Key Roles of Microbial Sulfur and Ammonium Oxidizers in Determining the Coastal Seafloor Ecological State

Recent evidence suggests that there is a major switch in coastal seafloor microbial ecology already at a mildly deteriorated macrofauna state. This knowledge is of critical value in the management and conservation of the coastal seafloor. This study aimed to determine the relationships between seafloor microbiota and macrofauna on a large regional scale. We compared prokaryote, macrofauna, chemical, and geographical data from 1,546 seafloor samples which varied in their exposure to aquaculture activities along the Norwegian and Icelandic coast. We found that the seafloor samples contained either a sulfur oxidizer network (42.4%, n=656), or an ammonium oxidizer network of microbes (44.0%, n=681). Very few samples contained neither of the networks (9.8%, n=151), or both (3.8%, n=58). Samples with a sulfur oxidizer network had a tenfold higher risk of macrofauna loss (95% CI: 9.5 to 15.6), while those with an ammonium oxidizer network had a tenfold lower risk (95% CI: 0.068 to 0.11). The sulfur oxidizer network was negatively correlated with the distance to aquaculture sites (Spearman rho = -0.42, p < 0.01), and was present in all Icelandic samples (n = 274). The ammonium oxidizer network was absent from Icelandic samples, and positively correlated to the distance from aquaculture sites (Spearman rho = 0.67, p < 0.01). Based on 357 high-quality metagenome-assembled genomes (MAGs), we found that the main metabolic process for the ammonium oxidizer network was cobalamin-dependent, while the sulfur oxidizer network was associated with both ammonium retention and sulfur metabolism. In conclusion, our findings highlight the critical roles of sulfur and ammonium oxidizers in mild macrofauna deterioration.