Taxonomic distribution of metabolic functions underpins nutrient cycling in Trichodesmium consortia

Abstract

The photosynthetic and diazotrophic cyanobacterium Trichodesmium is a key contributor to marine biogeochemical cycles in the subtropical-oligotrophic oceans. Trichodesmium forms colonies that harbor a distinct microbial community, which expands their functional potential and is predicted to influence the cycling of carbon, nitrogen, phosphorus and iron (C, N, P, and Fe). To link key traits to taxa and elucidate how community structure influences nutrient cycling, we assessed Red Sea Trichodesmium colonies using metagenomics and metaproteomics. This diverse consortium comprises bacteria that typically associate with algae and particles, such as the ubiquitous Alteromonas macleodii, but also lineages specific to Trichodesmium, such as members from the order Balneolales. These bacteria carry functional traits that would influence resource cycling in the consortium, including siderophore biosynthesis, reduced phosphorus metabolism, vitamins, denitrification, and dissimilatory-nitrate-reduction-to-ammonium (DNRA) pathways. Denitrification and DNRA appeared to be modular as bacteria collectively completed the steps for these pathways. The vast majority of associated bacteria were auxotrophic for vitamins, indicating the interdependency of consortium members. Trichodesmium in turn may rely on associated bacteria to meet its high Fe demand as several lineages can synthesize the photolabile siderophores vibrioferrin, rhizoferrin, and petrobactin, enhancing the bioavailability of particulate-Fe to the entire consortium. Our results highlight that Trichodesmium is a hotspot for C, N, P, Fe, and vitamin exchange. The functional redundancy of nutrient cycling in the consortium likely underpins its resilience within an ever-changing global environment. ImportanceColonies of the cyanobacteria Trichodesmium act as a biological hotspot for the usage and recycling of key resources such as C, N, P and Fe within an otherwise oligotrophic environment. While Trichodesmium colonies are known to interact with a unique community of algae and particle-associated microbes, our understanding of the taxa that populate these colonies and the gene functions they encode is still limited. Characterizing the taxa and adaptive strategies that influence consortium physiology and its concomitant biogeochemistry is critical in a future ocean predicted to have increasing particulate fluxes and resource-depleted regions.