Biogeographic shifts in the microbial co-occurrence network features of three domains across complex environmental gradients in subtropical coastal waters

Abstract Background Bacteria, Archaea, and Microeukaryotes comprise taxonomic domains that interact in mediating biogeochemical cycles in coastal waters. Many studies have revealed contrasting biogeographic patterns of community structure and assembly mechanisms in microbial communities from different domains in coastal ecosystems; however, knowledge of specific biogeographic patterns on microbial co-occurrence relationships across complex coastal environmental gradients remains limited. Using a dense sampling scheme at the regional scale, SSU rRNA gene amplicon sequencing, and network analysis, we investigated intra- and inter-domain co-occurrence relationships and network topology-based biogeographic patterns from three microbial domains in coastal waters that show environmental gradients across the inshore-nearshore-offshore continuum in the East China Sea. Results Overall, we found the highest complexity and connectivity in the bacterial network, the highest modularity in the archaeal network, and the lowest complexity, connectivity, and modularity in the microeukaryotic network. Although microbial co-occurrence networks from the three domains showed distinct topological features, they exhibited a consistent biogeographic pattern across the inshore-nearshore-offshore continuum. Specifically, the nearshore zones with intermediate levels of terrestrial impacts reflected by multiple environmental factors (including water temperature, salinity, pH, dissolved oxygen, and nutrient-related parameters) had a higher intensity of microbial co-occurrence for all three domains. In contrast, the intensity of microbial co-occurrence was weaker in both the inshore and the offshore zones at the two ends of the environmental gradients. Archaea occupied a central position in the microbial inter-domain co-occurrence network. In particular, members of the Thaumarchaeota Marine Group I (MGI, now placed within the Family Nitrosopumilaceae of the Phylum Thermoproteota) appeared to be the hubs in the biogeographic shift between inter-domain network modules across environmental gradients. Conclusions Our work offers new insights into microbial biogeography by integrating network features into biogeographic patterns, towards a better understanding of the potential of microbial interactions in shaping biogeographic patterns of coastal marine microbiota.