Complex seafloor topography promotes ciliate population expansion but maintains high community similarity and stability in the deep sea

Environmental selection and neutral processes drive diversification and evolution, thereby influencing the biodiversity and biogeography of the microbiome. The deep sea, with its vast and complex geological structures, is ideal for studying microbial biogeography; however, it remains underexplored due to technical limitations. Based on the Anna Karenina principle, we hypothesize that environmental selection induced by complex topography increases community heterogeneity, which further leads to instability of deep-sea microbial communities. To test this, near-bottom water samples were collected from the trench ridge cross-linked zone with complex topography and from the abyssal plain in the western Pacific Ocean. Utilizing next-generation and third-generation sequencing technologies, we analyzed population expansion, ecological niches, and community structure and dynamics, including beta diversity, stability and assembly process, of the deep-sea ciliates. The results indicated that both environmental selection and neutral processes were important factors driving the ciliate communities, while their relative importance varied across different topographies in the deep sea. In the topographically complex region, environmental selection promoted the population expansion of specific ciliate species, indicated by higher haplotype diversity and increased distinct amplicon sequence variants aligning to the same species. This specific population expansion resulted in higher alpha diversity but lower beta diversity. Higher niche breadth and niche overlap values, and more positive interactions, were observed in the co-occurrence network of ciliates in the topographically complex region, leading to higher community stability. In the abyssal plain, however, neutral processes dominated the ciliate community assembly, with limited population expansion, lower alpha diversity but higher community heterogeneity. These findings contradict our hypothesis based on the Anna Karenina principle. Our study challenges the Anna Karenina principle and provides novel insights into the diversity and dynamics of deep-sea ciliate communities under varying topographic complexities from individual species to community-wide scales. • Complex seafloor topography promotes the population expansion of specific ciliate species. • Higher niche widths and overlaps lead to more bio-interactions under complex topography. • Complex topography stabilizes communities but reduces heterogeneity, defying Anna Karenina principle. • Lower alpha diversity but higher heterogeneity in abyssal plains is mainly driven by neutral processes.