Transcriptional responses of Trichodesmium to natural inverse gradients of Fe and P availability

E Cerdan-Garcia,C Mahaffey,C M Moore,D Polyviou,E M S Woodward,L Wrightson,J C Robidart,M C Lohan,T S Bibby,A Baylay

doi:10.1038/s41396-021-01151-1

Abstract

The filamentous diazotrophic cyanobacterium Trichodesmium is responsible for a significant fraction of marine di-nitrogen (N2) fixation. Growth and distribution of Trichodesmium and other diazotrophs in the vast oligotrophic subtropical gyres is influenced by iron (Fe) and phosphorus (P) availability, while reciprocally influencing the biogeochemistry of these nutrients. Here we use observations across natural inverse gradients in Fe and P in the North Atlantic subtropical gyre (NASG) to demonstrate how Trichodesmium acclimates in situ to resource availability. Transcriptomic analysis identified progressive upregulation of known iron-stress biomarker genes with decreasing Fe availability, and progressive upregulation of genes involved in the acquisition of diverse P sources with decreasing P availability, while genes involved in N2 fixation were upregulated at the intersection under moderate Fe and P availability. Enhanced N2 fixation within the Fe and P co-stressed transition region was also associated with a distinct, consistent metabolic profile, including the expression of alternative photosynthetic pathways that potentially facilitate ATP generation required for N2 fixation with reduced net oxygen production. The observed response of Trichodesmium to availability of both Fe and P supports suggestions that these biogeochemically significant organisms employ unique molecular, and thus physiological responses as adaptations to specifically exploit the Fe and P co-limited niche they construct.

Highlights

In low nitrogen (N) marine environments, diazotrophs, organisms capable of fixing atmospheric di-N into biologically available ammonia (NH3) [1, 2] contribute to a significant fraction of new N input in the oceans
Opposing the dFe gradient, an increasing eastward trend was observed for dissolved organic P (DOP) and total dissolved surface P (TDP), while dissolved inorganic phosphate (DIP) was slightly elevated at the easternmost stations (6 and 7) (Fig. 1c, d)
External forcing, including upwelling of waters with excess P The natural inverse gradients in Fe and P availability captured in and dust-borne Fe inputs, provides the drivers for this study enabled a holistic view of the in situ molecular response biogeochemical gradients of the type sampled [13]

Summary

Introduction

In low nitrogen (N) marine environments, diazotrophs, organisms capable of fixing atmospheric di-N into biologically available ammonia (NH3) [1, 2] contribute to a significant fraction of new N input in the oceans. Trichodesmium’s distribution and N2 fixation activity is restricted by the availability of nutrients such as iron (Fe) and phosphorus (P) [7,8,9] This is distinctly evident across latitudinal gradients in the Atlantic, where low dust Fe flux south of the inter-tropical convergence zone (ITCZ) in the South Atlantic subtropical gyre limits the activity of Trichodesmium and other N2 fixers, resulting in relatively high residual P concentrations [9, 10]. Increased dust flux north of the ITCZ provides sufficient Fe for Trichodesmium to flourish and drawdown surface P to nanomolar concentrations [7, 11,12,13] Such boundaries between high-Fe/low-P and low-Fe/high-P regions represent constructed niches which appear widespread in low latitude oligotrophic oceans [9, 11, 14]. Evidence for Fe and P co-limitation [15] and observed physiological responses of Trichodesmium under these conditions have led to suggestions that the organism may be adapted to nutrient costress [16,17,18,19]

Methods

Results

Conclusion