Community organization and network complexity and stability: contrasting strategies of prokaryotic versus eukaryotic microbiomes in the Bohai Sea and Yellow Sea

Abstract

ABSTRACT Unraveling the effects of spatial gradients on microbiome assembly and association is a challenging topic that remains understudied in the coastal ecosystem. Here, we aimed to investigate the effects of spatial variation on the network complexity and stability of plankton microbiomes in the Bohai Sea and Yellow Sea. These seas serve as spawning and nursery grounds for economically important fisheries valued at billions of dollars annually. Environmental heterogeneity structures microbial communities into distinct spatial patterns, leading to complex direct/indirect relationships and broader ecological niches of bacterioplankton compared to microeukaryotic communities. Interestingly, salinity gradients positively influenced the richness of rare subgroups of bacterioplankton, while the rare microeukaryotic subgroups showed an opposite trend. Abundant subgroups of prokaryotic/eukaryotic microbiomes exhibited greater environmental niche breadth and lower phylogenetic distance compared to the rare subgroups. Stochastic processes contributed greatly to microbiome dynamics, and deterministic processes governed the bacterioplankton organization with a lower phylogenetic turnover rate. Compared to microeukaryotes, bacterioplankton exhibit higher network modularity, complexity, and robustness and lower fragmentation, and vulnerability. These observations offer vital insights into the anti-interference ability and resistance of plankton microbiomes in response to environmental gradients in terms of organization and survival strategy as well as their adaptability to environmental disturbances. IMPORTANCE An in-depth understanding of community organization and stability of coastal microbiomes is crucial to determining the sustainability of marine ecosystems, such as the Bohai Sea and Yellow Sea. Distinct responses between prokaryotic and eukaryotic microbiomes to spatial heterogeneity were observed in terms of geographical distribution, phylogenetic distance, niche breadth, and community assembly process. Environmental variations are significantly correlated with the dynamics of rare eukaryotic plankton subcommunities compared to prokaryotic plankton subcommunities. Deterministic processes shaped prokaryotic plankton community organization with a lower phylogenic turnover rate. Rare subgroups had noticeably higher phylogenetic distance and lower niche breadth than the corresponding abundant subgroups. Prokaryotic microbiomes had higher molecular network complexity and stability compared to microeukaryotes. Results presented here show how environmental gradients alter both the geographical characteristics of the microbial organization in coastal seas and also their co-occurrence network complexity and stability and thus have critical implications for nutrient and energy cycling.