Untangling molecular survival strategies of marine nitrogen fixing communities in the nutrient limited North Atlantic Ocean

Abstract

The availability of nitrogen (N) is one of the crucial limiting factors constraining the growth and activity of phytoplankton, which in turn have major roles in global primary production and biogeochemical cycling in the oceans. Organisms capable of N2 fixation, termed diazotrophs, are essential to the external supply of bioavailable N to surface oceans, including the filamentous cyanobacteria Trichodesmium spp., which are responsible for the largest fraction of open ocean N2 fixation. The availability of iron (Fe) and phosphorus (P)constrain the activity and biogeography of diazotrophs, and are often scarce in oligotrophic subtropical gyres; while reciprocally the activity and biogeography of diazotrophs influence the biogeochemistry of these nutrients. As such, diazotrophs have evolved strategies to adapt and acclimate under low-nutrient environments while maintaining their N2 fixation activity. Therefore, the goal of this thesis was to investigate the molecular activity of microbial communities in natural environments through gene expression analysis. Specifically, the role of limiting nutrients Fe and P on diversity and abundance of diazotrophs in the North Atlantic will be investigated. Understanding the controls on the biogeography and physiology of diazotrophs in situ is therefore key to accurately model their role in biogeochemical cycles. During a research cruise across the subtropical North Atlantic Ocean (26th June to 12thAugust 2017), two natural opposing surface gradients in Fe and P were encountered. This ‘natural laboratory’ served as a sampling platform to use targeted molecular techniques, in parallel with physiological and chemical measurements, to characterise the in situ diazotroph community. While Trichodesmium spp. dominated across the transect, the overall diazotrophdiversity varied among sampling locations, resulting in diverse biogeographical niches including UCYN-A, and gamma-proteobacteria. A gene expression analysis suggested that it is the supply of nutrients that influences the composition and activity of the diazotrophic community. Given the dominance of Trichodesmium spp. in the sampling stations, and their ecological importance in marine ecosystems, the thresholds of nutrient requirements were evaluated for Trichodesmium’s physiology and resulting N2 fixation over the ‘natural laboratory’ environment. Using high-throughput metatranscriptomic (gene expression)analysis, three distinct transcriptomic responses were defined as: (1) an Fe-stress transcriptome (when dFe was low and characterised by the expression of known Fe-stress biomarkers); (2) a P-stress transcriptome (when P was low and characterised by the expression of known P-stress biomarkers); and (3) a N2 fixing transcriptome (characterised by the enhanced transcription of N2 fixation associated genes and elevated N2 fixation rates observed at the intersection of the antithetical gradients of Fe and P). The response of Trichodesmium to availability of both Fe and P provides evidence that these biogeochemically significant organisms employ integrated molecular and physiological strategies to exploit the Fe and P co-limited niche they create, and enhance its N2 fixation activity. As such, the co-limitation physiological response of Trichodesmium should be considered when integrating diazotrophs in global biogeochemical models.
Finally, Trichodesmium lives in consortia with a complex of microbial organisms that are thought to have roles in the ecosystem function of Trichodesmium holobiont (e.g. nutrient acquisition, anoxic metabolism), that need to be considered in understanding the ecological success of the host. In a second sampling cruise in the Sargasso Sea region of the North Atlantic (21st to 27th of July 2016), a novel single-colony sampling and sequencing approach
was used to characterise the Trichodesmium associated microbial community, focusing on the colony-to-colony differences. Results revealed the colonies consisted of one single species of Trichodesmium, and the associated communities were significantly distinct between colony morphologies as well as between Trichodesmium species.
Combined, these findings reveal the distribution, transcriptomic response and taxonomic differentiation of associated communities of components of the diazotroph communities in the North Atlantic. Such discoveries unveil strategies evolved to survive in Fe:P co-limited ocean gyres, which are key to understanding the biogeochemical contribution of marine diazotrophs in a global oceanic context.

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ORCID for Elena Cerdan Garcia: orcid.org/0000-0002-0409-7722

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