomes from the earliest divergent Frankia cluster: They come in teams
Open this publication in new window or tab >>Metagenomes from the earliest divergent Frankia cluster: They come in teams
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(English)Manuscript (preprint) (Other academic)
National Category
Other Biological Topics
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-139963 (URN)
Available from: 2017-02-22 Created: 2017-02-22 Last updated: 2017-02-22Bibliographically approved
3. Cucurbitales vs. Rosales: Analysis of bacterial metabolism based on candidate gene expression profiling in root nodules of Datisca glomerata and Ceanothus thyrsiflorus
Open this publication in new window or tab >>Cucurbitales vs. Rosales: Analysis of bacterial metabolism based on candidate gene expression profiling in root nodules of Datisca glomerata and Ceanothus thyrsiflorus
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(English)Manuscript (preprint) (Other academic)
National Category
Other Biological Topics
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-139966 (URN)
Available from: 2017-02-22 Created: 2017-02-22 Last updated: 2017-02-22Bibliographically approved
4. The N-metabolites of roots and actinorhizal nodules from Alnus glutinosa and Datisca glomerata: can D-glomerata change N-transport forms when nodulated?
Open this publication in new window or tab >>The N-metabolites of roots and actinorhizal nodules from Alnus glutinosa and Datisca glomerata: can D-glomerata change N-transport forms when nodulated?
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2016 (English)In: Symbiosis, ISSN 0334-5114, E-ISSN 1878-7665, Vol. 70, no 1, p. 149-157Article in journal (Refereed) Published
Abstract [en]

To gain more insight in nitrogen metabolism in actinorhizal nodules, a comparison between the N metabolite profiles in roots vs. nodules was initiated for one host plant from the best-examined order of actinorhizal plants, Fagales, A. glutinosa (Betulaceae), a temperate tree, and one host plant from the Cucurbitales order, Datisca glomerata (Datiscaceae). For both symbioses, the symbiotic transcriptomes have been published and can be used to assess the expression of genes representing specific metabolic pathways in nodules. The amino acid profiles of roots in this study suggest that A. glutinosa transported aspartate, glutamate and citrulline in the xylem, a combination of nitrogenous solutes not published previously for this species. The amino acid profiles of D. glomerata roots depended on whether the plants were nodulated or grown on nitrate; roots of nodulated plants contained increased amounts of arginine. Although bacterial transcriptome data showed no symbiotic auxotrophy for branched chain amino acids (leucine, isoleucine, valine) in either symbiosis, D. glomerata nodules contained comparatively high levels of these amino acids. This might represent a response to osmotic stress.

Keywords
Actinorhiza, Frankia, Nitrogen-fixation, Arginine, Gamma-aminobutyrate (GABA), Citrulline
National Category
Biological Sciences
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-134209 (URN)10.1007/s13199-016-0407-x (DOI)000381764800017 ()
Available from: 2016-10-13 Created: 2016-10-03 Last updated: 2017-11-29Bibliographically approved

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