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Background <p>The hadal zone, characterized by extreme hydrostatic pressure and geographic isolation, hosts microbial communities uniquely adapted to these harsh conditions. While niche partitioning has been observed in other deep-sea environments, its existence within hadal trench ecosystems remains controversial. Focusing on the Mariana Trench, we investigated whether nitrite-oxidizing bacteria (NOB) exhibit depth-stratified ecological specialization between slope (6000–10,000&#xa0;m) and bottom (&gt; 10,000&#xa0;m) sediments. By analysing the genomic features and ecological interactions of NOB, we aimed to resolve their functional roles in nitrogen cycling under distinct hadal microniches.</p> Results <p>We reconstructed 8 high-quality NOB metagenome-assembled genomes (MAGs) from 58 sediment metagenomes, revealing stark niche differentiation between depth zones. Slope-dominant NOB harboured expanded genetic arsenals for antioxidation (e.g. superoxide dismutase) and osmoprotection (compatible solute transporters), Suggesting enhanced adaptive capacity to pressure-adjacent stresses. Metatranscriptomics revealed 1.48 × (<i>nxrA</i>) and 1.28 × (<i>aclA</i>) greater expression of nitrite oxidation and carbon fixation genes in slope communities than in their bottom counterparts. Network analysis identified slope NOB as keystone taxa with elevated among-module connectivity and intramodule linkages, in contrast with bottom NOB, which exhibited localized nitrate-production gene networks. Functional profiling revealed complementary biogeochemical roles: slope NOB primarily consumed nitrite, whereas bottom populations dominated nitrate synthesis.</p> Conclusion <p>Our multiomics analysis revealed depth-dependent niche partitioning among hadal NOB, with transcriptional and network evidence supporting distinct pressure adaptation strategies and biogeochemical functions. The slope-bottom differentiation in stress response systems and nitrogen transformation pathways highlights how micron-scale environmental gradients drive microbial specialization in Earth’s deepest ecosystems. These findings establish NOB as critical mediators of hadal biogeochemical cycles and provide a framework for understanding microbial resilience in extreme biospheres.</p> <p><MediaObject ID="MOESM2"> <VideoObject FileRef="MediaObjects/40168_2025_2192_MOESM2_ESM.mp4" VideoID="9RPbM9VJpW-i6vhNYUrSyW"> <Caption Language="En" xml:lang="en"> <CaptionContent> <p>Video Abstract</p> </CaptionContent> </Caption> </VideoObject> </MediaObject></p>

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Clear niche partitioning of nitrite-oxidizing bacteria from the bottom and the slope of Mariana Trench

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年10月16日

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  • Yongxin Lv,
  • Lizhi Zhang,
  • Yu Zhang

摘要

Background

The hadal zone, characterized by extreme hydrostatic pressure and geographic isolation, hosts microbial communities uniquely adapted to these harsh conditions. While niche partitioning has been observed in other deep-sea environments, its existence within hadal trench ecosystems remains controversial. Focusing on the Mariana Trench, we investigated whether nitrite-oxidizing bacteria (NOB) exhibit depth-stratified ecological specialization between slope (6000–10,000 m) and bottom (> 10,000 m) sediments. By analysing the genomic features and ecological interactions of NOB, we aimed to resolve their functional roles in nitrogen cycling under distinct hadal microniches.

Results

We reconstructed 8 high-quality NOB metagenome-assembled genomes (MAGs) from 58 sediment metagenomes, revealing stark niche differentiation between depth zones. Slope-dominant NOB harboured expanded genetic arsenals for antioxidation (e.g. superoxide dismutase) and osmoprotection (compatible solute transporters), Suggesting enhanced adaptive capacity to pressure-adjacent stresses. Metatranscriptomics revealed 1.48 × (nxrA) and 1.28 × (aclA) greater expression of nitrite oxidation and carbon fixation genes in slope communities than in their bottom counterparts. Network analysis identified slope NOB as keystone taxa with elevated among-module connectivity and intramodule linkages, in contrast with bottom NOB, which exhibited localized nitrate-production gene networks. Functional profiling revealed complementary biogeochemical roles: slope NOB primarily consumed nitrite, whereas bottom populations dominated nitrate synthesis.

Conclusion

Our multiomics analysis revealed depth-dependent niche partitioning among hadal NOB, with transcriptional and network evidence supporting distinct pressure adaptation strategies and biogeochemical functions. The slope-bottom differentiation in stress response systems and nitrogen transformation pathways highlights how micron-scale environmental gradients drive microbial specialization in Earth’s deepest ecosystems. These findings establish NOB as critical mediators of hadal biogeochemical cycles and provide a framework for understanding microbial resilience in extreme biospheres.

Video Abstract