The eyes of deep-sea fishes and the changing nature of visual scenes with depth

The visual scenes viewed by ocean animals change dramatically with depth. In the brighter epipelagic depths, daylight provides an extended field of illumination. In mesopelagic depths down to 1000 m the visual scene is semi-extended, with the downwelling daylight providing increasingly dim extended illumination with depth. In contrast, greater depths increase the prominence of point-source bioluminescent flashes. In bathypelagic depths (below 1000 m daylight no longer penetrates, and the visual scene consists exclusively of point-source bioluminescent flashes. In this paper, I show that the eyes of fishes match this change from extended to point-source illumination, becoming increasingly foveate and spatially acute with increasing depth. A sharp fovea is optimal for localizing point sources. Quite contrary to their reputation as 'degenerate' and 'regressed', I show here that the remarkably prominent foveae and relatively large pupils of bathypelagic fishes give them excellent perception and localization of bioluminescent flashes up to a few tens of metres distant. In a world with almost no food, where fishes are weak and must swim very slowly this range of detection (and interception) is energetically realistic, with distances greater than this physically beyond range. Larger and more sensitive eyes would give bathypelagic fishes little more than the useless ability to see flashes beyond reach.     

Vision in the dimmest habitats on Earth

A very large proportion of the world's animal species are active in dim light, either under the cover of night or in the depths of the sea. The worlds they see can be dim and extended, with light reaching the eyes from all directions at once, or they can be composed of bright point sources, like the multitudes of stars seen in a clear night sky or the rare sparks of bioluminescence that are visible in the deep sea. The eye designs of nocturnal and deep-sea animals have evolved in response to these two very different types of habitats, being optimised for maximum sensitivity to extended scenes, or to point sources, or to both. After describing the many visual adaptations that have evolved across the animal kingdom for maximising sensitivity to extended and point-source scenes, I then use case studies from the recent literature to show how these adaptations have endowed nocturnal animals with excellent vision. Nocturnal animals can see colour and negotiate dimly illuminated obstacles during flight. They can also navigate using learned terrestrial landmarks, the constellations of stars or the dim pattern of polarised light formed around the moon. The conclusion from these studies is clear: nocturnal habitats are just as rich in visual details as diurnal habitats are, and nocturnal animals have evolved visual systems capable of exploiting them. The same is certainly true of deep-sea animals, as future research will no doubt reveal.     

深远海浮游动物生态学研究进展

深远海浮游生态系统依据水深的差别可以被划分为几个子系统,包括上层、中层、深层和深渊层等。目前大量的研究结果表明在海洋上层,由于光照、温度、海冰和营养盐补充等因素的影响,浮游生物群落往往呈现出显著的时空变化。但在海洋中层及更深的区域,传统观点认为随着水深的增加,海洋的理化环境趋向于稳定,在这一区域生态系统的时空变化要弱于海洋上层。同时受调查技术和经费的限制,人们对于这一广阔区域内浮游生态系统时空变化规律的认识要局限的多。随着我国海洋科学的发展和海洋强国战略的实施,海洋科学研究也逐渐由过去的以近海研究为主发展到当前的近海、边缘海和深远海研究协同发展。但与我国近海浮游生态学过去数十年间积累的大量研究成果相比,我国科学家对深远海,特别是中层、深层和深渊层浮游生态学方面的研究极为缺乏。从大洋浮游动物群落的垂直分布及其变化、种间关系与生态位分化、深海浮游动物群落在碳沉降和生物地球化学循环中的作用等多个角度全面总结了当前国内外深海浮游生态学的研究进展,同时介绍过去十余年来深海浮游生态学研究技术手段上的巨大进步,以期为今后国内同行的研究提供参考和借鉴。     

Long-wave sensitivity in deep-sea stomiid dragonfish with far-red bioluminescence: evidence for a dietary origin of the chlorophyll-derived retinal photosensitizer of Malacosteus niger

Both residual downwelling sunlight and bioluminescence, which are the two main sources of illumination available in the deep sea, have limited wavebands concentrated around 450-500 nm. Consequently, the wavelengths of maximum absorption (lambdamax) of the vast majority of deep-sea fish visual pigments also cluster in this part of the spectrum. Three genera of deep-sea loose-jawed dragonfish (Aristostomias, Pachystomias and Malacosteus), however, in addition to the blue bioluminescence typical of most deep-sea animals, also produce far-red light (maximum emission >700 nm) from suborbital photophores. All three genera are sensitive in this part of the spectrum, to which all other animals of the deep sea are blind, potentially affording them a private waveband for illuminating prey and for interspecific communication that is immune from detection by predators and prey. Aristostomias and Pachystomias enhance their long-wave visual sensitivity by the possession of at least three visual pigments that are long-wave shifted (lambdamax values ca. 515, 550 and 590 nm) compared with those of other deep-sea fishes. Malacosteus, on the other hand, although it does possess two of these red-shifted pigments (lambdamax values ca. 520 and 540 nm), lacks the most long-wave-sensitive pigments found in the other two genera. However, it further enhances its long-wave sensitivity with a chlorophyll-derived photosensitizer within its outer segments. The fluorescence emission and excitation spectra of this pigment are very similar to spectra obtained from mesopelagic copepods, which are an important component of diet of Malacosteus, suggesting a dietary origin for this pigment.     

Optical parameters of euphausiid eyes as a function of habitat depth

Summary The relationships between habitat depth, eye diameter relative to body length, and the dimensions of rhabdoms and crystalline cones have been examined for 13 species of three oceanic euphausiid genera with habitats ranging from near-surface waters to the deep-sea. Rate of eye growth decreases with depth. Longer rhabdoms may increase the visual sensitivity to point and extended light sources by an eye of a particular size with depth. Larger interommatidial angles suggest that visual acuity decreases at depth. Depth-related changes in euphausiid eyes are considered with respect to the probable roles of vision and bioluminescence in the deep-sea. Unusual features of the eyes of several species are described.     

Major imprint of surface plankton on deep ocean prokaryotic structure and activity

Deep ocean microbial communities rely on the organic carbon produced in the sunlit ocean, yet it remains unknown whether surface processes determine the assembly and function of bathypelagic prokaryotes to a larger extent than deep‐sea physicochemical conditions. Here, we explored whether variations in surface phytoplankton assemblages across Atlantic, Pacific and Indian ocean stations can explain structural changes in bathypelagic (ca. 4,000 m) free‐living and particle‐attached prokaryotic communities (characterized through 16S rRNA gene sequencing), as well as changes in prokaryotic activity and dissolved organic matter (DOM) quality. We show that the spatial structuring of prokaryotic communities in the bathypelagic strongly followed variations in the abundances of surface dinoflagellates and ciliates, as well as gradients in surface primary productivity, but were less influenced by bathypelagic physicochemical conditions. Amino acid‐like DOM components in the bathypelagic reflected variations of those components in surface waters, and seemed to control bathypelagic prokaryotic activity. The imprint of surface conditions was more evident in bathypelagic than in shallower mesopelagic (200–1,000 m) communities, suggesting a direct connectivity through fast‐sinking particles that escape mesopelagic transformations. Finally, we identified a pool of endemic deep‐sea prokaryotic taxa (including potentially chemoautotrophic groups) that appear less connected to surface processes than those bathypelagic taxa with a widespread vertical distribution. Our results suggest that surface planktonic communities shape the spatial structure of the bathypelagic microbiome to a larger extent than the local physicochemical environment, likely through determining the nature of the sinking particles and the associated prokaryotes reaching bathypelagic waters.     

Spectral sensitivity of vision and bioluminescence in the midwater shrimp Sergestes similis

In the oceanic midwater environment, many fish, squid, and shrimp use luminescent countershading to remain cryptic to silhouette-scanning predators. The mid-water penaeid shrimp, Sergestes similis Hansen, responds to downward-directed light with a dim bioluminescence that dynamically matches the spectral radiance of oceanic down-welling light at depth. Although the sensory basis of luminescent countershading behavior is visual, the relationship between visual and behavioral sensitivity is poorly understood. In this study, visual spectral sensitivity, based on microspectrophotometry and electrophysiological measurements of photoreceptor response, is directly compared to the behavioral spectral efficiency of luminescent countershading. Microspectrophotometric measurements on single photoreceptors revealed only a single visual pigment with peak absorbance at 495 nm in the blue-green region of the spectrum. The peak electrophysiological spectral sensitivity of dark-adapted eyes was centered at about 500 nm. The spectral efficiency of luminescent countershading showed a broad peak from 480 to 520 nm. Both electrophysiological and behavioral data closely matched the normalized spectral absorptance curve of a rhodopsin with lambda(max) = 495 nm, when rhabdom length and photopigment specific absorbance were considered. The close coupling between visual spectral sensitivity and the spectral efficiency of luminescent countershading attests to the importance of bioluminescence as a camouflage strategy in this species.     

Eye-Size Variability in Deep-Sea Lanternfishes (Myctophidae): An Ecological and Phylogenetic Study

One of the most common visual adaptations seen in the mesopelagic zone (200–1000 m), where the amount of light diminishes exponentially with depth and where bioluminescent organisms predominate, is the enlargement of the eye and pupil area. However, it remains unclear how eye size is influenced by depth, other environmental conditions and phylogeny. In this study, we determine the factors influencing variability in eye size and assess whether this variability is explained by ecological differences in habitat and lifestyle within a family of mesopelagic fishes characterized by broad intra- and interspecific variance in depth range and luminous patterns. We focus our study on the lanternfish family (Myctophidae) and hypothesise that lanternfishes with a deeper distribution and/or a reduction of bioluminescent emissions have smaller eyes and that ecological factors rather than phylogenetic relationships will drive the evolution of the visual system. Eye diameter and standard length were measured in 237 individuals from 61 species of lanternfishes representing all the recognised tribes within the family in addition to compiling an ecological dataset including depth distribution during night and day and the location and sexual dimorphism of luminous organs. Hypotheses were tested by investigating the relationship between the relative size of the eye (corrected for body size) and variations in depth and/or patterns of luminous-organs using phylogenetic comparative analyses. Results show a great variability in relative eye size within the Myctophidae at all taxonomic levels (from subfamily to genus), suggesting that this character may have evolved several times. However, variability in eye size within the family could not be explained by any of our ecological variables (bioluminescence and depth patterns), and appears to be driven solely by phylogenetic relationships.     

Visual perception of light organ patterns in deep‐sea shrimps and implications for conspecific recognition

Darkness and low biomass make it challenging for animals to find and identify one another in the deep sea. While spatiotemporal variation in bioluminescence is thought to underlie mate recognition for some species, its role in conspecific recognition remains unclear. The deep‐sea shrimp genus, Sergestes sensu lato (s.l.), is one group that is characterized by species‐specific variation in light organ arrangement, providing us the opportunity to test whether organ variation permits recognition to the species level. To test this, we analyzed the visual capabilities of three species of Sergestes s.l. in order to (a) test for sexual dimorphism in eye‐to‐body size scaling relationships, (b) model the visual ranges (i.e., sighting distances) over which these shrimps can detect intraspecific bioluminescence, and (c) assess the maximum possible spatial resolution of the eyes of these shrimps to estimate their capacity to distinguish the light organs of each species. Our results showed that relative eye size scaled negatively with body length across species and without sexual dimorphism. Though the three species appear capable of detecting one another's bioluminescence over distances ranging from < 1 to ~6 m, their limited spatial resolution suggests they cannot resolve light organ variation for the purpose of conspecific recognition. Our findings point to factors other than conspecific recognition (e.g., neutral drift, phenotypic constraint) that have led to the extensive diversification of light organs in Sergestes s.l and impart caution about interpreting ecological significance of visual characters based on the resolution of human vision. This work provides new insight into deep‐sea animal interaction, supporting the idea that—at least for these mesopelagic shrimps—nonvisual signals may be required for conspecific recognition.     

Vertical gradients in species richness and community composition across the twilight zone in the North Pacific Subtropical Gyre

Although metazoan animals in the mesopelagic zone play critical roles in deep pelagic food webs and in the attenuation of carbon in midwaters, the diversity of these assemblages is not fully known. A metabarcoding survey of mesozooplankton diversity across the epipelagic, mesopelagic and upper bathypelagic zones (0–1500 m) in the North Pacific Subtropical Gyre revealed far higher estimates of species richness than expected given prior morphology‐based studies in the region (4,024 OTUs, 10‐fold increase), despite conservative bioinformatic processing. Operational taxonomic unit (OTU) richness of the full assemblage peaked at lower epipelagic–upper mesopelagic depths (100–300 m), with slight shoaling of maximal richness at night due to diel vertical migration, in contrast to expectations of a deep mesopelagic diversity maximum as reported for several plankton groups in early systematic and zoogeographic studies. Four distinct depth‐stratified species assemblages were identified, with faunal transitions occurring at 100 m, 300 m and 500 m. Highest diversity occurred in the smallest zooplankton size fractions (0.2–0.5 mm), which had significantly lower % OTUs classified due to poor representation in reference databases, suggesting a deep reservoir of poorly understood diversity in the smallest metazoan animals. A diverse meroplankton assemblage also was detected (350 OTUs), including larvae of both shallow and deep living benthic species. Our results provide some of the first insights into the hidden diversity present in zooplankton assemblages in midwaters, and a molecular reappraisal of vertical gradients in species richness, depth distributions and community composition for the full zooplankton assemblage across the epipelagic, mesopelagic and upper bathypelagic zones.     

HOW DO SPERM WHALES CATCH SQUIDS?

Vision may play a central role in sperm whale predation. Two complementary hypotheses regarding the detection and capture of prey items are presented, based on a review of mesopelagic ecology. The first hypothesis postulates that sperm whales locate their prey visually, either silhouetted against the midwater "sky," or by searching for bioluminescence produced by the movements of their prey. The second hypothesis postulates that sperm whales create a zone of stimulated bioluminescence around the mouth, which attracts squids and other visual predators. Studies of midwater fishes and invertebrates document the importance of vision in mesopelagic communities. If sperm whales search for silhouetted prey, they should be oriented upside-down to improve visual coverage and to facilitate the transition from search to prey capture. Prey capture events should be marked by excursions toward the surface. If they lure their prey, they should swim at a steady pace, with little rapid acceleration, and spend most of their time foraging at depths with the greatest potential for stimulated bioluminescence.     

Evolution in the deep sea: Biological traits, ecology and phylogenetics of pelagic copepods

Deep-sea biodiversity has received increasing interest in the last decade, mainly focusing on benthic communities. In contrast, studies of zooplankton in the meso- to bathypelagic zones are relatively scarce. In order to explore evolutionary processes in the pelagic deep sea, the present study focuses on copepods of two clausocalanoid families, Euchaetidae and Aetideidae, which are abundant and species-rich in the deep-sea pelagic realm. Molecular phylogenies based on concatenated-portioned data on 18S, 28S and internal transcribed spacer 2 (ITS2), as well as mitochondrial cytochrome c oxidase subunit I (COI), were examined on 13 species, mainly from Arctic and Antarctic regions, together with species-specific biological traits (i.e. vertical occurrence, feeding behaviour, dietary preferences, energy storage, and reproductive strategy). Relationships were resolved on genus, species and even sub-species levels, the latter two established by COI with maximum average genetic distances ranging from ?5.3% at the intra-specific, and 20.6% at the inter-specific level. There is no resolution at a family level, emphasising the state of Euchaetidae and Aetideidae as sister families and suggesting a fast radiation of these lineages, a hypothesis which is further supported by biological parameters. Euchaetidae were similar in lipid-specific energy storage, reproductive strategy, as well as feeding behaviour and dietary preference. In contrast, Aetideidae were more diverse, comprising a variety of characteristics ranging from similar adaptations within Paraeuchaeta, to genera consisting of species with completely different reproductive and feeding ecologies. Reproductive strategies were generally similar within each aetideid genus, but differed between genera. Closely related species (congeners), which were similar in the aforementioned biological and ecological traits, generally occurred in different depth layers, suggesting that vertical partitioning of the water column represents an important mechanism in the speciation processes for these deep-sea copepods. High COI divergence between Arctic and Antarctic specimens of the mesopelagic cosmopolitan Gaetanus tenuispinus and the bipolar Aetideopsis minor suggest different geographic forms, potentially cryptic species or sibling species. On the contrary, Arctic and Antarctic individuals of the bathypelagic cosmopolitans Gaetanus brevispinus and Paraeuchaeta barbata were very similar in COI sequence, suggesting more gene flow at depth and/or that driving forces for speciation were less pronounced in bathypelagic than at mesopelagic depths.     

Deep-Sea Bioluminescence Blooms after Dense Water Formation at the Ocean Surface

The deep ocean is the largest and least known ecosystem on Earth. It hosts numerous pelagic organisms, most of which are able to emit light. Here we present a unique data set consisting of a 2.5-year long record of light emission by deep-sea pelagic organisms, measured from December 2007 to June 2010 at the ANTARES underwater neutrino telescope in the deep NW Mediterranean Sea, jointly with synchronous hydrological records. This is the longest continuous time-series of deep-sea bioluminescence ever recorded. Our record reveals several weeks long, seasonal bioluminescence blooms with light intensity up to two orders of magnitude higher than background values, which correlate to changes in the properties of deep waters. Such changes are triggered by the winter cooling and evaporation experienced by the upper ocean layer in the Gulf of Lion that leads to the formation and subsequent sinking of dense water through a process known as “open-sea convection”. It episodically renews the deep water of the study area and conveys fresh organic matter that fuels the deep ecosystems. Luminous bacteria most likely are the main contributors to the observed deep-sea bioluminescence blooms. Our observations demonstrate a consistent and rapid connection between deep open-sea convection and bathypelagic biological activity, as expressed by bioluminescence. In a setting where dense water formation events are likely to decline under global warming scenarios enhancing ocean stratification, in situ observatories become essential as environmental sentinels for the monitoring and understanding of deep-sea ecosystem shifts.     

First records of sea snakes (Elapidae: Hydrophiinae) diving to the mesopelagic zone (>200 m)

Viviparous sea snakes (Elapidae: Hydrophiinae) are fully marine reptiles distributed in the tropical and subtropical waters of the Indian and Pacific Oceans. Their known maximum diving depth ranges between 50 and 100 m and this is thought to limit their ecological ranges to shallow habitats. We report two observations, from industry‐owned remotely operated vehicles, of hydrophiine sea snakes swimming and foraging at depths of approximately 250 m in the Browse Basin on Australia's North West Shelf, in 2014 and 2017. These observations show that sea snakes are capable of diving to the dim‐lit, cold‐water mesopelagic zone, also known as the ‘twilight’ zone. These record‐setting dives raise new questions about the thermal tolerances, diving behaviour and ecological requirements of sea snakes. In addition to significantly extending previous diving records for sea snakes, these observations highlight the importance of university‐industry collaboration in surveying understudied deep‐sea habitats.     

Life in the unthinking depths: energetic constraints on encephalization in marine fishes

Several hypotheses have been proposed to explain the limitation of brain size in vertebrates. Here, we test three hypotheses of brain size evolution using marine teleost fishes: the direct metabolic constraints hypothesis (DMCH), the expensive tissue hypothesis and the temperature‐dependent hypothesis. Our analyses indicate that there is a robust positive correlation between encephalization and basal metabolic rate (BMR) that spans the full range of depths occupied by teleosts from the epipelagic (< 200 m), mesopelagic (200–1000 m) and bathypelagic (> 4000 m). Our results disentangle the effects of temperature and metabolic rate on teleost brain size evolution, supporting the DMCH. Our results agree with previous findings that teleost brain size decreases with depth; however, we also recover a negative correlation between trophic level and encephalization within the mesopelagic zone, a result that runs counter to the expectations of the expensive tissue hypothesis. We hypothesize that mesopelagic fishes at lower trophic levels may be investing more in neural tissue related to the detection of small prey items in a low‐light environment. We recommend that comparative encephalization studies control for BMR in addition to controlling for body size and phylogeny.     

Energetic and life-history patterns of deep-sea benthic, benthopelagic and seamount-associated fish

A review of energy use and the life histories of deep-water demersal fishes suggests that there are two primary groups or guilds; those that live dispersed over the sea floor and those that aggregate in association with topographic features like seamounts. Dispersed deep-sea fishes typically have a body plan designed for slow cruising or 'sit and wait' predation, and are characterized by very low energy stores and metabolic rates. Scaled for body size, the metabolism of these fishes was comparable to that of bathypelagic fishes. On the other hand, aggregatory deep-water species are characterized by robust morphology and strong locomotory ability to maintain themselves in environments characterized by strong, variable currents. Their flesh has high protein and lipid but low water content. The metabolic rate of orange roughy, an aggregating deep-water species, was substantially higher than that of dispersed deep-water fishes and was comparable to that of haddock, a shelf demersal species. However, although the estimated ration of orange roughy was higher than that of dispersed demersal deep-water species, its growth rate was comparable and its growth efficiency was far lower due to its high metabolic costs. Large deep-water dispersed fish species are characterized by late maturity and an extended reproductive period, but these characteristics are less pronounced than in deep seamount-associated species, which may live in excess of 100 years.     

Illuminating the evolution of bioluminescence in sharks

The evolutionary context in which shark bioluminescence originated is poorly understood, despite it being critical to uncovering influential factors in the evolutionary history and diversity of living chondrichthyans as well as the mechanisms of deep-water colonization by vertebrates. This study provides the first joint reconstruction of the habitats, lifestyles, and occurrence of bioluminescence in the evolution of squalomorph sharks using ancestral state estimation analysis to resolve the timing of deep-sea colonization, the evolutionary origin of bioluminescence and the ancestral ecologies of this group. The results suggest that most squalomorphs originated in neritic environments from where they colonized deep waters on several independent occasions during the Late Jurassic and Early Cretaceous, predating most of the previous estimates of the timing of this event. The colonization of the deep sea took place via the benthic zone, in contrast to the view that an intermediate mesopelagic stage occurred during this ecological transition. Finally, the analyses accounting for uncertainty of the presence of bioluminescence strongly support that this trait evolved only once among sharks in a bathydemersal ancestor. This study reveals that shark bioluminescence evolved in a complex scenario that combines elements of several previous proposals, and enriches our perspective on the sequence of events that characterized the vertebrate conquest of the deep sea.     

Distinct protistan assemblages characterize the euphotic zone and deep sea (2500 m) of the western North Atlantic (Sargasso Sea and Gulf Stream)

Protistan diversity was characterized at three locations in the western North Atlantic (Sargasso Sea and Gulf Stream) by sequencing 18S rRNA genes in samples from euphotic (< or = 125 m) and bathypelagic depths (2500 m). A total of 923 partial-length protistan sequences were analysed, revealing 324 distinct operational taxonomic units (OTUs) determined by an automated OTU-calling program set to 95% sequence similarity. Most OTUs were comprised of only one or two sequences suggesting a large but rare pool of protistan diversity. Many OTUs from both depth strata were associated with recently described novel alveolate and stramenopile lineages while many OTUs from the bathypelagic were affiliated with Acantharea, Polycystinea and Euglenozoa and were not observed in euphotic zone libraries. Protistan assemblages from the euphotic zone and the deep sea were largely composed of distinct OTUs; only 28 of the 324 protistan OTUs were detected in both shallow and deep sea clone libraries. The diversity of protistan assemblages in the deep sea was distinctly lower than the diversity of euphotic zone assemblages. Protistan assemblages from the Gulf Stream were the most diverse for either depth strata. Overall, protistan assemblages from different stations but comparable depths were more similar than the assemblages from different depths at the same station. These data suggest that particular groups of protistan OTUs formed distinct 'shallow' and 'deep-sea' assemblages across widely spaced oceanic locales.     

Ocular morphology in antarctic notothenioid fishes

Beneath the sea ice at McMurdo Sound, Antarctica, notothenioid fishes are subject to extreme seasonal variation in the annual light cycle including 4 months of continual darkness. Gross and microscopic anatomy of the eyes of 18 species revealed ocular morphology that was generally similar to that of coastal fishes elsewhere in the world, and unlike that of deep sea fishes living in perpetual darkness. The spectacle was well developed as were hyaloid arteries at the vitreoretinal interface. Fourteen species had a choroid body, and its presence was considered a primitive character state for notothenioids. The choroid body was absent in phyletically derived groups. The choroid body was especially large in Dissostichus mawsoni, the only species with a rod dominated retina. Retinae were 154–279 μm thick with layering and sublayering typical for teleosts. Although all species had both rods and cones, there was marked interspecific variation in the ratio of cones:rods and in the total number of visual cells. Non-Antarctic notothenioids from New Zealand had more visual cells than most species from McMurdo Sound. Retinae appeared balanced for vision under dim but seasonally variable light conditions and not specially adapted to the 4-month period of winter darkness. Retinal histology reflected the ecology and depth range of most species. Based on ecology and retinal histology, four groups of species were recognized: (1) Non-Antarctic, (2) cryopelagic (including two visually oriented benthic species), (3) pelagic and benthopelagic, and (4) benthic.     

Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean

Fluorescence in situ hybridization (FISH) in combination with polynucleotide probes revealed that the two major groups of planktonic Archaea (Crenarchaeota and Euryarchaeota) exhibit a different distribution pattern in the water column of the Pacific subtropical gyre and in the Antarctic Circumpolar Current system. While Euryarchaeota were found to be more dominant in nearsurface waters, Crenarchaeota were relatively more abundant in the mesopelagic and bathypelagic waters. We determined the abundance of archaea in the mesopelagic and bathypelagic North Atlantic along a south-north transect of more than 4,000 km. Using an improved catalyzed reporter deposition-FISH (CARD-FISH) method and specific oligonucleotide probes, we found that archaea were consistently more abundant than bacteria below a 100-m depth. Combining microautoradiography with CARD-FISH revealed a high fraction of metabolically active cells in the deep ocean. Even at a 3,000-m depth, about 16% of the bacteria were taking up leucine. The percentage of Euryarchaeota and Crenarchaeaota taking up leucine did not follow a specific trend, with depths ranging from 6 to 35% and 3 to 18%, respectively. The fraction of Crenarchaeota taking up inorganic carbon increased with depth, while Euryarchaeota taking up inorganic carbon decreased from 200 m to 3,000 m in depth. The ability of archaea to take up inorganic carbon was used as a proxy to estimate archaeal cell production and to compare this archaeal production with total prokaryotic production measured via leucine incorporation. We estimate that archaeal production in the mesopelagic and bathypelagic North Atlantic contributes between 13 to 27% to the total prokaryotic production in the oxygen minimum layer and 41 to 84% in the Labrador Sea Water, declining to 10 to 20% in the North Atlantic Deep Water. Thus, planktonic archaea are actively growing in the dark ocean although at lower growth rates than bacteria and might play a significant role in the oceanic carbon cycle.