Non-diazotrophic Trichodesmium species are active in N2 fixing colonies

Trichodesmium is a globally important nitrogen-fixing cyanobacterial genus. Until recently, it was assumed that all Trichodesmium species fix nitrogen. However, non-diazotrophic candidate species were recently identified in metagenome assembled genomes (non-diazotrophic Trichodesmium or NDT hereafter). This raises questions about the ecological significance of non-nitrogen fixing Trichodesmium species and the overall niche and biogeochemical role of the genus. We re-analyzed existing metagenomes and metaproteomics data of hand-picked Trichodesmium colonies traversing the Atlantic Ocean, including both bulk populations and individual colonies, this time including NDT metagenome assembled genomes. We found proteomic evidence that non-diazotrophic Trichodesmium species coexist within nitrogen fixing colonies and that multiple different NDT species were present in most samples. Proteomic signatures indicate that the non-diazotrophs were growing, photosynthesizing, using organic nitrogen, and metabolically active. Though they were in low abundance in the bulk metaproteomes, evidence of non-diazotrophic Trichodesmium was found in a significant fraction of the individual colonies. We developed an ecological model that indicates that non-diazotrophic Trichodesmium filaments can reach stable, low abundance populations by growing while attached to diazotrophic colonies. The proteomic and model evidence suggests that non-diazotrophic Trichodesmium cells might survive by coexisting and interacting with diazotrophic colonies in order to acquire fixed nitrogen.