Dissolved organic matter uptake by Trichodesmium in the Southwest Pacific

Mar Benavides,Solange Duhamel,Patrick Raimbault,Sophie Bonnet,Hugo Berthelot

doi:10.1038/srep41315

Abstract

The globally distributed diazotroph Trichodesmium contributes importantly to nitrogen inputs in the oligotrophic oceans. Sites of dissolved organic matter (DOM) accumulation could promote the mixotrophic nutrition of Trichodesmium when inorganic nutrients are scarce. Nano-scale secondary ion mass spectrometry (nanoSIMS) analyses of individual trichomes sampled in the South Pacific Ocean, showed significant 13C-enrichments after incubation with either 13C-labeled carbohydrates or amino acids. These results suggest that DOM could be directly taken up by Trichodesmium or primarily consumed by heterotrophic epibiont bacteria that ultimately transfer reduced DOM compounds to their host trichomes. Although the addition of carbohydrates or amino acids did not significantly affect bulk N2 fixation rates, N2 fixation was enhanced by amino acids in individual colonies of Trichodesmium. We discuss the ecological advantages of DOM use by Trichodesmium as an alternative to autotrophic nutrition in oligotrophic open ocean waters.

Highlights

Nitrogen is recognized as the proximate limiting nutrient for primary production in the oceans[1]
We present evidence of carbohydrate and amino acid uptake by natural Trichodesmium colonies in conditions usually regarded as optimal for their autotrophic growth (Table S1)
The addition of either carbohydrates or amino acids increased per-trichome N2 fixation rates compared to the control at both LDA and LDB, but only amino acid additions induced statistically significant per-trichome N2 fixation enhancements (Fig. 1e,f)

Summary

Introduction

Nitrogen is recognized as the proximate limiting nutrient for primary production in the oceans[1]. While global nitrogen budget estimations determine that denitrification exceeds N2 fixation considerably[3], recent improvements in the 15N2 isotope tracer method used to measure biological N2 fixation have evidenced that formerly published rates could be underestimated by a factor of ~2 to 64–8, and could be high enough to balance denitrification on a global basis. In chronically stratified open ocean regions such as the vast subtropical gyres, primary production depends largely on external fixed nitrogen inputs provided by N2 fixation performed by prokaryotes termed ‘diazotrophs’. Diazotrophic cyanobacteria are photosynthetic prokaryotes (with the exception of the photoheterotrophic Candidatus Atelocyanobacterium thalassa which cannot photosynthesize)[17] that thrive in oligotrophic tropical and subtropical waters of the oceans where they provide an important source of fixed nitrogen for other phytoplankton[13]. We quantify the uptake of carbohydrates and amino acids and their effect on N2 fixation by natural Trichodesmium colonies using nano-scale secondary ion mass spectrometry (nanoSIMS)

Methods

Results

Conclusion