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Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis
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.
Number of Authors: 17
2017 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370Article in journal (Refereed) Epub ahead of print
Abstract [en]

Dinitrogen (N2)-fixation by cyanobacteria in symbiosis with feathermosses is the primary pathway of biological N input into boreal forests. Despite its significance, little is known about the cyanobacterial gene repertoire and regulatory rewiring needed for the establishment and maintenance of the symbiosis. To determine gene acquisitions and regulatory changes allowing cyanobacteria to form and maintain this symbiosis, we compared genomically closely related symbiotic-competent and incompetent Nostoc strains, using a proteogenomics approach and an experimental setup allowing for controlled chemical and physical contact between partners. Thirty-two gene families were found only in the genomes of symbiotic strains, including some never before associated with cyanobacterial symbiosis. We identified conserved orthologs that were differentially expressed in symbiotic strains, including protein families involved in chemotaxis and motility, NO regulation, sulfate/phosphate transport, and glycosyl-modifying and oxidative stress-mediating exoenzymes. The physical moss-cyanobacteria epiphytic symbiosis is distinct from other cyanobacteria-plant symbioses, with Nostoc retaining motility, and lacking modulation of N2-fixation, photosynthesis, GS-GOGAT cycle, and heterocyst formation. The results expand our knowledgebase of plant-cyanobacterial symbioses, provide a model of information and material exchange in this ecologically significant symbiosis, and suggest new currencies, namely nitric oxide and aliphatic sulfonates, may be involved in establishing and maintaining the cyanobacteria-feathermoss symbiosis. 

Place, publisher, year, edition, pages
2017.
Keyword [en]
Boreal forest, Comparative genomic, Transcriptomic, Proteomic, Exoproteomic
National Category
Other Biological Topics
Research subject
Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-146126DOI: 10.1038/ismej.2017.134OAI: oai:DiVA.org:su-146126DiVA: diva2:1135450
Available from: 2017-08-23 Created: 2017-08-23 Last updated: 2017-08-25
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)
Opponent
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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