Spatiotemporal Variations Dictate Stable and Resilient Microbiome Interactions in the Chesapeake Bay

Abstract Background: Annually reoccurring microbial populations with strong spatial and temporal variations have been identified in estuarine environments, especially in those with long residence time such as the Chesapeake Bay (CB). However, it is unclear how microbial taxa interact with each other (e.g., mutualistic and competitive interactions) and how these interactions respond to their surrounding environments. Specifically, there is a lack of understanding of how these interactions influence microbiome population dynamics, and its adaptability and resilience to estuarine gradients. Results: Here, we constructed co-occurrence networks on prokaryotic microbial communities in the Bay, which included seasonal samples from seven spatial stations along the salinity gradients for three consecutive years. Our results showed that spatiotemporal variations of planktonic microbiomes promoted differentiations of the characteristics and stability of prokaryotic microbial networks in the CB estuary. Prokaryotic microbial networks are more stable seasonally than spatially, and microbes were more strongly connected during warm season compared to the associations during cold season. In addition, microbial interactions were more stable in the lower Bay (ocean side) than those in the upper Bay (freshwater side). Interestingly, compared to the abundant groups, the rare taxa such as SAR116 clade, SAR11 clade III, and OM182 clade contributed greatly to the stability and resilience of prokaryotic microbial interactions in the Bay. Modularity and cluster structures of microbial networks varied spatiotemporally, which provided valuable insights into the ‘small world’ (a group of more interconnected species), network stability, and habitat partitioning/preferences. Multivariate regression tree (MRT) analysis and Piecewise structural equation modeling (SEM) indicated that temperature, salinity and total suspended substances directly or indirectly (through nutrient availability, particulate carbon and Chl a) affected the distribution and associations of microbial groups, such as Actinobacteria, Bacteroidetes, Cyanobacteria, Planctomycetes, Proteobacteria, and Verrucomicrobia.Conclusion: Our results shed light on how spatiotemporal variations alter the nature and stability of prokaryotic microbial networks in the estuarine ecosystem, as well as the ability of planktonic microbiomes and their interactions to resist future disturbances.