Abyssal foraminifera attached to polymetallic nodules from the eastern Clarion Clipperton Fracture Zone: a preliminary description and comparison with North Atlantic dropstone assemblages

Anthropogenic disturbances such as fishing, mining, oil drilling, bioprospecting, warming, and acidification in the deep sea are increasing, yet generalities about deep-sea biogeography remain elusive. Owing to the lack of perceived environmental variability and geographical barriers, ranges of deep-sea species were traditionally assumed to be exceedingly large. In contrast, seamount and chemosynthetic habitats with reported high endemicity challenge the broad applicability of a single biogeographic paradigm for the deep sea. New research benefiting from higher resolution sampling, molecular methods and public databases can now more rigorously examine dispersal distances and species ranges on the vast ocean floor. Here, we explore the major outstanding questions in deep-sea biogeography. Based on current evidence, many taxa appear broadly distributed across the deep sea, a pattern replicated in both the abyssal plains and specialized environments such as hydrothermal vents. Cold waters may slow larval metabolism and development augmenting the great intrinsic ability for dispersal among many deep-sea species. Currents, environmental shifts, and topography can prove to be dispersal barriers but are often semipermeable. Evidence of historical events such as points of faunal origin and climatic fluctuations are also evident in contemporary biogeographic ranges. Continued synthetic analysis, database construction, theoretical advancement and field sampling will be required to further refine hypotheses regarding deep-sea biogeography.

Deep-sea floors represent one of the largest and most complex ecosystems on Earth but remain essentially unexplored. The vastness and remoteness of this ecosystem make deep-sea sampling difficult, hampering traditional taxonomic observations and diversity assessment. This problem is particularly true in the case of the deep-sea meiofauna, which largely comprises small-sized, fragile, and difficult-to-identify metazoans and protists. Here, we introduce an ultra-deep sequencing-based metagenetic approach to examine the richness of benthic foraminifera, a principal component of deep-sea meiofauna. We used Illumina sequencing technology to assess foraminiferal richness in 31 unsieved deep-sea sediment samples from five distinct oceanic regions. We sequenced an extremely short fragment (36 bases) of the small subunit ribosomal DNA hypervariable region 37f, which has been shown to accurately distinguish foraminiferal species. In total, we obtained 495,978 unique sequences that were grouped into 1,643 operational taxonomic units, of which about half (841) could be reliably assigned to foraminifera. The vast majority of the operational taxonomic units (nearly 90%) were either assigned to early (ancient) lineages of soft-walled, single-chambered (monothalamous) foraminifera or remained undetermined and yet possibly belong to unknown early lineages. Contrasting with the classical view of multichambered taxa dominating foraminiferal assemblages, our work reflects an unexpected diversity of monothalamous lineages that are as yet unknown using conventional micropaleontological observations. Although we can only speculate about their morphology, the immense richness of deep-sea phylotypes revealed by this study suggests that ultra-deep sequencing can improve understanding of deep-sea benthic diversity considered until now as unknowable based on a traditional taxonomic approach.