Trenches apart, yet worm to worm: inter- and intra-trench comparisons reveal divergent and convergent dynamics in hadal nematode biodiversity

Abstract

The hadal zone, the deepest part of the global ocean, encompasses several extreme ecosystems with elevated biological activity, contrasting the general trend of declining biomass and biodiversity with increasing water depth. These bathymetrically isolated habitats act as depocenters and are characterized by high hydrostatic pressure and unique environmental conditions that provide an opportunity to fundamentally explore biogeographic patterns and the genetic diversity of deep-sea meiofauna, which remain poorly understood. In this study, we compared nematode communities in two geographically distant trench systems, the Aleutian Trench (North Pacific) and the South Sandwich Trench (South Atlantic), separated by 17 000 km. Environmental DNA (eDNA) sequencing targeting the ribosomal 18S region was combined with a metaphylogeography approach. Comparative analyses were performed for intra- and inter-trench, biodiversity and genetic differentiation across environmentally characterised trench-specific habitats. Our findings reveal evidence for the meiofauna paradox in hadal settings, demonstrating distinct nematode communities that appear to be shaped by availability and quality of food. Furthermore, environmental filtering appeared to contribute to assembly of habitat specific communities according to localised environmental condition. Finally, we observed shared haplotypes among some dominating nematode genera, suggesting potential connectivity between habitats associated within or even across hadal trenches might exist. Overall, this study provides valuable insights on how environmental factors drive nematode biodiversity and genetic diversity in the hadal realm. Environmental heterogeneity plays a pivotal role in shaping nematode communities, influencing their population structure and connectivity by creating spatially variable habitats that drive diversification, local adaptation, and gene flow patterns.