Blue light promotes zero-valent sulfur production in a deep-sea bacterium.

Increasing evidence has shown that light exists in a diverse range of deep-sea environments. We unexpectedly found that blue light is necessary to produce excess zero-valent sulfur (ZVS) in Erythrobacter flavus 21-3, a bacterium that has been recently isolated from a deep-sea cold seep. E. flavus 21-3 is able to convert thiosulfate to ZVS using a novel thiosulfate oxidation pathway comprising a thiosulfate dehydrogenase (TsdA) and a thiosulfohydrolase (SoxB). Using proteomic, bacterial two-hybrid and heterologous expression assays, we found that the light-oxygen-voltage histidine kinase LOV-1477 responds to blue light and activates the diguanylate cyclase DGC-2902 to produce c-di-GMP. Subsequently, the PilZ domain-containing protein mPilZ-1753 binds to c-di-GMP and activates TsdA through direct interaction. Finally, Raman spectroscopy and gene knockout results verified that TsdA and two SoxB homologs cooperate to regulate ZVS production. As ZVS is an energy source for E. flavus 21-3, we propose that deep-sea blue light provides E. flavus 21-3 with a selective advantage in the cold seep, suggesting a previously unappreciated relationship between light-sensing pathways and sulfur metabolism in a deep-sea microorganism.

The earliest evidence of deep-sea vertebrates.

Vertebrate macroevolution has been punctuated by fundamental habitat transitions from shallow marine origins to terrestrial, freshwater, and aerial environments. Invasion of the deep sea is a less well-known ecological shift because of low fossilization potential and continual loss of abyssal fossil record by ocean floor subduction. Therefore, there has been a lack of convincing evidence of bottom-living vertebrates from pre-Paleogene deep seas. Here, we describe trace fossils from abyssal plain turbidites of the Tethys Ocean, which, combined with nannofossil dating, indicate that fishes have occupied the deep seafloor since at least the Early Cretaceous (Hauterivian-Barremian). These structures are identical to those produced by modern demersal fishes that feed by either scratching the substrate or expose their prey by water flow generated by suction or jetting. The trace fossils suggest activity of at least three fish species exploiting a productive abyssal invertebrate sediment fauna. These observations are consistent with Early Cretaceous vertebrate transition to the deep sea triggered by the availability of new food sources. Our results anticipate the appearance of deep-seafloor fishes in the fossil record by over 80 My while reassessing the mode of vertebrate colonization of the deep sea.

Coastal upwelling drives ecosystem temporal variability from the surface to the abyssal seafloor.

Long-term biological time series that monitor ecosystems across the ocean's full water column are extremely rare. As a result, classic paradigms are yet to be tested. One such paradigm is that variations in coastal upwelling drive changes in marine ecosystems throughout the water column. We examine this hypothesis by using data from three multidecadal time series spanning surface (0 m), midwater (200 to 1,000 m), and benthic (~4,000 m) habitats in the central California Current Upwelling System. Data include microscopic counts of surface plankton, video quantification of midwater animals, and imaging of benthic seafloor invertebrates. Taxon-specific plankton biomass and midwater and benthic animal densities were separately analyzed with principal component analysis. Within each community, the first mode of variability corresponds to most taxa increasing and decreasing over time, capturing seasonal surface blooms and lower-frequency midwater and benthic variability. When compared to local wind-driven upwelling variability, each community correlates to changes in upwelling damped over distinct timescales. This suggests that periods of high upwelling favor increase in organism biomass or density from the surface ocean through the midwater down to the abyssal seafloor. These connections most likely occur directly via changes in primary production and vertical carbon flux, and to a lesser extent indirectly via other oceanic changes. The timescales over which species respond to upwelling are taxon-specific and are likely linked to the longevity of phytoplankton blooms (surface) and of animal life (midwater and benthos), which dictate how long upwelling-driven changes persist within each community.

Alternating regimes of shallow and deep-sea diversification explain a species-richness paradox in marine fishes.

The deep sea contains a surprising diversity of life, including iconic fish groups such as anglerfishes and lanternfishes. Still, >65% of marine teleost fish species are restricted to the photic zone <200 m, which comprises less than 10% of the ocean's total volume. From a macroevolutionary perspective, this paradox may be explained by three hypotheses: 1) shallow water lineages have had more time to diversify than deep-sea lineages, 2) shallow water lineages have faster rates of speciation than deep-sea lineages, or 3) shallow-to-deep sea transition rates limit deep-sea richness. Here we use phylogenetic comparative methods to test among these three non-mutually exclusive hypotheses. While we found support for all hypotheses, the disparity in species richness is better described as the uneven outcome of alternating phases that favored shallow or deep diversification over the past 200 million y. Shallow marine teleosts became incredibly diverse 100 million y ago during a period of warm temperatures and high sea level, suggesting the importance of reefs and epicontinental settings. Conversely, deep-sea colonization and speciation was favored during brief episodes when cooling temperatures increased the efficiency of the ocean's carbon pump. Finally, time-variable ecological filters limited shallow-to-deep colonization for much of teleost history, which helped maintain higher shallow richness. A pelagic lifestyle and large jaws were associated with early deep-sea colonists, while a demersal lifestyle and a tapered body plan were typical of later colonists. Therefore, we also suggest that some hallmark characteristics of deep-sea fishes evolved prior to colonizing the deep sea.

Deep-Pelagic Fishes Are Anything But Similar: A Global Synthesis.

Deep-pelagic fishes are among the most abundant vertebrates on Earth. They play a critical role in sequestering carbon, providing prey for harvestable fishing stocks and linking oceanic layers and trophic levels. However, knowledge of these fishes is scarce and fragmented, hampering the ability of both the scientific community and stakeholders to address them effectively. While modelling approaches incorporating these organisms have advanced, they often oversimplify their functional and ecological diversity, potentially leading to misconceptions. To address these gaps, this synthesis examines the biodiversity and ecology of global deep-pelagic fishes. We review pelagic ecosystem classifications and propose a new semantic framework for deep-pelagic fishes. We evaluate different sampling methods, detailing their strengths, limitations and complementarities. We provide an assessment of the world's deep-pelagic fishes comprising 1554 species, highlighting major groups and discussing regional variability. By describing their morphological, behavioural and ecological diversity, we show that these organisms are far from homogeneous. Building on this, we call for a more realistic approach to the ecology of deep-pelagic fishes transitioning between very different ecological niches during diel vertical migrations. To facilitate this, we introduce the concept of 'diel-modulated realised niche' and propose a conceptual model synthesising the multiple drivers responsible for such transitions.

Third-Generation Sequencing Reveals the Adaptive Role of the Epigenome in Three Deep-Sea Polychaetes.

The roles of DNA methylation in invertebrates are poorly characterized, and critical data are missing for the phylum Annelida. We fill this knowledge gap by conducting the first genome-wide survey of DNA methylation in the deep-sea polychaetes dominant in deep-sea vents and seeps: Paraescarpia echinospica, Ridgeia piscesae, and Paralvinella palmiformis. DNA methylation calls were inferred from Oxford Nanopore sequencing after assembling high-quality genomes of these animals. The genomes of these worms encode all the key enzymes of the DNA methylation metabolism and possess a mosaic methylome similar to that of other invertebrates. Transcriptomic data of these polychaetes support the hypotheses that gene body methylation strengthens the expression of housekeeping genes and that promoter methylation acts as a silencing mechanism but not the hypothesis that DNA methylation suppresses the activity of transposable elements. The conserved epigenetic profiles of genes responsible for maintaining homeostasis under extreme hydrostatic pressure suggest DNA methylation plays an important adaptive role in these worms.

Diversity and structure of the deep-sea sponge microbiome in the equatorial Atlantic Ocean.

Sponges (phylum Porifera) harbour specific microbial communities that drive the ecology and evolution of the host. Understanding the structure and dynamics of these communities is emerging as a primary focus in marine microbial ecology research. Much of the work to date has focused on sponges from warm and shallow coastal waters, while sponges from the deep ocean remain less well studied. Here, we present a metataxonomic analysis of the microbial consortia associated with 23 individual deep-sea sponges. We identify a high abundance of archaea relative to bacteria across these communities, with certain sponge microbiomes comprising more than 90 % archaea. Specifically, the archaeal family Nitrosopumilaceae is prolific, comprising over 99 % of all archaeal reads. Our analysis revealed that sponge microbial communities reflect the host sponge phylogeny, indicating a key role for host taxonomy in defining microbiome composition. Our work confirms the contribution of both evolutionary and environmental processes to the composition of microbial communities in deep-sea sponges.

Evolution of bioluminescence in Anthozoa with emphasis on Octocorallia.

Bioluminescence is a widespread phenomenon that has evolved multiple times across the tree of life, converging among diverse fauna and habitat types. The ubiquity of bioluminescence, particularly in marine environments where it is commonly used for communication and defense, highlights the adaptive value of this trait, though the evolutionary origins and timing of emergence remain elusive for a majority of luminous organisms. Anthozoan cnidarians are a diverse group of animals with numerous bioluminescent species found throughout the world's oceans, from shallow waters to the light-limited deep sea where bioluminescence is particularly prominent. This study documents the presence of bioluminescent Anthozoa across depth and explores the diversity and evolutionary origins of bioluminescence among Octocorallia-a major anthozoan group of marine luminous organisms. Using a phylogenomic approach and ancestral state reconstruction, we provide evidence for a single origin of bioluminescence in Octocorallia and infer the age of occurrence to around the Cambrian era, approximately 540 Ma-setting a new record for the earliest timing of emergence of bioluminescence in the marine environment. Our results further suggest this trait was largely maintained in descendants of a deep-water ancestor and bioluminescent capabilities may have facilitated anthozoan diversification in the deep sea.

A deep-sea isopod that consumes Sargassum sinking from the ocean's surface.

Most deep-ocean life relies on organic carbon from the surface ocean. While settling primary production rapidly attenuates in the water column, pulses of organic material can be quickly transported to depth in the form of food falls. One example of fresh material that can reach great depths across the tropical Atlantic Ocean and Caribbean Sea is the pelagic macroalgae Sargassum. However, little is known about the deep-ocean organisms able to use this food source. Here, we encountered the isopod Bathyopsurus nybelini at depths 5002-6288 m in the Puerto Rico Trench and Mid-Cayman Spreading Center using the Deep Submergence Vehicle Alvin. In most of the 32 observations, the isopods carried fronds of Sargassum. Through an integrative suite of morphological, DNA sequencing, and microbiological approaches, we show that this species is adapted to feed on Sargassum by using a specialized swimming stroke, having serrated and grinding mouthparts, and containing a gut microbiome that provides a dietary contribution through the degradation of macroalgal polysaccharides and fixing nitrogen. The isopod's physiological, morphological, and ecological adaptations demonstrate that vertical deposition of Sargassum is a direct trophic link between the surface and deep ocean and that some deep-sea organisms are poised to use this material.

Genetic divergence and migration patterns of a galatheoid squat lobster highlight the need for deep-sea conservation.

Information on genetic divergence and migration patterns of vent- and seep-endemic macrobenthos can help delimit biogeographical provinces and provide scientific guidelines for deep-sea conservation under the growing threats of anthropogenic disturbances. Nevertheless, related studies are still scarce, impeding the informed conservation of these hotspots of deep-sea biodiversity. To bridge this knowledge gap, we conducted a population connectivity study on the galatheoid squat lobster Shinkaia crosnieri - a deep-sea foundation species widely distributed in vent and seep ecosystems in the Northwest Pacific. With the application of an interdisciplinary methodology involving population genomics and oceanographic approaches, we unveiled two semi-isolated lineages of S. crosnieri with limited and asymmetrical gene flow potentially shaped by the geographic settings, habitat types, and ocean currents - one comprising vent populations in the Okinawa Trough, with those inhabiting the southern trough area likely serving as the source; the other being the Jiaolong (JR) seep population in the South China Sea. The latter might have recently experienced a pronounced demographic contraction and exhibited genetic introgression from the Okinawa Trough lineage, potentially mediated by the intrusion of the North Pacific Intermediate Water. We then compared the biogeographic patterns between S. crosnieri and two other representative and co-occurring vent- and seep-endemic species using published data. Based on their biogeographical subdivisions and source-sink dynamics, we highlighted the southern Okinawa Trough vents and the JR seep warrant imperative conservation efforts to sustain the deep-sea biodiversity in the Northwest Pacific.