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.