Cymbiomics: multipartite interactions and a large-scale approach to pinpointing symbiotic competence of cyanobacteria

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The symbiotic interaction between cyanobacteria and eukaryotic hosts had a profound impact on the evolution of life on this planet. It was a cyanobacterial symbiont that eventually was turned into the chloroplasts for carbon-fixation. Yet, there is another prominent type of cyanobacteria in symbiosis (cyanobionts). Here, the interaction revolves around the ability of cyanobionts to perform nitrogen-fixation. In several cases, these cyanobionts are tightly integrated into the host body but have not (yet) been domesticated into an organelle. Such extant interactions are best-described in land plants (Embryophyta), but also the fungus Geosiphon—for which one of the few known natural populations thrives close to Göttingen. The manifold occurrence of symbiotic cyanobacteria, many of which are still capable of living together and apart from their host, warrants the question what made them eligible for a symbiosis in the first place. In all cyanobacterial symbioses, multipartite interactions between the host, the cyanobiont, and an associated microbial community occur. We therefore hypothesize that the cyanobacteria capable to be cyanobionts must have the ability to not only communicate with their hosts but also to function in—and perhaps even shape—a multi-organism biofilm. Here we will explore two questions: i) What manifests the symbiotic competence of these cyanobacterial lineages? and ii) Is the competence of the cyanobacterial partner determined by the capacity to recruit the functionally correct microbiome? We will carry out a three-pronged approach. First, we will leverage the SAG collection in Göttingen and sequence cyanobacterial strains isolated from symbiotic and non-symbiotic conditions; contextualized with publicly available genomes, these data will be combined with genome-wide association studies and comparative genomics to pinpoint genetic factors that is common to all cyanobacteria that are clearly capable of symbiosis. Second, we will sample naturally occurring cyanobionts and their microbiome from multiple individuals of Geosiphon and the cyanobiont-bearing plants Gunnera, Azolla and Anthoceros. Third, we will use the Anthoceros lab system to phenotype the cyanobacterial strains sequenced for symbiotic competency and determine the microbiome of the Anthoceros–cyanobacteria symbiosis after cyanobacterial inoculation. Altogether, our data will determine factors linked to the symbiotic capabilities of the cyanobacteria—both in natural and cultivated cyanobionts. Possible follow-up studies will include generation of cyanobacteria that are knocked out in the identified candidate genes.