Density-dependent oxylipin production in natural diatom communities: possible implications for plankton dynamics

Ennio Russo,Greta Busseni,Adrianna Ianora,Diana Sarno,Ylenia Carotenuto,Angelo Fontana,Giuliana D’Ippolito,Eric Von Elert,Domenico D’Alelio

doi:10.1038/s41396-019-0518-5

Abstract

Oxylipins are important signal transduction lipoxygenase-derived products of fatty acids that regulate a variety of physiological and pathological processes in plants and animals. In marine diatoms, these molecules can be highly bioactive, impacting zooplankton grazers, bacteria and other phytoplankton. However, the ultimate cause for oxylipin production in diatoms is still poorly understood, from an evolutionary perspective. Here we analysed production of particulate linear oxygenated fatty acids (LOFAs, previously named non-volatile oxylipins) from natural phytoplankton collected weekly for 1 year. We demonstrate for the first time that diatoms are the main LOFA producers in natural phytoplankton assemblages. Interestingly, LOFA-per-cell production decreased with increasing diatom density and was not due to major changes in diatom community composition. An inverse relation was confirmed at a global scale by analysing diatom lipoxygenase unigenes and metagenomes from Tara Oceans datasets. A network analysis suggested that different LOFAs could contribute to modulate co-variations of different diatom taxa. Overall, we offer new insights in diatom chemical ecology, possibly explaining the evolution of oxylipin synthesis in diatoms.

Highlights

In marine systems, diatoms are one of the most important phytoplankton groups actively synthesizing oxylipins from membrane-bound polyunsaturated fatty acids upon activation by lipoxygenases (LOX) [1,2,3,4,5,6,7,8,9]
The role of oxylipins in diatom chemical ecology is still debated and, in this perspective, field data can pave the way for hypothesis-driven laboratory setups
Qualitative and quantitative characterization of particulate Linear oxygenated fatty acid (LOFA) from our data confirm that HTrA and EPA represent relevant oxylipin precursors in diatoms [1, 3, 5, 7, 36], and suggest that the relative contribution of DHA at sea may be higher than previously thought [14]

Summary

Introduction

Diatoms are one of the most important phytoplankton groups actively synthesizing oxylipins from membrane-bound polyunsaturated fatty acids upon activation by lipoxygenases (LOX) [1,2,3,4,5,6,7,8,9]. Laboratory evidence suggests that oxylipins can deter grazing [20,21,22], affect the growth of diatom-associated bacteria [23,24,25] and inhibit the growth of several phytoplankton taxa in a dose-dependent manner [26, 27]. These results suggest a role of oxylipins as defensive or allelopathic compounds to exclude predators or competitors as well as a role as info-chemicals synchronizing cell death of phytoplankton blooms [28,29,30]. Only few field surveys have so far investigated oxylipin variations in time and space [18, 31,32,33,34,35,36,37]

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Results

Conclusion