Deep-sea mining of commercially valuable polymetallic nodule fields will generate a seabed sediment plume into the water column. Yet, the response of bacterioplankton communities, critical in regulating energy and matter fluxes in marine ecosystems, to such disturbances is unknown. Metacommunity theory, traditionally used in general ecology for macroorganisms, offers mechanistic understanding on the relative role of spatial differences compared with local environmental conditions (habitat filtering) for community assembly. We examined bacterioplankton metacommunities using 16S rRNA amplicons from the Clarion-Clipperton Zone (CCZ) in the eastern Pacific Ocean and in global ocean transect samples to determine sensitivity of these assemblages to environmental perturbations. Habitat filtering was the main assembly mechanism of bacterioplankton community composition in the epi- and mesopelagic waters of the CCZ and the Tara Oceans transect. Bathy- and abyssopelagic bacterioplankton assemblages were mainly assembled by undetermined metacommunity types or neutral and dispersal-driven patch-dynamics for the CCZ and the Malaspina transect. Environmental disturbances may alter the structure of upper-ocean microbial assemblages, with potentially even more substantial, yet unknown, impact on deep-sea communities. Predicting such responses in bacterioplankton assemblage dynamics can improve our understanding of microbially-mediated regulation of ecosystem services in the abyssal seabed likely to be exploited by future deep-sea mining operations.