Bioturbation determines the response of benthic ammonia-oxidizing microorganisms to ocean acidification

Ocean acidification (OA), caused by the dissolution of increasing concentrations of atmospheric carbon dioxide (CO2) in seawater, is projected to cause significant changes to marine ecology and biogeochemistry. Potential impacts on the microbially driven cycling of nitrogen are of particular concern. Specifically, under seawater pH levels approximating future OA scenarios, rates of ammonia oxidation (the rate-limiting first step of the nitrification pathway) have been shown to dramatically decrease in seawater, but not in underlying sediments. However, no prior study has considered the interactive effects of microbial ammonia oxidation and macrofaunal bioturbation activity, which can enhance nitrogen transformation rates. Using experimental mesocosms, we investigated the responses to OA of ammonia oxidizing microorganisms inhabiting surface sediments and sediments within burrow walls of the mud shrimp Upogebia deltaura. Seawater was acidified to one of four target pH values (pHT 7.90, 7.70, 7.35 and 6.80) in comparison with a control (pHT 8.10). At pHT 8.10, ammonia oxidation rates in burrow wall sediments were, on average, fivefold greater than in surface sediments. However, at all acidified pH values (pH < = 7.90), ammonia oxidation rates in burrow sediments were significantly inhibited (by 79-97%; p < 0.01), whereas rates in surface sediments were unaffected. Both bacterial and archaeal abundances increased significantly as pHT declined; by contrast, relative abundances of bacterial and archaeal ammonia oxidation (amoA) genes did not vary. This research suggests that OA could cause substantial reductions in total benthic ammonia oxidation rates in coastal bioturbated sediments, leading to corresponding changes in coupled nitrogen cycling between the benthic and pelagic realms.

pH and calcium change in the microenvironment of a benthic foraminifer (Ammonia sp.) and its size during experiments

Calcareous foraminifera are well known for their CaCO3 shells. Yet, CaCO3 precipitation acidifies the calcifying fluid. Calcification without pH regulation would therefore rapidly create a negative feedback for CaCO3 precipitation. In unicellular organisms, like foraminifera, an effective mechanism to counteract this acidification could be the externalization of H+ from the site of calcification. In this study we show that a benthic symbiont-free foraminifer Ammonia sp. actively decreases pH within its extracellular microenvironment only while precipitating calcite. During chamber formation events the strongest pH decreases occurred in the vicinity of a newly forming chamber (range of gradient about 100 µm) with a recorded minimum of 6.31 (< 10 µm from the shell) and a maximum duration of 7 h. The acidification was actively regulated by the foraminifera and correlated with shell diameters, indicating that the amount of protons removed during calcification is directly related to the volume of calcite precipitated. The here presented findings imply that H+ expulsion as a result of calcification may be a wider strategy for maintaining pH homeostasis in unicellular calcifying organisms.