Warming Iron-Limited Oceans Enhance Nitrogen Fixation and Drive Biogeographic Specialization of the Globally Important Cyanobacterium Crocosphaera

Nina Yang,Fei-Xue Fu,Carlin A Merkel,Hai-Bo Jiang,David A Hutchins,Michelle A Demers,Naomi M Levine,Yu-An Lin,Nicholas J Hawco,Eric A Webb,Ping-Ping Qu

doi:10.3389/fmars.2021.628363

Abstract

Primary productivity in the nutrient-poor subtropical ocean gyres depends on new nitrogen inputs from nitrogen fixers that convert inert dinitrogen gas into bioavailable forms. Temperature and iron (Fe) availability constrain marine nitrogen fixation, and both are changing due to anthropogenic ocean warming. We examined the physiological responses of the globally important marine nitrogen fixer, Crocosphaera watsonii across its full thermal range as a function of iron availability. At the lower end of its thermal range, from 22 to 27°C, Crocosphaera growth, nitrogen fixation, and Nitrogen-specific Iron Use Efficiencies (N-IUEs, mol N fixed hour–1 mol Fe–1) increased with temperature. At an optimal growth temperature of 27°C, N-IUEs were 66% higher under iron-limited conditions than iron-replete conditions, indicating that low-iron availability increases metabolic efficiency. However, Crocosphaera growth and function decrease from 27 to 32°C, temperatures that are predicted for an increasing fraction of tropical oceans in the future. Altogether, this suggests that Crocosphaera are well adapted to iron-limited, warm waters, within prescribed limits. A model incorporating these results under the IPCC RCP 8.5 warming scenario predicts that Crocosphaera N-IUEs could increase by a net 47% by 2100, particularly in higher-latitude waters. These results contrast with published responses of another dominant nitrogen fixer (Trichodesmium), with predicted N-IUEs that increase most in low-latitude, tropical waters. These models project that differing responses of Crocosphaera and Trichodesmium N-IUEs to future warming of iron-limited oceans could enhance their current contributions to global marine nitrogen fixation with rates increasing by ∼91 and ∼22%, respectively, thereby shifting their relative importance to marine new production and also intensifying their regional divergence. Thus, interactive temperature and iron effects may profoundly transform existing paradigms of nitrogen biogeochemistry and primary productivity in open ocean regimes.

Highlights

Marine phytoplankton are important facilitators of biogeochemical cycling in the ocean, and contribute nearly half of the of the Earth’s net primary production (Behrenfeld et al, 2006)
The thermal optimum for Crocosphaera growth under both forms. Temperature and iron (Fe)-replete and Fe-limited treatments was at 27◦C, with the thermal minimum and maximum at 20 and 36◦C, respectively
For Crocosphaera, N2-fixation rates and cell-specific growth rates across all growth temperature and Fe experimental conditions were measured at four time points during steady-state exponential growth to establish the linear relationship using a two-way least squares fit between the two rates under varying temperature and Fe availability (Supplementary Figure 4)

Summary

Introduction

Marine phytoplankton are important facilitators of biogeochemical cycling in the ocean, and contribute nearly half of the of the Earth’s net primary production (Behrenfeld et al, 2006). In the subtropical and tropical ocean gyres where large expanses of nutrient-poor surface waters persist, low concentrations of bioavailable nitrogen generally limit phytoplankton growth (Moore et al, 2013) In these regions, nitrogen-fixing cyanobacteria (N2-fixers) or diazotrophs provide an essential ecosystem service by converting or “fixing” inert dinitrogen gas (N2) into bioavailable ammonia (NH3) that fuels primary productivity (Zehr et al, 2001; Sohm et al, 2011). While many microbial groups contribute to biological nitrogen fixation (N2-fixation), cyanobacteria of the filamentous Trichodesmium and unicellular Crocosphaera genera are estimated to account for nearly half of the global total (Zehr and Capone, 2020) These two diazotrophic groups are key components of the marine nitrogen cycle and so, will help to determine how the availability of this limiting nutrient responds to ongoing changes in the ocean environment (Hutchins and Fu, 2017)

Methods

Results

Conclusion