Global declines in oceanic nitrification rates as a consequence of ocean acidification

Abstract

Ocean acidification produced by dissolution of anthropogenic carbon dioxide (CO(2)) emissions in seawater has profound consequences for marine ecology and biogeochemistry. The oceans have absorbed one-third of CO(2) emissions over the past two centuries, altering ocean chemistry, reducing seawater pH, and affecting marine animals and phytoplankton in multiple ways. Microbially mediated ocean biogeochemical processes will be pivotal in determining how the earth system responds to global environmental change; however, how they may be altered by ocean acidification is largely unknown. We show here that microbial nitrification rates decreased in every instance when pH was experimentally reduced (by 0.05-0.14) at multiple locations in the Atlantic and Pacific Oceans. Nitrification is a central process in the nitrogen cycle that produces both the greenhouse gas nitrous oxide and oxidized forms of nitrogen used by phytoplankton and other microorganisms in the sea; at the Bermuda Atlantic Time Series and Hawaii Ocean Time-series sites, experimental acidification decreased ammonia oxidation rates by 38% and 36%. Ammonia oxidation rates were also strongly and inversely correlated with pH along a gradient produced in the oligotrophic Sargasso Sea (r(2) = 0.87, P < 0.05). Across all experiments, rates declined by 8-38% in low pH treatments, and the greatest absolute decrease occurred where rates were highest off the California coast. Collectively our results suggest that ocean acidification could reduce nitrification rates by 3-44% within the next few decades, affecting oceanic nitrous oxide production, reducing supplies of oxidized nitrogen in the upper layers of the ocean, and fundamentally altering nitrogen cycling in the sea.

Fig. 1.

Experiment locations overlaid on dissolved inorganic carbon (DIC) concentrations at 200 m depth from Goyet et al. (52). The location of the HOT experiments is denoted by the white square, the SPOT experiment is denoted by a black square, BATS is denoted by a white circle, and the locations of the two Sargasso Sea experiments are denoted by black circles.

Fig. 2.

Reductions in ammonia oxidation rates in ocean acidification experiments in (A) the Sargasso Sea, at (B) BATS, at (C) SPOT, at (D) HOT 209, and at (E) HOT 210. pH_total values are noted along the horizontal axis (calculated pH_total values are shown for the HOT 209 experiment). Statistically significant differences among means (P < 0.05) were determined via one-way ANOVA, and error bars denote 1 SD of triplicate treatments. Ammonia oxidation rates at SPOT were calculated from the linear accumulation of ¹⁵N label in the oxidized pool over the course of the experiment; all other values represent end-point measurements.

Fig. 3.

Correspondence between ammonia oxidation rates and pH_total for all experiments. Ammonia oxidation rates were renormalized to the maximum rate measured in the experiment. For the Sargasso Sea regression line, y = 310x – 2,410, r² = 0.87, and P < 0.05. Calculated pH_total values are shown for HOT 209, and error bars denote 1 SD among triplicate treatments, except in the case of rate measurements in the Sargasso Sea, where error bars denote the SE of triplicate measurements.

Fig. 4.

Renormalized acidification-driven decreases in ammonia oxidation rates. Rate reductions are expressed as a percentage decrease in rates in acidified seawater compared with controls and are normalized to a 0.1 unit decrease in pH from 8.1 to 8. Previously reported data for >0.5 pH changes in Huesemann et al. (8) are included for comparison and denoted by the orange line; other colors are for experiments that are identical to those in Fig. 3. The mean reduction is denoted by the dashed gray line.