Insights into prokaryotic communities and their potential functions in biogeochemical cycles in cold seep

Abstract

ABSTRACT Microorganisms are significant drivers of organic matter mineralization and are essential in marine biogeochemical cycles. However, the variations and influencing factors in prokaryotic communities from cold-seep sediments to the water column and the specific role of these microorganisms in biogeochemical cycles in the water column above cold seep remain unclear. Here, we investigated prokaryotic communities and their roles in nitrogen/sulfur cycling processes and conducted in situ dissolved organic matter (DOM) enrichment experiments to explore the effects of diverse sources of DOM on prokaryotic communities. Field investigations showed that the prokaryotic communities in the near-bottom water were more similar to those in the deep layer of the euphotic zone (44.60%) and at a depth of 400 m (50.89%) than those in the sediment (18.00%). DOM enrichment experiments revealed that adding dissolved organic nitrogen (DON) and phosphorus DOP caused a notable increase in the relative abundances of Rhodobacterales and Vibrionales, respectively. A remarkable increase was observed in the relative abundance of Alteromonadales and Pseudomonadales after the addition of dissolved organic sulfur (DOS). The metagenomic results revealed that Proteobacteria served as the keystone taxa in mediating the biogeochemical cycles of nitrogen, phosphorus, and sulfur in the Haima cold seep. This study highlights the responses of prokaryotes to DOM with different components and the microbially driven elemental cycles in cold seeps, providing a foundational reference for further studies on material energy metabolism and the coupled cycling of essential elements mediated by deep-sea microorganisms. IMPORTANCE Deep-sea cold seeps are among the most productive ecosystems, sustaining unique fauna and microbial communities through the release of methane and other hydrocarbons. Our study revealed that the influence of seepage fluid on the prokaryotic community in the water column is surprisingly limited, which challenges conventional views regarding the impact of seepage fluids. In addition, we identified that different DOM compositions play a crucial role in shaping the prokaryotic community composition, providing new insights into the factors driving microbial diversity in cold seeps. Furthermore, the study highlighted Proteobacteria as key and multifaceted drivers of biogeochemical cycles in cold seeps, emphasizing their significant contribution to complex interactions and processes. These findings offer a fresh perspective on the dynamics of cold-seep environments and their microbial communities, advancing our understanding of the biogeochemical functions in deep-sea environments.