Environmental genomics points to non-diazotrophic 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 planktons primary productivity at large-scale. Here, we report the genome-resolved metagenomic characterization of two newly identified marine species we tentatively named Ca. Trichodesmium miru and Ca. Trichodesmium nobis. Near-complete environmental genomes for those closely related candidate species revealed unexpected functional features including a lack of the entire nitrogen fixation gene apparatus and hydrogen recycling genes concomitant with the enrichment of nitrogen assimilation genes and apparent acquisition of the nirb gene from a non-cyanobacterial lineage. These comparative genomic insights were cross-validated by complementary metagenomic investigations. Our results contrast with the current paradigm that Trichodesmium species are necessarily capable of nitrogen fixation. The black queen hypothesis could explain gene loss linked to nitrogen fixation among Trichodesmium species, possibly triggered by gene acquisitions from the colony epibionts. Critically, the candidate species are not only widespread in the 3-2000 m planktonic size fraction of the surface of the oceans and seas, but might also substantially expand the ecological niche of Trichodesmium, stressing the need to disconnect taxonomic signal for this genus from a microbial communitys ability to fix nitrogen. Especially, differentiating diazotrophic from non-diazotrophic populations when counting Trichodesmium filaments and colonies might help refine our understanding of the marine nitrogen balance. While culture representatives are needed to move beyond metagenomic insights, we are reminded that established links between taxonomic lineages and functional traits might not always hold true.