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Concept: Mariana Trench

228

The past was a world of giants, with abundant whales in the sea and large animals roaming the land. However, that world came to an end following massive late-Quaternary megafauna extinctions on land and widespread population reductions in great whale populations over the past few centuries. These losses are likely to have had important consequences for broad-scale nutrient cycling, because recent literature suggests that large animals disproportionately drive nutrient movement. We estimate that the capacity of animals to move nutrients away from concentration patches has decreased to about 8% of the preextinction value on land and about 5% of historic values in oceans. For phosphorus (P), a key nutrient, upward movement in the ocean by marine mammals is about 23% of its former capacity (previously about 340 million kg of P per year). Movements by seabirds and anadromous fish provide important transfer of nutrients from the sea to land, totalling ∼150 million kg of P per year globally in the past, a transfer that has declined to less than 4% of this value as a result of the decimation of seabird colonies and anadromous fish populations. We propose that in the past, marine mammals, seabirds, anadromous fish, and terrestrial animals likely formed an interlinked system recycling nutrients from the ocean depths to the continental interiors, with marine mammals moving nutrients from the deep sea to surface waters, seabirds and anadromous fish moving nutrients from the ocean to land, and large animals moving nutrients away from hotspots into the continental interior.

Concepts: Plant, Fish, Ecology, Oceanography, Ocean, Mariana Trench, Whale, Forage fish

36

The deep ocean, covering a vast expanse of the globe, relies almost exclusively on a food supply originating from primary production in surface waters. With well-documented warming of oceanic surface waters and conflicting reports of increasing and decreasing primary production trends, questions persist about how such changes impact deep ocean communities. A 24-y time-series study of sinking particulate organic carbon (food) supply and its utilization by the benthic community was conducted in the abyssal northeast Pacific (∼4,000-m depth). Here we show that previous findings of food deficits are now punctuated by large episodic surpluses of particulate organic carbon reaching the sea floor, which meet utilization. Changing surface ocean conditions are translated to the deep ocean, where decadal peaks in supply, remineralization, and sequestration of organic carbon have broad implications for global carbon budget projections.

Concepts: United States, Oceanography, Pacific Ocean, Ocean, Mariana Trench, Carbon cycle, Deep sea, Abyssal zone

20

Sediments in deep ocean trenches may contain crucial information on past earthquake history and constitute important sites of carbon burial. Here we present 14C data on bulk organic carbon (OC) and its thermal decomposition fractions produced by ramped pyrolysis/oxidation for a core retrieved from the >7.5 km-deep Japan Trench. High-resolution 14C measurements, coupled with distinctive thermogram characteristics of OC, reveal hemipelagic sedimentation interrupted by episodic deposition of pre-aged OC in the trench. Low δ13C values and diverse 14C ages of thermal fractions imply that the latter material originates from the adjacent margin, and the co-occurrence of pre-aged OC with intervals corresponding to known earthquake events implies tectonically triggered, gravity-flow-driven supply. We show that 14C ages of thermal fractions can yield valuable chronological constraints on sedimentary sequences. Our findings shed new light on links between tectonically driven sedimentological processes and marine carbon cycling, with implications for carbon dynamics in hadal environments.

Concepts: Sediment, Sedimentary rock, Carbon, Ocean, Mariana Trench, Deep sea, Oceanic trench, Hadal zone

19

The Challenger Deep in the Mariana Trench is the deepest point in the ocean (10,994 m). Certain deep-sea animals can withstand the extreme pressure at this great depth. The amphipod Hirondellea gigas is a resident of the Challenger Deep. Amphipods are common inhabitants at great depths and serve as scavengers. However, there is relatively little information available regarding the physiology of H. gigas or this organism’s ecological interactions in the hadopelagic zone. To understand the feeding behavior of this scavenger in the deepest oligotrophic hadal zone, we analyzed the digestive enzymes in whole-body extracts. We describe the detection of amylase, cellulase, mannanase, xylanase, and α-glycosidase activities that are capable of digesting plant-derived polysaccharides. Our identification of glucose, maltose, and cellobiose in the H. gigas extracts indicated that these enzymes function under great pressure in situ. In fact, the glucose content of H. gigas averaged 0.4% (w/dry-w). The purified H. gigas cellulase (HGcel) converted cellulose to glucose and cellobiose at an exceptional molar ratio of 2:1 and efficiently produced glucose from dried wood, a natural cellulosic biomass, at 35 °C. The enzyme activity increased under a high hydrostatic pressure of 100 MPa at 2 °C, conditions equivalent to those found in the Challenger Deep. An analysis of the amino acid sequence of HGcel supported its classification as a family 31 glycosyl hydrolase. However, none of the enzymes of this family had previously been shown to possess cellulase activity. These results strongly suggested that H. gigas adapted to its extreme oligotrophic hadal oceanic environment by evolving digestive enzymes capable of digesting sunken wooden debris.

Concepts: Protein, Enzyme, Starch, Cellulose, Ocean, Mariana Trench, Deep sea, Challenger Deep

14

Hadal oceans at water depths below 6,000 m are the least-explored aquatic biosphere. The Challenger Deep, located in the western equatorial Pacific, with a water depth of ∼11 km, is the deepest ocean on Earth. Microbial communities associated with waters from the sea surface to the trench bottom (0 ∼10,257 m) in the Challenger Deep were analyzed, and unprecedented trench microbial communities were identified in the hadal waters (6,000 ∼10,257 m) that were distinct from the abyssal microbial communities. The potentially chemolithotrophic populations were less abundant in the hadal water than those in the upper abyssal waters. The emerging members of chemolithotrophic nitrifiers in the hadal water that likely adapt to the higher flux of electron donors were also different from those in the abyssal waters that adapt to the lower flux of electron donors. Species-level niche separation in most of the dominant taxa was also found between the hadal and abyssal microbial communities. Considering the geomorphology and the isolated hydrotopographical nature of the Mariana Trench, we hypothesized that the distinct hadal microbial ecosystem was driven by the endogenous recycling of organic matter in the hadal waters associated with the trench geomorphology.

Concepts: Water, Earth, Pacific Ocean, Ocean, Mariana Trench, Deep sea, Challenger Deep, Nereus

9

Whale carcasses create remarkable habitats in the deep-sea by producing concentrated sources of organic matter for a food-deprived biota as well as places of evolutionary novelty and biodiversity. Although many of the faunal patterns on whale falls have already been described, the biogeography of these communities is still poorly known especially from basins other than the NE Pacific Ocean. The present work describes the community composition of the deepest natural whale carcass described to date found at 4204 m depth on Southwest Atlantic Ocean with manned submersible Shinkai 6500. This is the first record of a natural whale fall in the deep Atlantic Ocean. The skeleton belonged to an Antarctic Minke whale composed of only nine caudal vertebrae, whose degradation state suggests it was on the bottom for 5-10 years. The fauna consisted mainly of galatheid crabs, a new species of the snail Rubyspira and polychaete worms, including a new Osedax species. Most of the 41 species found in the carcass are new to science, with several genera shared with NE Pacific whale falls and vent and seep ecosystems. This similarity suggests the whale-fall fauna is widespread and has dispersed in a stepping stone fashion, deeply influencing its evolutionary history.

Concepts: United States, Atlantic Ocean, Pacific Ocean, Ocean, Antarctica, Mariana Trench, Equator, Southern Ocean

8

Recent modeling studies have proposed different scenarios to explain the slowdown in surface temperature in the most recent decade. Some of these studies seem to support the idea of internal variability and/or rearrangement of heat between the surface and the ocean interior. Others suggest that radiative forcing might also play a role. Our examination of observational data over the past two decades shows some significant differences compared to model results from reanalyses, and provides the most definitive explanation of how the heat was redistributed. We find that cooling in the top 100-meter layer of the Pacific Ocean was mainly compensated by warming in the 100- to 300-meter layer of the Indian and Pacific Oceans in the past decade since 2003.

Concepts: Fish, Atlantic Ocean, Indian Ocean, Pacific Ocean, Ocean, Mariana Trench, World Ocean, Oceans

7

The deep sea is a massive, largely oligotrophic ecosystem, stretched over nearly 65% of the planet’s surface. Deep-sea planktonic communities are almost completely dependent upon organic carbon sinking from the productive surface, forming a vital component of global biogeochemical cycles. However, despite their importance, viruses from the deep ocean remain largely unknown. Here, we describe the first complete genomes of deep-sea viruses assembled from metagenomic fosmid libraries. “Candidatus Pelagibacter” (SAR11) phage HTVC010P and Puniceispirillum phage HMO-2011 are considered the most abundant cultured marine viruses known to date. Remarkably, some of the viruses described here recruited as many reads from deep waters as these viruses do in the photic zone, and, considering the gigantic scale of the bathypelagic habitat, these genomes provide information about what could be some of the most abundant viruses in the world at large. Their role in the viral shunt in the global ocean could be very significant. Despite the challenges encountered in inferring the identity of their hosts, we identified one virus predicted to infect members of the globally distributed SAR11 cluster. We also identified a number of putative proviruses from diverse taxa, including deltaproteobacteria, bacteroidetes, SAR11, and gammaproteobacteria. Moreover, our findings also indicate that lysogeny is the preferred mode of existence for deep-sea viruses inhabiting an energy-limited environment, in sharp contrast to the predominantly lytic lifestyle of their photic-zone counterparts. Some of the viruses show a widespread distribution, supporting the tenet “everything is everywhere” for the deep-ocean virome.

Concepts: Bacteria, Microbiology, Virus, Oceanography, Ocean, Mariana Trench, Deep sea, Bathyal zone

4

Microplastics are small plastic particles (<1 mm) originating from the degradation of larger plastic debris. These microplastics have been accumulating in the marine environment for decades and have been detected throughout the water column and in sublittoral and beach sediments worldwide. However, up to now, it has never been established whether microplastic presence in sediments is limited to accumulation hot spots such as the continental shelf, or whether they are also present in deep-sea sediments. Here we show, for the first time ever, that microplastics have indeed reached the most remote of marine environments: the deep sea. We found plastic particles sized in the micrometre range in deep-sea sediments collected at four locations representing different deep-sea habitats ranging in depth from 1100 to 5000 m. Our results demonstrate that microplastic pollution has spread throughout the world's seas and oceans, into the remote and largely unknown deep sea.

Concepts: Oceanography, Atlantic Ocean, Sea, Ocean, Mariana Trench, Marine debris, Seven Seas, Deep sea

3

Wood falls on the deep-sea floor represent a significant source of energy into the food-limited deep sea. Unique communities of primarily wood- and sulfide-obligate species form on these wood falls. However, little is known regarding patterns and drivers of variation in the composition of wood fall communities through space and time, and thus, how wood falls contribute to deep-sea biodiversity. Eighteen Acacia logs varying in size were placed and retrieved after five years at a 3200 m site in the Pacific Ocean. We found that the taxonomic composition and structure of deep-sea wood fall communities varied considerably and equated with considerable differences in energy usage and availability. Our findings suggest that natural variability in wood falls may contribute significantly to deep-sea diversity.

Concepts: Earth, Atlantic Ocean, Space, Pacific Ocean, Australia, Ocean, Mariana Trench, Deep sea