Nitrogen starvation induces distinct photosynthetic responses and recovery dynamics in diatoms and prasinophytes.

Justin D Liefer,Zoe V Finkel,Douglas A Campbell,Andrew J Irwin,Aneri Garg,Adrianna Ianora

doi:10.1371/journal.pone.0195705

Abstract

Nitrogen stress is an important control on the growth of phytoplankton and varying responses to this common condition among taxa may affect their relative success within phytoplankton communities. We analyzed photosynthetic responses to nitrogen (N) stress in two classes of phytoplankton that often dominate their respective size ranges, diatoms and prasinophytes, selecting species of distinct niches within each class. Changes in photosynthetic structures appeared similar within each class during N stress, but photophysiological and growth responses were more species- or niche-specific. In the coastal diatom Thalassiosira pseudonana and the oceanic diatom T. weissflogii, N starvation induced large declines in photosynthetic pigments and Photosystem II (PSII) quantity and activity as well as increases in the effective absorption cross-section of PSII photochemistry (σʹPSII). These diatoms also increased photoprotection through energy-dependent non-photochemical quenching (NPQ) during N starvation. Resupply of N in diatoms caused rapid recovery of growth and relaxation of NPQ, while recovery of PSII photochemistry was slower. In contrast, the prasinophytes Micromonas sp., an Arctic Ocean species, and Ostreococcus tauri, a temperate coastal eutrophile, showed little change in photosynthetic pigments and structures and a decline or no change, respectively, in σʹPSII with N starvation. Growth and PSII function recovered quickly in Micromonas sp. after resupply of N while O. tauri failed to recover N-replete levels of electron transfer from PSII and growth, possibly due to their distinct photoprotective strategies. O. tauri induced energy-dependent NPQ for photoprotection that may suit its variable and nutrient-rich habitat. Micromonas sp. relies upon both energy-dependent NPQ and a sustained, energy-independent NPQ mechanism. A strategy in Micromonas sp. that permits photoprotection with little change in photosynthetic structures is consistent with its Arctic niche, where low temperatures and thus low biosynthetic rates create higher opportunity costs to rebuild photosynthetic structures.

Highlights

Among photosynthetic organisms phytoplankton are especially subject to rapid variation in light and nutrient conditions
We demonstrate that the photosynthetic response to dynamic nutrient conditions varies in complex ways with respect to taxa and niche and may be a key feature determining the success of a phytoplankton species
Both a coastal and open ocean diatom displayed large declines in photosynthetic pigments while both a coastal and Arctic open ocean prasinophyte showed small changes in photosynthetic pigments. This similarity in pigment dynamics within diatoms and prasinophytes indicates the importance of cell size and phylogeny in determining changes in the material structure of photosynthesis during N-stress

Summary

Introduction

Among photosynthetic organisms phytoplankton are especially subject to rapid variation in light and nutrient conditions. Sustained changes in light between maximum availability and darkness occur on time scales of minutes, in coastal environments, to days in the open ocean [1]. The effects of dynamic nutrient stress on photosynthetic response are much less studied than the responses to varying light intensity under nutrient replete conditions. Insufficient availability of nutrients such as nitrogen (N) can cause excess light absorption relative to the biosynthetic sinks for this energy, potentially resulting in photo-oxidative damage to a cell [4]. How photosynthetic responses to nutrient stress vary across phytoplankton taxa, cell sizes, and ecological niches is poorly understood, which presents a major challenge for effectively modelling phytoplankton dynamics [5,6,7]

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Conclusion