218 / 2025-04-15 10:45:27

Mechanism of Estuarine Sediment Virus-host Interactions in Global RDOC Degradation

Estuarine Sediments,Virus-host Interactions,RDOC Degradation,Biogeochemical cycles

Sediments are both sources and sinks in the Earth's biogeochemical cycles. Dissolved organic carbon (DOC) accounts for over 90% of the total marine organic carbon pool, with a substantial portion converted into recalcitrant DOC (RDOC) by the microbial carbon pump (MCP), subsequently accumulating in sediments (Jiao et al., 2024). Estuaries are located at the interface of terrestrial and marine ecosystems, with frequent human activities, high microbial diversity, and biogeochemical dynamics. Estuarine environments not only receive RDOC inputs from terrestrial and anthropogenic sources but also generate significant amounts of marine-derived RDOC in situ. The microbial degradation of various RDOC in estuarine sediment may have greatly influenced element cycles and ecological functions in global marine ecosystems (Gao et al., 2024; Jiao et al., 2024). Whereas virus-host interactions fairly drive biogeochemical processes in estuaries (Luo et al., 2022), their roles in RDOC degradation remain poorly understood.

In this study, 240 metagenomic samples from seven types of aquatic sedimentary ecosystems globally were analyzed. A total of 1,708 MAGs (ANI<98%, completeness≥50%, contamination<5%) were obtained, which varied in abundance across ecosystems. The estuarine samples showed outstanding alpha diversity, while the beta diversity analysis suggests the transitional feature of the estuarine sedimentary microbial community between land and ocean. 29,098 vOTUs (ANI<95%, coverage>85%) were also identified, with a significant fraction of unclassified vOTUs (n = 20,463, 70%). The alpha diversities of estuarine sedimentary viral communities were significantly higher than those in other sedimentary environments. The compositions of viral communities of global sedimentary samples were generally similar to those of prokaryotic communities, suggesting the wide prokaryotic host range and potential frequent spread of viruses in global sediments. Based on these results, we hypothesize that estuaries play the gathering and transferring roles in global sedimentary ecosystems.

Preliminary analysis of microbial RDOC-degrading genes in sediments revealed ecosystem-specific metabolic patterns. Viruses from ridge and cold seep sediments displayed diverse RDOC degradation potential, while those from trench sediments were particularly enriched in genes of degrading cellulose and chitin. Notably, prokaryotes and viruses from estuarine sediments—especially Changjiang River Estuaries, Jiulong River Estuaries, and Pearl River Estuaries from China—exhibited high degradation potential for various RDOC of terrestrial (hemicellulose and pectin), anthropogenic (pesticides), and multiple (starch and chitin) sources. RDOC-degrading genes in prokaryotes from cold seep sediments were enriched in pesticides, starch, and chitin degradation, while those from deep-sea sediments were enriched in plastics, pesticides, and chitin. Besides, prokaryotes from trench sediments showed the potential for pesticides, polycyclic aromatic hydrocarbons (PAHs), and chitin degradation.

These findings highlight the critical roles of estuarine viruses and their microbial hosts in linking carbon cycling processes across global sedimentary ecosystems.