Diversity and connectivity of bacterial communities in polymetallic nodule-rich abyssal plains (Eastern Tropical Pacific)

Polymetallic nodules of the abyssal seafloor are considered potential resources of nickel, cobalt, copper, as well as rare earth elements. The Clarion-Clipperton Fracture Zone (CCZ) hosts potential nodule mining sites licensed to several contractors for exploration of the metal resources. A solid understanding of natural conditions and their variability is fundamental for assessing environmental risks of future mining, particularly regarding microbial communities that play key roles in biogeochemical processes and ecosystem functioning. In this study, we sequenced 16S ribosomal RNA (rRNA) genes from environmental samples across polymetallic nodule fields in the Pacific Ocean to investigate baseline patterns of benthic bacterial diversity. Bacterial communities were compared among sediments, nodules, and bottom waters. Samples from the DISCOL Experimental Area in the Peru basin are included in the analysis to provide a broader spatial perspective. The patterns of benthic bacterial diversity and connectivity observed in this study corroborate those previously reported, extending across spatial scales from tens to thousands of kilometers. These patterns include: higher bacterial alpha-diversity in sediments compared to nodules and bottom waters, and benthic bacterial communities enriched by taxa that are potentially involved in metal cycling and resilient to metal toxicity (e.g., Hyphomicrobiaceae, Magnetospiraceae, Methyloligallaceae, Kiloniellaceae). Our findings underscore the significance of these patterns for the management of mining activities in deep-sea environments. The most abundant taxa showed a high connectivity between areas investigated, with differences mostly controlled by isolation-by-distance. Still, bacterial community structures showed substantial differences among investigated areas that were partly driven by the availability of trophic resources and nodule coverage. Turnover in community structure on a regional scale was small and mainly controlled by distance. However, community composition in terms of relative abundances showed a high variability even on local scales <30km, most likely due to spatial heterogeneity in environmental conditions (e.g., topography and nodule coverage). These results indicate that environmental management of deep-sea mining and conservation strategies should consider both regional connectivity and local heterogeneity in microbial communities. Establishing no-take or reference areas with similar microbial composition to mining sites will be essential to preserve ecosystem functions and services.