Reduced nitrogenase efficiency dominates response of the globally important nitrogen fixer Trichodesmium to ocean acidification

Ya-Wei Luo,Haizheng Hong,Sven A Kranz,Futing Zhang,Brian M Hopkinson,Dalin Shi,Rong Shen

doi:10.1038/s41467-019-09554-7

Ya-Wei Luo, Haizheng Hong + Show 5 more

Open Access

https://doi.org/10.1038/s41467-019-09554-7

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Abstract

The response of the prominent marine dinitrogen (N2)-fixing cyanobacteria Trichodesmium to ocean acidification (OA) is critical to understanding future oceanic biogeochemical cycles. Recent studies have reported conflicting findings on the effect of OA on growth and N2 fixation of Trichodesmium. Here, we quantitatively analyzed experimental data on how Trichodesmium reallocated intracellular iron and energy among key cellular processes in response to OA, and integrated the findings to construct an optimality-based cellular model. The model results indicate that Trichodesmium growth rate decreases under OA primarily due to reduced nitrogenase efficiency. The downregulation of the carbon dioxide (CO2)-concentrating mechanism under OA has little impact on Trichodesmium, and the energy demand of anti-stress responses to OA has a moderate negative effect. We predict that if anthropogenic CO2 emissions continue to rise, OA could reduce global N2 fixation potential of Trichodesmium by 27% in this century, with the largest decrease in iron-limiting regions.

Highlights

The response of the prominent marine dinitrogen (N2)-fixing cyanobacteria Trichodesmium to ocean acidification (OA) is critical to understanding future oceanic biogeochemical cycles
It should be noted that the model is conventionally named as a cellular model, it simulates the daily-average response of a filamentous trichome consisting of multiple cells, despite the fact that N2 fixation and photosynthesis in Trichodesmium have been shown to be segregated spatially in different cells along a trichome and/ or temporally at different time over a diel cycle[21,22]
In the model framework (Fig. 1), the total intracellular Fe quota (Fe discussed hereafter refers to Fe quota, i.e., the cellular Fe to carbon ratioÀ, unlÁess otherwise spÀecifieÁd), QFe, consistÀs of ÁFe in nitrogenÀase ÁQNFeF, photosystems QPFeS, maintenance QMFeT and storage QSFTe, and the energy produced from the photosystems (E) is allocated to concentrating mechanisms (CCM) (ECCM), carbon (C) fixation (ECF), N2 fixation (ENF), maintenance (EMT) and anti-stress against OA (EAts) (Fig. 1)

Summary

Introduction

The response of the prominent marine dinitrogen (N2)-fixing cyanobacteria Trichodesmium to ocean acidification (OA) is critical to understanding future oceanic biogeochemical cycles. In this study, using experimentally-measured intracellular Fe in photosystems and nitrogenase together with other parameters obtained from the literature, we quantitatively analyze intracellular Fe and energy allocations in Trichodesmium in response to OA and examine how they modulate its growth and N2 fixation. The results of these quantitative analyses provide parameterization schemes for an optimality-based Trichodesmium cellular model, in which growth rate is maximized by optimizing allocation of intracellular Fe and energy under varying levels of OA and intracellular Fe. By using the model to study different physiological processes, we find that the reduced nitrogenase efficiency dominates the response of Trichodesmium to OA. We project that N2 fixation potential by Trichodesmium in the global ocean may be reduced by 27% by the end of this century if anthropogenic CO2 emissions continue to rise

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