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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. 

Abstract Species are a fundamental unit of biodiversity. Yet, the existence of clear species boundaries among bacteria has long been a subject of debate. Here, we studied species boundaries in the context of the phylogenetic history of Nostoc, a widespread genus of photoautotrophic and nitrogen-fixing cyanobacteria that includes many lineages that form symbiotic associations with plants (e.g. cycads and bryophytes) and fungi (e.g. cyanolichens). We found that the evolution of Nostoc was characterized by eight rapid radiations, many of which were associated with major events in the evolution of plants. In addition, incomplete lineage sorting associated with these rapid radiations outweighed reticulations during Nostoc evolution. We then show that the pattern of diversification of Nostoc shapes the distribution of average nucleotide identities (ANIs) into a complex mosaic, wherein some closely related clades are clearly isolated from each other by gaps in genomic similarity, while others form a continuum where genomic species boundaries are expected. Nevertheless, recently diverged Nostoc lineages often form cohesive clades that are maintained by within-clade gene flow. Boundaries to homologous recombination between these cohesive clades persist even when the potential for gene flow is high, i.e. when closely related clades of Nostoc co-occur or are locally found in symbiotic associations with the same lichen-forming fungal species. Our results demonstrate that rapid radiations are major contributors to the complex speciation history of Nostoc. This underscores the need to consider evolutionary information beyond thresholds of genomic similarity to delimit biologically meaningful units of biodiversity for bacteria.