Association of Microbial Networks with the Coastal Seafloor Macrofauna Ecological State

Recent evidence suggests that there is a major switch in coastal seafloor microbial ecology already at a mildly deteriorated macrofaunal state. This knowledge is of critical value in the management and conservation of the coastal seafloor. We therefore aimed to determine the relationships between seafloor microbiota and macrofauna on a regional scale. We compared prokaryote, macrofauna, chemical, and geographical data from 1546 seafloor samples, which varied in their exposure to aquaculture activities along the Norwegian and Icelandic coasts. We found that the seafloor samples contained either a network centralized by a sulfur oxidizer (42.4% of samples, n = 656) or a network centralized by an archaeal ammonium oxidizer (44.0% of samples, n = 681). Very few samples contained neither network (9.8% of samples, n = 151) or both (3.8% of samples, n = 58). Samples with a sulfur oxidizer network had a 10-fold higher risk of macrofauna loss (odds ratios, 95% CI: 9.5 to 15.6), while those with an ammonium oxidizer network had a 10-fold lower risk (95% CI: 0.068 to 0.11). The sulfur oxidizer network was negatively correlated to distance from Norwegian 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 distance from Norwegian aquaculture sites (Spearman rho = 0.67, p < 0.01). Based on 356 high-quality metagenome-assembled genomes (MAGs), we found that bicarbonate-dependent carbon fixation and low-affinity oxygen respiration were associated with the ammonium oxidizer network, while the sulfur oxidizer network was associated with ammonium retention, sulfur metabolism, and high-affinity oxygen respiration. In conclusion, our findings highlight the critical roles of microbial networks centralized by sulfur and ammonium oxidizers in mild macrofauna deterioration, which should be included as an essential part of seafloor surveillance.