Discovery of nondiazotrophic Trichodesmium species abundant and widespread in the open ocean

Abstract

Filamentous and colony-forming cells within the cyanobacterial genus Trichodesmium might account for nearly half of nitrogen fixation in the sunlit ocean, a critical mechanism that sustains plankton's primary productivity. Trichodesmium has long been portrayed as a diazotrophic genus. By means of genome-resolved metagenomics, here we reveal that nondiazotrophic Trichodesmium species not only exist but also are abundant and widespread in the open ocean, benefiting from a previously overlooked functional lifestyle to expand the biogeography of this prominent marine genus. Near-complete environmental genomes for those closely related candidate species reproducibly shared functional features including a lack of genes related to nitrogen fixation, hydrogen recycling, and hopanoid lipid production concomitant with the enrichment of nitrogen assimilation genes. Our results elucidate fieldwork observations of Trichodesmium cells fixing carbon but not nitrogen. The Black Queen hypothesis and burden of low-oxygen concentration requirements provide a rationale to explain gene loss linked to nitrogen fixation among Trichodesmium species. Disconnecting taxonomic signal for this genus from a microbial community's ability to fix nitrogen will help refine our understanding of the marine nitrogen balance. Finally, we are reminded that established links between taxonomic lineages and functional traits do not always hold true.