The deep sea is the most extensive biome within the biosphere, encompassing more than 90% of the ocean's total microbial population. Microbes in the deep ocean play a significant role in the biological carbon pump (BCP) by transforming particulate organic carbon (POC) into dissolved organic carbon (DOC). However, depth-resolved functional partitioning between particle-attached microorganisms (PAM) and free-living microorganisms (FLM), and their respective ecological roles across the full water column, remains poorly characterized. Here, we present a genome-resolved metagenomic and functional analysis of 75 size-fractionated samples from the Western Pacific Ocean (WPO), spanning the epipelagic to abyssopelagic zones. We recovered 1,517 metagenome-assembled genomes (MAGs; 664 near-complete, 558 high-quality, 295 medium-quality) representing 26 classified bacterial and archaeal phyla. Our MAG inventory, spanning four pelagic depth zones and paired size fractions, complements prior depth- or site-focused efforts such as the Malaspina circumnavigation, Station ALOHA, and South China Sea surveys. Permutational multivariate analysis of variance (PERMANOVA) revealed that both lifestyles and depth together influenced microbial community composition in the water column, with divergence between PAM and FLM peaking in the mesopelagic zone (genus-level, R² = 0.247, p = 0.002). The co-occurrence network analysis indicated a depth-structured microbial community, with FLM genera predominant in the epipelagic zone and PAM genera more prevalent in the meso and abyssopelagic zones. The constructed network comprised 113 positive and zero negative associations, indicating niche-based co-occurrence among the microbes. The FLM communities were enriched for deep-sea chemolithoautotrophic lineages (SAR324 and Nitrospinota) and the refractory dissolved organic matter (DOM)-degrading SAR202 clade, whereas alphaproteobacterial and cyanobacterial signatures characterized PAM communities. Carbon fixation and refractory DOM degradation pathways were more prevalent in FLM communities across all depths. In contrast, PAM communities reorganized their metabolism with depth, shifting from a photosynthesis signature in the epipelagic to oxidative phosphorylation and quorum sensing in the meso- and bathypelagic, and to a broad generalist gene repertoire in the abyssal zone. Collectively, these findings indicate that the mesopelagic twilight zone serves as the main hotspot for PAM–FLM functional divergence in the WPO.

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