Due to the scarcity of organic matter (OM) sources in the bathypelagic (1000–4000 m depth), prokaryotic metabolism is believed to be concentrated on particles originating from the surface. However, the structure of active bathypelagic prokaryotic communities and how it changes across environmental gradients remains unexplored. Using a combination of 16S rRNA gene and transcripts sequencing, metagenomics, and substrate uptake potential measurements, here we aimed to explore how water masses aging and the quality of OM influence the structure of the active microbiome, and the potential implications for community function. We found that the relative contribution of taxa with a free-living lifestyle to the active microbiome increased in older water masses that were enriched in recalcitrant OM, suggesting that these prokaryotes may also play a substantial role in the bathypelagic metabolism of vast areas of the ocean. In comparison to particle-associated prokaryotes, free-living prokaryotes exhibited lower potential metabolic rates, and harbored a limited number of two-component sensory systems, suggesting they have less ability to sense and respond to environmental cues. In contrast, particle-associated prokaryotes carried genes for particle colonization and carbohydrate utilization that were absent in prokaryotes with a free-living lifestyle. Consistently, we observed that prokaryotic communities inhabiting older waters displayed reduced abilities to colonize particles, and higher capabilities to use complex carbon sources, compared to communities in waters with a higher proportion of labile OM. Our results provide evidence of regionalization of the bathypelagic active prokaryotic microbiome, unveiling a niche partitioning based on the quality of OM.

中文翻译：

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水老化和有机碳源的质量驱动活跃的深海原核微生物组的生态位划分

由于深海（1000-4000米深度）有机物（OM）来源稀缺，原核代谢被认为集中在源自表面的颗粒上。然而，活跃的深海原核生物群落的结构及其如何随着环境梯度的变化仍有待探索。结合 16S rRNA 基因和转录本测序、宏基因组学和底物吸收潜力测量，我们旨在探索水团老化和 OM 质量如何影响活性微生物组的结构，以及对群落功能的潜在影响。我们发现，在富含顽固性 OM 的较老水团中，具有自由生活生活方式的类群对活跃微生物组的相对贡献有所增加，这表明这些原核生物也可能在大片海洋区域的深海代谢中发挥重要作用。与颗粒相关的原核生物相比，自由生活的原核生物表现出较低的潜在代谢率，并且拥有数量有限的二元感觉系统，这表明它们感知和响应环境线索的能力较低。相比之下，与颗粒相关的原核生物携带颗粒定殖和碳水化合物利用的基因，而这些基因在具有自由生活生活方式的原核生物中是不存在的。我们一致地观察到，与不稳定 OM 比例较高的水域中的群落相比，居住在较旧水域中的原核群落表现出较低的定殖颗粒能力，以及较高的使用复杂碳源的能力。我们的结果提供了深海活跃原核微生物组区域化的证据，揭示了基于 OM 质量的生态位划分。