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Abstract Nostoc cyanobacteria are among the few organisms capable of fixing both carbon and nitrogen. These metabolic features are essential for the cyanolichen symbiosis, where Nostoc supplies both carbon (as glucose) and nitrogen (as ammonium) to a cyanolichen-forming fungal partner. This nutrient flow was established by seminal biochemical studies published in the 20th century. Since then, cyanolichen metabolism has received little attention, and the molecular mechanisms that underlie the physiology of lichenized Nostoc remain mostly unknown. Here, we aimed to elucidate the genomic and transcriptional changes that enable Nostoc’s metabolic role in cyanolichens. We used comparative genomics across 243 genomes of Nostoc s. lat. coupled with metatranscriptomic experiments using Peltigera cyanolichens. We found that genes for photoautotrophic carbon fixation are upregulated in lichenized Nostoc. This likely results in a higher rate of carbon fixation that allows Nostoc to provide carbon to the fungal partner while meeting its own metabolic needs. We also found that the transfer of ammonium from Nostoc to the lichen-forming fungus is facilitated by two molecular mechanisms: (i) transcriptional downregulation of glutamine synthetase, the key enzyme responsible for ammonium assimilation in Nostoc; and (ii) frequent losses of a putative high-affinity ammonium permease, which likely reduces Nostoc’s capacity to recapture leaked ammonium. Finally, we found that the development of motile hormogonia is downregulated in lichenized Nostoc, which resembles the repression of motility in Nostoc symbionts after they colonize symbiotic cavities of their plant hosts. Our results pave the way for a revival of cyanolichen ecophysiology in the omics era.
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Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism
Abstract Interactions between Sphagnum (peat moss) and cyanobacteria play critical roles in terrestrial carbon and nitrogen cycling processes. Knowledge of the metabolites exchanged, the physiological processes involved, and the environmental conditions allowing the formation of symbiosis is important for a better understanding of the mechanisms underlying these interactions. In this study, we used a cross-feeding approach with spatially resolved metabolite profiling and metatranscriptomics to characterize the symbiosis between Sphagnum and Nostoc cyanobacteria. A pH gradient study revealed that the Sphagnum–Nostoc symbiosis was driven by pH, with mutualism occurring only at low pH. Metabolic cross-feeding studies along with spatially resolved matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI) identified trehalose as the main carbohydrate source released by Sphagnum, which were depleted by Nostoc along with sulfur-containing choline-O-sulfate, taurine and sulfoacetate. In exchange, Nostoc increased exudation of purines and amino acids. Metatranscriptome analysis indicated that Sphagnum host defense was downregulated when in direct contact with the Nostoc symbiont, but not as a result of chemical contact alone. The observations in this study elucidated environmental, metabolic, and physiological underpinnings of the widespread plant–cyanobacterial symbioses with important implications for predicting carbon and nitrogen cycling in peatland ecosystems as well as the basis of general host-microbe interactions.
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- Award ID(s):
- 1737899
- PAR ID:
- 10364324
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 16
- Issue:
- 4
- ISSN:
- 1751-7362
- Format(s):
- Medium: X Size: p. 1074-1085
- Size(s):
- p. 1074-1085
- Sponsoring Org:
- National Science Foundation
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