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

Abstract

Ocean acidification (OA), caused by the dissolution of increasing concentrations of atmospheric carbon dioxide (CO 2 ) 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 (pH T 7.90, 7.70, 7.35 and 6.80) in comparison with a control (pH T 8.10). At pH T 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 pH T 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.

Simulation of Coastal Processes affecting pH with Impacts on Carbon and Nutrient Biogeochemistry

“…Previous studies were focused either in predicting the effects of future pH reduction or investigating the biogeochemical outcomes of coastal pH decline on certain organisms' response/survival or merely on the processes ultimately determining CO 2 fate and impact in aquatic systems (e.g. Andersson et al, 2007;Kitidis et al, 2011;Widdicombe et al, 2009;Laverock et al, 2014). Marine systems however, constitute of specific features, more complex than simple chemical or thermodynamic equilibria which are necessary, nonetheless, for any calculation or prediction model.…”

Bioturbation Effects of Chironomid Larvae on Nitrogen Release and Ammonia-Oxidizing Bacteria Abundance in Sediments

“…In these studies, the results indicate that bioturbation can have a great impact on denitrification, and very low nitrification can occur [15,17]. However, another study shows bioturbation related to ammonia oxidation, which is generally considered to be the critical rate-limiting step of the nitrification process [18]. Since different phenomena behind the larvae bioturbation on N release have been observed, the apparently contradictory results may illustrate the relative importance of capturing more realistic and accurate information about the sediment microenvironment.…”

Ocean acidification and climate change: advances in ecology and evolution

“…The importance of species-environment interactions is considered in more detail by Laverock et al [57], who show that ocean acidification has the potential to significantly modify the relationship between benthic macroinfauna (here, the burrowing shrimp Upogebia deltaura) and ammoniaoxidizing microorganisms inhabiting burrow walls. They show that under low pH conditions, ammonia oxidation associated with burrow walls significantly reduces and that ocean acidification has the potential to negate the positive impact that shrimp bioturbation otherwise has on microbial nitrogen cycling.…”