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Understanding the factors that modulate prokaryotic assemblages and their niche partitioning in marine environments is a longstanding challenge in marine microbial ecology. This study analyzes amplicon sequence variant (ASV) diversity and co-occurrence of prokaryotic (Archaea and Bacteria) communities through coastal-oceanic gradients in the NW Iberian upwelling system and adjacent open-ocean (Atlantic Ocean). Biogeographic patterns were investigated in relation with environmental conditions, mainly focusing on the optical signature of the dissolved organic matter (DOM). Alpha- and beta-diversity were horizontally homogeneous [with the only exception of Archaea (∼1700 m depth), attributed to the influence of Mediterranean water, MW], while beta-diversity was significantly vertically stratified. Prokaryotic communities were structured in four clusters (upper subsurface, lower subsurface, intermediate, and deep clusters). Deep (>2000 m) archaeal and bacterial assemblages, and intermediate (500-2000 m) Bacteria (mainly SAR202 and SAR406), were significantly related to humic-like DOM (FDOM-M), while intermediate Archaea were additionally related to biogeochemical attributes of the high-salinity signature of MW. Lower subsurface (100-500 m) Archaea (particularly one ASV belonging to the genus Candidatus Nitrosopelagicus) were mainly related to the imprint of high-salinity MW, while upper subsurface (≤100 m) archaeal assemblages (particularly some ASVs belonging to Marine Group II) were linked to protein-like DOM (aCDOM254). Conversely, both upper and lower subsurface bacterial assemblages were mainly linked to aCDOM254 (particularly ASVs belonging to Rhodobacteraceae, Cyanobacteria, and Flavobacteriaceae) and nitrite concentration (mainly members of Planctomycetes). Most importantly, our analysis unveiled depth-ecotypes, such as the ASVs MarG.II_1 belonging to the archaeal deep cluster (linked to FDOM-M) and MarG.II_2 belonging to the upper subsurface cluster (related to FDOM-T and aCDOM254). This result strongly suggests DOM-mediated vertical niche differentiation, with further implications for ecosystem functioning. Similarly, positive and negative co-occurrence relationships also suggested niche partitioning (e.g., between the closely related ASVs Thaum._Nit._Nit._Nit._1 and _2) and competitive exclusion (e.g., between Thaum._Nit._Nit._Nit._4 and _5), supporting the finding of non-randomly, vertically structured prokaryotic communities. Overall, differences between Archaea and Bacteria and among closely related ASVs were revealed in their preferential relationship with compositional changes in the DOM pool and environmental forcing. Our results provide new insights on the ecological processes shaping prokaryotic assembly and biogeography.

To study the response of bacteria to different size-fractions of naturally occurring dissolved organic matter (DOM), a natural prokaryotic community from North Atlantic mesopelagic waters (1000 m depth) was isolated and grown in (i) 0.1-μm filtered seawater (CONTROL), (ii) the low-molecular-weight (1 kDa) and low-molecular-weight DOM fractions (H + L-DOM), to test the potential effect of ultrafiltration on breaking the DOM size continuum. Prokaryotic abundance and leucine incorporation were consistently higher in the H + L-DOM niche than in the L-DOM and CONTROL treatments, suggesting a different interaction with each DOM fraction and the disruption of the structural DOM continuum by ultrafiltration, respectively. Rhodobacterales (Alphaproteobacteria) and Flavobacteriales (Bacteroidetes) were particularly enriched in L-DOM and closely related to the colored DOM (CDOM) fraction, indicating the tight link between these groups and changes in DOM aromaticity. Conversely, some other taxa that were rare or undetectable in the original bacterial community were enriched in the H + L-DOM treatment (e.g., Alteromonadales belonging to Gammaproteobacteria), highlighting the role of the rare biosphere as a seed bank of diversity against ecosystem disturbance. The relationship between the fluorescence of protein-like CDOM and community composition of populations in the H + L-DOM treatment suggested their preference for labile DOM. Conversely, the communities growing on the L-DOM niche were coupled to humic-like CDOM, which may indicate their ability to degrade more reworked DOM and/or the generation of refractory substrates (as by-products of the respiration processes). Most importantly, L- and/or H + L-DOM treatments stimulated the growth of unique bacterial amplicon sequence variants (ASVs), suggesting the potential of environmental selection (i.e., changes in DOM composition and availability), particularly in the light of climate change scenarios. Taken together, our results suggest that different size-fractions of DOM induced niche-specialization and differentiation of mesopelagic bacterial communities.