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Shared and divergent genomic changes associated with the evolutionary transitions of Nostoc to a plant symbiont
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The cyanobacteria belonging to the genus Nostoc comprise free-living strains but also facultative plant-symbionts. Symbiotic strains can enter into symbiosis with a taxonomically diverse range of host plants. Little is known about genomic changes associated with evolutionary transition of Nostoc from free-living to plant symbiont. Here we compared the genomes derived from eleven symbiotic Nostoc strains isolated from different host plants and infer phylogenetic relationships between strains. Phylogenetic reconstructions of 89 Nostocales showed that symbiotic Nostoc strains with a broad host range, entering epiphytic and intracellular or extracellular endophytic interactions, form a monophyletic clade indicating a common evolutionary history. A polyphyletic origin was found for Nostoc strains which enter only extracellular symbioses, suggesting that this trait was most likely gained several times in the evolution of the Nostocales. Facultative symbiotic Nostoc strains showed enriched functions in the transport and metabolism of organic sulfur, chemotaxis and motility, as well as the uptake of phosphate, amino acid and ammonium. The genomes of the intracellular clade differ from that of other Nostoc strains by a gain/enrichment of genes encoding proteins to generate L-methionine from sulfite and pathways for the degradation of the plant metabolites vanillin and vanillate, and of the macromolecule xylan present in plant cell-walls. These compounds could function as C sources for members of the intracellular clade. Molecular clock analysis suggested that the intracellular clade emerged ~600 million years ago, which would predate the origin of land plants. This suggest that intracellular cyanobacterial symbioses may have even predated the emergence of extant terrestrial plants.

Keyword [en]
Cyanobacteria, Symbiosis, Evolution, Plant-microbe interaction
National Category
Evolutionary Biology
Research subject
Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-146124OAI: oai:DiVA.org:su-146124DiVA: diva2:1135441
Available from: 2017-08-23 Created: 2017-08-23 Last updated: 2017-08-25Bibliographically approved
In thesis
1. Cyanobacteria in symbiosis with boreal forest feathermosses: from genome evolution and gene regulation to impact on the ecosystem
Open this publication in new window or tab >>Cyanobacteria in symbiosis with boreal forest feathermosses: from genome evolution and gene regulation to impact on the ecosystem
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Among dinitrogen (N2)-fixing some cyanobacteria can establish symbiosis with a broad range of host plants from all plant lineages including bryophytes, ferns, gymnosperms, and angiosperms. In the boreal forests, the symbiosis between epiphytic cyanobacteria and feathermosses Hylocomium splendens and Pleurozium schreberi is ecologically important. The main input of biological N to the boreal forests is through these cyanobacteria, and thus, they greatly contribute to the productivity of this ecosystem. Despite the ecological relevance of the feathermoss symbiosis, our knowledge about the establishment and maintenance of cyanobacterial-plant partnerships in general is limited, and particularly our understanding of the feathermoss symbiosis is rudimentary.

The first aim of this thesis was to gain insight on the genomic rearrangements that enabled cyanobacteria to form a symbiosis with feathermosses, and their genomic diversity and similarities with other plant-symbiotic cyanobacteria partnerships. Genomic comparison of the feathermoss isolates with the genomes of free-living cyanobacteria highlighted that functions such as chemotaxis and motility, the transport and metabolism of organic sulfur, and the uptake of phosphate and amino acids were enriched in the genome of plant-symbiotic cyanobacteria.

The second aim of this PhD study was to identify cyanobacterial molecular pathways involved in forming the feathermoss symbiosis and the regulatory rewiring needed to maintain it. Global transcriptional and post-transcriptional regulation in cyanobacteria during the early phase of establishment of the feathermoss symbiosis, and after colonization of the moss were investigated. The results revealed that the putative symbiotic gene repertoire includes pathways never before associated with cyanobacteria-plant symbioses, such as nitric-oxide sensing and regulation, and the transport and metabolism of aliphatic sulfonate.

The third aim was to explore the role of the cyanobacterial community in contributing to the temporal variability of N2-fixation activity. Results from a field-study showed that temporal variation in N2-fixation rates could be explained to a high degree by changes in cyanobacterial community composition and activity. In particular, the cyanobacteria belonging to the genus Stigonema - although not dominating the community- appeared to be the main contributors to the N2-fixation activities. Based on this result, it is suggested that this genus is responsible for the main input of N in the boreal forest ecosystems.

The last aim was to understand how the relationship between cyanobacterial community composition and N2-fixation activity will be affected by climatic changes such as, increased temperature (11oC compared to 19oC) and CO2 level (500 ppm compared to 1000 ppm). Laboratory experiments highlighted that 30 weeks of combined elevation of temperature and CO2 resulted in increased N2-fixation activity and moss growth rates. The observed increases were suggested to be allocated to reduced cyanobacterial diversity and changes in community composition, resulting in the dominance of cyanobacteria adapted to the future abiotic condition.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University, 2017. 72 p.
Keyword
Cyanobacteria, Feathermosses, Symbiosis, Boreal forest, Gene flow, Proteogenomic, Transcriptomic, Community structure and composition, Dinitrogen fixation
National Category
Biological Sciences
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-146127 (URN)978-91-7649-942-9 (ISBN)978-91-7649-943-6 (ISBN)
Public defence
2017-10-06, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
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Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: Manuscript. Paper 4: Manuscript.

Available from: 2017-09-13 Created: 2017-08-23 Last updated: 2017-09-06Bibliographically approved

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