Stochastic and Deterministic Assembly Processes in Seamount Microbial Communities

Abstract

Seamounts are ubiquitous in the ocean. However, little is known about how seamount habitat features influence the local microbial community. In this study, the microbial populations of sediment cores from sampling depths of 0.1 to 35 cm from 10 seamount summit sites with a water depth of 1,850 to 3,827 m across the South China Sea (SCS) Basin were analyzed. Compared with nonseamount ecosystems, isolated seamounts function as oases for microbiomes, with average moderate to high levels of microbial abundance, richness, and diversity, and they harbor distinct microbial communities. The distinct characteristics of different seamounts provide a high level of habitat heterogeneity, resulting in the wide range of microbial community diversity observed across all seamounts. Using dormant thermospores as tracers to study the effect of dispersal by ocean currents, the observed distance-decay biogeography across different seamounts shaped simultaneously by the seamounts' naturally occurring heterogeneous habitat and the limitation of ocean current dispersal was found. We also established a framework that links initial community assembly with successional dynamics in seamounts. Seamounts provide resource-rich and dynamic environments, which leads to a dominance of stochasticity during initial community establishment in surface sediments. However, a progressive increase in deterministic environmental selection, correlated with resource depletion in subsurface sediments, leads to the selective growth of rare species of surface sediment communities in shaping the subsurface community. Overall, the study indicates that seamounts are a previously ignored oasis in the deep sea. This study also provides a case study for understanding the microbial ecology in globally widespread seamounts. IMPORTANCE Although there are approximately 25 million seamounts in the ocean, surprisingly little is known about seamount microbial ecology. We provide evidence that seamounts are island-like habitats harboring microbial communities distinct from those of nonseamount habitats, and they exhibit a distance-decay pattern. Environmental selection and dispersal limitation simultaneously shape the observed biogeography. Coupling empirical data with a null mode revealed a shift in the type and strength, which controls microbial community assembly and succession from the seamount surface to the subsurface sediments as follows: (i) community assembly is initially primarily driven by stochastic processes such as dispersal limitation, and (ii) changes in the subsurface environment progressively increase the importance of environmental selection. This case study contributes to the mechanistic understanding essential for a predictive microbial ecology of seamounts.

Keywords: South China Sea; neutral theory; niche theory; seamount.

FIG 1

Location and bathymetric profile of the SCS seamount sediment cores. Map of the South China Sea showing the 10 seamount sampling locations and bathymetry of the study area.

FIG 2

Comparison of the SCS seamount sedimentary microbiome. (A) Microbial abundance, Chao1 richness, Shannon index, and TOC content with water depth in the SCS seamount surface sediment (orange frame) and the SCS nonseamount surface sediment (gray frame). (B) Thermospore abundance, Chao1 richness, and Shannon index with water depth in the SCS seamount surface sediment. (C and D) Richness estimates and Shannon index based on OTU 0.03. (E) Microbial community composition of seawater, global nonseamount surface sediment, and the SCS seamount sediment samples visualized by nonmetric multidimensional scaling. Each circle represents one microbial community. (F and G) Seamount sediment microbial and thermospore abundance, Chao 1 richness, and Shannon index changes with TOC concentration variation.

FIG 3

Taxonomic composition of seamount and nonseamount microbial communities at the phylum (A) and order levels (B) using bacteria and archaeal universal primers. The microbial sequence was transformed to Z-scores before calculating abundance. The OTUs with less than 0.1% total relative sequence abundance of each collected sample were not displayed.

FIG 4

Comparison of the seamount surface sediment microbiome. (A to D) Distance-decay biogeographic patterns of in situ microorganisms (A and B) and thermospore communities (C and D) at horizontal distances and vertical distances. (E and F) Null model investigating the seamount surface sediment microbial community assembly process across horizontal distance (E) and vertical distance (F). (G and H) Venn diagrams showing the numbers of endemism and cosmopolitan OTUs (gray cycle) among 10 different seamounts of in situ microorganisms (G) and thermospores (H).

FIG 5

Vertical community variation in microbial community composition (A) and predicted ecological functions (B) from the sediment-water interface sediment to the bottom of push core subsurface sediment samples. The predicted ecological functions based on 16S rRNA genes of microbial community composition.