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

(2025) 13:208 Lv et al. Microbiome https://doi.org/10.1186/s40168-025-02192-w Microbiome Open Access RESEARCH Clear niche partitioning of nitrite‑oxidizing bacteria from the bottom and the slope of Mariana Trench Yongxin Lv1,2,3,4, Lizhi Zhang3 and Yu Zhang1,2,4* Abstract 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. Keywords Hadal trench, Nitrite-oxidizing bacteria, Metagenome, Metatranscriptome *Correspondence: Yu Zhang Full list of author information is available at the end of the article © The Author(s) 2025. Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/. Lv et al. Microbiome (2025) 13:208 Introduction The Mariana Trench is the deepest part of the ocean, ranging from 6000 to 11,000 m in depth and accounting for approximately 45% of the ocean’s vertical depth gradient [1]. Characterized by extreme conditions such as high pressure, complete darkness, and low temperature, this environment shapes a unique microbial community that differs significantly from those found in other oceanic regions [2–5]. In terms of species diversity, Zhou et al. reported that 26± 7% of 16S rDNA fragments from the Challenger Deep sediment had not been previously identified in the SILVA database [6]. With respect to metabolic potential, Chen et al. reported that single-cell amplified genomes of deepsea Roseobacter and Alteromonas contained more genes related to mobilomes and metal transport [7]. Similarly, Zhu et al. reported that Bacteroidetes from the hadal zone possessed more CAZyme-related genes than did their counterparts in surface waters [8]. In addition, the V-shaped topography of the trench facilitates the accumulation of materials from lateral transport and the ocean surface at the bottom, leading to ecological differences between the bottom and slope [9, 10]. For example, the proportion of novel 16S rDNA fragments increases with depth, and anammox activity has been observed only in surface sediments at the bottom [6]. The accumulation of heavy metals here also suggests microbial detoxification processes [11]. In summary, the microorganisms in hadal trench sediments exhibit unique adaptations to their extreme environments [12]. Nitrite-oxidizing bacteria (NOB) possess nitrite oxidase, enabling them to produce nitrate [13]. In addition to comammox bacteria, they are the only known microbial sources of nitrate [14]. NOB can be categorized into two types based on their key enzyme nitrite oxidoreductase: the cytoplasmic type and the periplasmic type. The cytoplasmic type, such as Nitrobacter and Nitrococcus, thrives in environments with high nitrite concentrations, whereas the periplasmic type, including Nitrospira and Nitrospina, is better suited to low nitrite concentrations [13]. All NOB groups are capable of carbon fixation through the Calvin‒Benson‒Bassham (CBB) cycle or the reverse tricarboxylic acid (rTCA) cycle [15–17]. Some NOB can also oxidize simple organic compounds, such as formate, in mixotrophic mode or oxidize hydrogen and sulphur compounds for energy [18, 19]. In previous studies on the Mariana Trench, NOB such as Nitrospira and Nitrospirae, but not comammox, were identified [5, 6]. Recent studies have demonstrated that nitrate serves as an essential electron acceptor in hadal trenches and may be even more important than oxygen. For example, the high hydrostatic pressure in the trench stimulates Page 2 of 15 the generation of intracellular reactive oxygen species (ROS), leading microbes to use alternative electron acceptors, such as nitrate from microbial nitrification [20], even in the presence of oxygen [20–23]. Therefore, as the sole producers of nitrate, NOB are expected to play a critical role in nitrogen and carbon cycling in the hadal environment. Previous studies have shown that microbes can evolve distinct metabolic traits and exhibit varying metabo (...truncated)