High genetic diversity in the pelagic deep-sea fauna of the Atacama Trench revealed by environmental DNA

Abstract

A current paradigm in marine biodiversity states that faunal richness decreases with depth. However, the deep-ocean ecosystem has been significantly under-sampled, hindering a complete view of its biodiversity. This situation is accentuated in ultra-deep waters, where the remote and extreme conditions unfit the traditional sampling methods. Using environmental DNA, we assessed the pelagic metazoan diversity of the Atacama Trench from the high-productive near-surface level down to ~8000 m depth. Our results show that waters deeper than 4000 m contributed up to 50% of the overall genetic diversity. These findings contrast with similar observations in the less-productive Kermadec Trench, where the diversity in deep waters was lower than in shallower waters. Moreover, both deep pelagic ecosystems exhibited some unknown phylogenetic clades within the dominant taxonomic groups: hydrozoans and copepods. The deep-ocean biota may thus contribute to global biodiversity far more than hitherto suggested, especially in zones influenced by high primary production. Our results underline the need for increased effort study these remote ecosystems and improve our understanding of their contribution to the ecology and biogeochemistry of the deep-sea pelagic and benthic realms.

Revealing zooplankton diversity in the midnight zone

“…The relative abundance of species observed in this study were consistent with previous research conducted using morphological and genetic approaches, extending down to the abyssopelagic zone (Kosobokova and Hirche, 2000;Vereshchaka et al, 2017;de Puelles et al, 2019;Ramıŕez-Flandes et al, 2022). In the study region off northern Chile, Calanoida and Euphausiacea dominated the zooplankton communities (Heinrich, 1973;Escribano and Hidalgo, 2000;Antezana, 2002), with Subeucalanus monachus and Euphausia mucronata adapting to hypoxic conditions in the upper 500 m (Binet, 1983;Antezana, 2002;Valdeś et al, 2007).…”

“…However, both studies reached maximum depths of 1500 m and 3000 m, respectively. In our study region, analysis of environmental DNA targeting the whole metazoan community suggested a gradual increase in diversity with depth down to 8000 m (Ramıŕez-Flandes et al, 2022), although this pattern was uncertain for the zooplankton group.…”

“…This might be due to environmental preferences, local adaptations, and even lineage evolution (if anything, over evolutionary scales), which may influence the shape of the diversity profiles for each group (Somero, 1992;Seibel and Drazen, 2007;Van der Spoel and Heyman, 2013). For example, Calanoida and Siphonophorae show higher diversity in the intermediate layers (1000-2000 m) (Yamaguchi et al, 2015;Hirai et al, 2021;Ramıŕez-Flandes et al, 2022), which is possibly associated with intense predatory-driven coevolution (Mackie et al, 1988;Robison, 2004). In contrast, other Eucarida, Euphausiacea, and Halocyprida exhibit higher diversity in the upper layer, possibly due to better adaptation to primary productivity in the photic zone and a close relationship with the shallow oxygen minimum zone (OMZ) typical of this region (Antezana, 2002;Mujica et al, 2022).…”

“…Previous studies have proposed a parabolic vertical pattern of diversity, with the maximum observed at depths between 1000 and 2000 m (Vinogradov, 1970;Angel and Fasham, 1975;Angel, 1979;Lindsay and Hunt, 2005;Yamaguchi et al, 2015). However, this pattern has been described based on specific taxonomic groups, mainly within the same genus or family, and on communities from the top 3000 m. Consequently, the general vertical pattern of zooplankton diversity from the surface to the ultra-deep zone (>3000 m) remains poorly known (Angel et al, 1982;Ramıŕez-Flandes et al, 2022). In benthic metazoans, where more studies have been conducted below 3000 m, a parabolic pattern of diversity with depth has also been observed.…”

“…Although these groups comprise the majority of zooplankton and are characterized by high levels of phylogenetic and taxonomic diversity, there are a total of 15 phyla and 41 functional groups (Bucklin et al, 2021). As in most regions, copepods dominate, constituting as much as 80% of the community in the upper 1000 m, but other groups, such as euphausiids, ostracods, and siphonophores, may also be abundant in the deep ocean (Steinberg et al, 2008;Ramıŕez-Flandes et al, 2022). Among the pelagic components, zooplankton are an ecologically sensitive and adaptable group that responds rapidly to environmental variation (Richardson and Schoeman, 2004).…”