Europa as an Abode of Life

Life as we know it on Earth depends on liquid water, a suite of `biogenic' elements (most famously carbon) and a useful source of free energy. Here we review Europa's suitability for life from the perspective of these three requirements. It is likely, though not yet certain, that Europa harbors a subsurface ocean of liquid water whose volume is about twice that of Earth's oceans. Little is known about Europa's inventory of carbon, nitrogen, and other biogenic elements, but lower bounds on these can be placed by considering the role of cometary delivery over Europa's history. Sources of free energy are challenging for a world covered with an ice layer kilometers thick, but it is possible that hydrothermal activity and/or organics and oxidants provided by the action of radiation chemistry at Europa's surface and subsequent mixing into Europa's ocean could provide the electron donors and acceptors needed to power a Europan ecosystem. It is not premature to draw lessons from the search for life on Mars with the Viking spacecraft for planning exobiological missions to Europa.     

Hidden Historical Habitat-Linked Population Divergence and Contemporary Gene Flow of a Deep-Sea Patellogastropod Limpet

Hydrothermal vents and hydrocarbon seeps in the deep ocean are rare oases fueled by chemosynthesis. Biological communities inhabiting these ecosystems are often distributed in widely separated habitats, raising intriguing questions on how these organisms achieve connectivity and whether habitat types facilitate intraspecific divergence. The deep-sea patellogastropod limpet Bathyacmaea nipponica that colonizes both vents and seeps across ∼2,400 km in the Northwest Pacific is a feasible model to answer these questions. We analyzed 123 individuals from four vents and three seeps using a comprehensive method incorporating population genomics and physical ocean modeling. Genome survey sequencing and genotyping-by-sequencing resulted in 9,838 single-nucleotide polymorphisms for population genomic analyses. Genetic divergence and demographic analyses revealed four habitat-linked (i.e., three seep and one vent) genetic groups, with the vent genetic group established via the opportunistic invasion of a few limpet larvae from a nearby seep genetic group. TreeMix analysis uncovered three historical seep-to-vent migration events. ADMIXTURE and divMigrate analyses elucidated weak contemporary gene flow from a seep genetic group to the vent genetic group. Physical ocean modeling underlined the potential roles of seafloor topography and ocean currents in shaping the genetic connectivity, contemporary migration, and local hybridization of these deep-sea limpets. Our study highlighted the power of integrating genomic and oceanographic approaches in deciphering the demography and diversification of deep-sea organisms. Given the increasing anthropogenic activities (e.g., mining and gas hydrate extraction) affecting the deep ocean, our results have implications for the conservation of deep-sea biodiversity and establishment of marine protected areas.     

Diet and prey consumption of Antarctic petrels Thalassoica antarctica at Svarthamaren, Dronning Maud Land, and at sea outside the colony

The diet of the Antarctic petrel Thalassoica antarctica was studied during two seasons at Svarthamaren, an inland colony in Dronning Maud Land, Antarctica, and in the pack ice off the coast of Svarthamaren. The most important food (wet mass) at Svarthamaren was crustaceans (67%), fish (29%) and squid (5%); however, individuals collected in the pack ice took mostly fish (87%). The prey composition and lengths of prey are comparable to what has been documented in other studies on this species. Estimates of food consumption by birds breeding at Svarthamaren (ca. 250,000 pairs) suggest that approximately 6500 tonnes of crustaceans, 2800 tonnes of fish and 435 tonnes of squid are consumed during the breeding season. The annual consumptions of these birds are estimated to be 34,100 tonnes of crustaceans, 14,700 tonnes of fish, and 2300 tonnes of squid. Satellite telemetry data indicate that Antarctic petrels from Svarthamaren may fly more than 3000 km during one foraging trip, and thus may cover a huge ocean area to obtain their prey. Received: 1 September 1997 / Accepted: 3 February 1998     

The effects of natural iron fertilisation on deep-sea ecology: the Crozet Plateau, Southern Indian Ocean

The addition of iron to high-nutrient low-chlorophyll (HNLC) oceanic waters stimulates phytoplankton, leading to greater primary production. Large-scale artificial ocean iron fertilization (OIF) has been proposed as a means of mitigating anthropogenic atmospheric CO(2), but its impacts on ocean ecosystems below the photic zone are unknown. Natural OIF, through the addition of iron leached from volcanic islands, has been shown to enhance primary productivity and carbon export and so can be used to study the effects of OIF on life in the ocean. We compared two closely-located deep-sea sites (～400 km apart and both at ～4200 m water depth) to the East (naturally iron fertilized; +Fe) and South (HNLC) of the Crozet Islands in the southern Indian Ocean. Our results suggest that long-term geo-engineering of surface oceanic waters via artificial OIF would lead to significant changes in deep-sea ecosystems. We found that the +Fe area had greater supplies of organic matter inputs to the seafloor, including polyunsaturated fatty acid and carotenoid nutrients. The +Fe site also had greater densities and biomasses of large deep-sea animals with lower levels of evenness in community structuring. The species composition was also very different, with the +Fe site showing similarities to eutrophic sites in other ocean basins. Moreover, major differences occurred in the taxa at the +Fe and HNLC sites revealing the crucial role that surface oceanic conditions play in changing and structuring deep-sea benthic communities.     

The dynamics of biogeographic ranges in the deep sea

Anthropogenic disturbances such as fishing, mining, oil drilling, bioprospecting, warming, and acidification in the deep sea are increasing, yet generalities about deep-sea biogeography remain elusive. Owing to the lack of perceived environmental variability and geographical barriers, ranges of deep-sea species were traditionally assumed to be exceedingly large. In contrast, seamount and chemosynthetic habitats with reported high endemicity challenge the broad applicability of a single biogeographic paradigm for the deep sea. New research benefiting from higher resolution sampling, molecular methods and public databases can now more rigorously examine dispersal distances and species ranges on the vast ocean floor. Here, we explore the major outstanding questions in deep-sea biogeography. Based on current evidence, many taxa appear broadly distributed across the deep sea, a pattern replicated in both the abyssal plains and specialized environments such as hydrothermal vents. Cold waters may slow larval metabolism and development augmenting the great intrinsic ability for dispersal among many deep-sea species. Currents, environmental shifts, and topography can prove to be dispersal barriers but are often semipermeable. Evidence of historical events such as points of faunal origin and climatic fluctuations are also evident in contemporary biogeographic ranges. Continued synthetic analysis, database construction, theoretical advancement and field sampling will be required to further refine hypotheses regarding deep-sea biogeography.     

Exponential decline of deep-sea ecosystem functioning linked to benthic biodiversity loss

BACKGROUND: Recent investigations suggest that biodiversity loss might impair the functioning and sustainability of ecosystems. Although deep-sea ecosystems are the most extensive on Earth, represent the largest reservoir of biomass, and host a large proportion of undiscovered biodiversity, the data needed to evaluate the consequences of biodiversity loss on the ocean floor are completely lacking. RESULTS: Here, we present a global-scale study based on 116 deep-sea sites that relates benthic biodiversity to several independent indicators of ecosystem functioning and efficiency. We show that deep-sea ecosystem functioning is exponentially related to deep-sea biodiversity and that ecosystem efficiency is also exponentially linked to functional biodiversity. These results suggest that a higher biodiversity supports higher rates of ecosystem processes and an increased efficiency with which these processes are performed. The exponential relationships presented here, being consistent across a wide range of deep-sea ecosystems, suggest that mutually positive functional interactions (ecological facilitation) can be common in the largest biome of our biosphere. CONCLUSIONS: Our results suggest that a biodiversity loss in deep-sea ecosystems might be associated with exponential reductions of their functions. Because the deep sea plays a key role in ecological and biogeochemical processes at a global scale, this study provides scientific evidence that the conservation of deep-sea biodiversity is a priority for a sustainable functioning of the worlds' oceans.     

深海钻探计划(DSDP)31航次296站晚新生代介形类

本文研究了深海钻探(DSDP)31航次296站晚新生代介形类动物群的性质及其古海洋学意义.此站钻孔上部上新统至全新统以超微浮游生物软泥和粘土为主的16块岩芯中,共分析获得介形类化石8属11种,计有:Poseidonamicus major Benson, P. anteropunctatus Whatley et al., P. punctatus Whatley et al., Pennyella dorsoserrata (Brady), Henryhowella sp., Pterygocythere mucronalatum (Brady), Abyssocythere sp., Abyssocythereis sulcatoperforata (Brady), Pelecocythere sp., Krithe sp. 1和Krithe sp.2.这些介形类属种均为冷海域深海区介形类分子.由此表明,西北太平洋边缘地区在晚新生代曾为一深海区.在第四纪,其深度可能和现今296站的深度大致相当;在上新世,其深度可能更深一些.研究结果证实,深海底栖介形类属种的分布具全球性;在相当长的地质时期内,介形类属种的形态和壳饰都非常稳定,无明显变化.同时,进一步证实,介形类个体大小变化与深度相关,同一种介形类壳体随水域深度加深而增大.     

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.     

Barophilic growth of bacteria from intestinal tracts of deep-sea invertebrates

Digestive tracts of abyssal scavenging amphipods and a deep-sea holothurian were examined for the presence of intestinal microflora capable of rapid proliferation under in situ pressures of 430 to 520 atmospheres (atm) and temperatures of 3–5°C. For two amphipod specimens, population doubling times of 5 and 6 hours were observed under in situ conditions, compared to 8 and 6 hours, respectively, at 1 atm. Growth enhancement under pressure was related inversely to initial population size and directly to concentration of available nutrient. In the case of the deposit-feeding holothurian, attached bacteria scraped from the intestinal lining showed a doubling time, under pressure, of 11 hours, compared to 36 hours for transient sediment bacteria that comprised the gut contents. These data suggest that deep-sea animals possess a commensal gut flora capable of responding to increased nutrient levels, via feeding of the host, without inhibition by the elevated hydrostatic pressures encountered in the deep ocean environment.     

How Can We Identify and Communicate the Ecological Value of Deep-Sea Ecosystem Services?

Submarine canyons are considered biodiversity hotspots which have been identified for their important roles in connecting the deep sea with shallower waters. To date, a huge gap exists between the high importance that scientists associate with deep-sea ecosystem services and the communication of this knowledge to decision makers and to the wider public, who remain largely ignorant of the importance of these services. The connectivity and complexity of marine ecosystems makes knowledge transfer very challenging, and new communication tools are necessary to increase understanding of ecological values beyond the science community. We show how the Ecosystem Principles Approach, a method that explains the importance of ocean processes via easily understandable ecological principles, might overcome this challenge for deep-sea ecosystem services. Scientists were asked to help develop a list of clear and concise ecosystem principles for the functioning of submarine canyons through a Delphi process to facilitate future transfers of ecological knowledge. These ecosystem principles describe ecosystem processes, link such processes to ecosystem services, and provide spatial and temporal information on the connectivity between deep and shallow waters. They also elucidate unique characteristics of submarine canyons. Our Ecosystem Principles Approach was successful in integrating ecological information into the ecosystem services assessment process. It therefore has a high potential to be the next step towards a wider implementation of ecological values in marine planning. We believe that successful communication of ecological knowledge is the key to a wider public support for ocean conservation, and that this endeavour has to be driven by scientists in their own interest as major deep-sea stakeholders.     

Protist diversity and function in the dark ocean – Challenging the paradigms of deep-sea ecology with special emphasis on foraminiferans and naked protists

The dark ocean and the underlying deep seafloor together represent the largest environment on this planet, comprising about 80% of the oceanic volume and covering more than two-thirds of the Earth's surface, as well as hosting a major part of the total biosphere. Emerging evidence suggests that these vast pelagic and benthic habitats play a major role in ocean biogeochemistry and represent an “untapped reservoir” of high genetic and metabolic microbial diversity. Due to its huge volume, the water column of the dark ocean is the largest reservoir of organic carbon in the biosphere and likely plays a major role in the global carbon budget. The dark ocean and the seafloor beneath it are also home to a largely enigmatic food web comprising little-known and sometimes spectacular organisms, mainly prokaryotes and protists. This review considers the globally important role of pelagic and benthic protists across all protistan size classes in the deep-sea realm, with a focus on their taxonomy, diversity, and physiological properties, including their role in deep microbial food webs. We argue that, given the important contribution that protists must make to deep-sea biodiversity and ecosystem processes, they should not be overlooked in biological studies of the deep ocean.     

Cesare Emiliani (1922–1995), pioneer of Ice Age studies and oxygen isotope stratigraphy

Cesare Emiliani established that the ice ages of the last half million years or so are cyclic phenomena, which gave strong support to the hypothesis of Milankovitch. He discovered the cycles when analyzing foraminifers from long deep-sea cores for their oxygen isotope composition (cores were from the Swedish Deep-Sea Expedition, from the Lamont collection and later from collections made at Miami). Emiliani’s method has become the standard procedure for interpreting the deep-sea record in terms of ocean and climate history. Emiliani introduced a time scale suggesting that the cycles are typically 40 000 years in duration, and he defended this scale for almost 20 years. He also thought that temperature was a more important influence on oxygen isotope variations of the ocean than the buildup and decay of northern hemisphere ice sheets. Both these notions proved incorrect. However, his insistence that the Milankovitch mechanism, in conjunction with ice dynamics and crustal response to loading, is the driving force behind the climate cycles of the Quaternary proved well founded.     

The western Mediterranean during the Last Glacial: Attacking a no-analog problem

Assemblages of planktic Foraminifera from the western Mediterranean during the last world ice volume maximum (18 000 yrs. B.P.) are presented for two rapid sedimentation rate deep-sea cores, one from the northern and one from the western part of the basin. The locations permit monitoring of hydrography in the Alboran Sea, where exchange occurs with the Atlantic, and in the northern Balearic Sea, where the warm Mediterranean out-flow to the world ocean is generated by a unique vertical mixing process. This latter makes a significant contribution to the heat budget of the global deep-sea. Thus the assemblages reflect western Mediterranean oceanography and interaction with the Atlantic during the last ice age. Quantitative empirical paleo-oceanographic interpretation of the faunas is not possible because they occur in relative abundances not seen in the North Atlantic or Mediterranean of today. However, some more general deductions of paleohydrography are possible. The faunas indicate that the western Mediterranean was considerably colder 18 000 yrs. B.P. and highly seasonal (large annual thermal contrast), reflecting the seas' nearly land-locked position. Climate surrounding the basin appears to have been quite variable over periods of less than 500 years. The faunas also indicate that interchange between the eastern and western Mediterranean seas was much altered during the glacial and that the character of the water returned to the Atlantic from the Mediterranean was quite different, probably colder, from that of the present. The deep world ocean would then have been lacking a significant heat source 18 000 yrs. B.P.     

Shell nacre ultrastructure and depressurisation dissolution in the deep-sea hydrothermal vent mussel Bathymodiolus azoricus

This study describes the micro-morphological features of the shell nacre in the vent mytilid Bathymodiolus azoricus collected along a bathymetric gradient of deep-sea hydrothermal vents of the mid-Atlantic ridge (MAR). Pressure-dependent crystallisation patterns were detected in animals subjected to post-capture hydrostatic simulations. We provide evidence for the following: (1) shell micro morphology in B. azoricus is similar to that of several vent and cold-seep species, but the prismatic shell layers may vary among bathymodiolids; (2) nacre micro-morphology of mussels from three vent sites of the MAR did not differ significantly; minor differences do not appear to be related to hydrostatic pressure, but rather to calcium ion availability; (3) decompression stress may cause drop off in pH of the pallial fluid that damages nascent crystals, and in a more advanced phase, the aragonite tablets as well as the continuous layer of mature nacre; and (4) adverse effects of decompression on calcium salt deposition in shells was diminished by re-pressurisation of specimens. The implications of the putative influence of hydrostatic pressure on biomineralisation processes in molluscs are discussed. An erratum to this article can be found at     

Reproductive strategy of the tiny abyssal scallop (Delectopecten vitreus macrocheiricolus) collected on the bottom of the Japan Sea,surmised from histological observations of the gonads

Two hundred and fifteen individuals of the tiny abyssal scallop (Delectopecten vitreus macrocheiricolus) were collected at a depth of around 3,000 m on the bottom of the Japan Sea during a cruise of the Yokosuka/Shinkai 6500 YK 01-06. The scallop population included specimens of 4 sizes, i.e., very small, small, middle, and large, with mantle sizes of 1-2mm, 3-5mm, 6-9mm, and 10-12mm, respectively. Histological observations revealed that the large-size group was at the stage just after oviposition or spermiation, or in the regressed stage of gametogenesis. The small- and middle-size groups were in the growing stage of gametogenesis. These results suggest that only the large-size individuals were responsible for reproduction and that the small- and middle-size individuals would participate in subsequent reproductions. This paper will discuss the reproductive strategy of this scallop living at such great depth.     

Global diversity and biogeography of deep-sea pelagic prokaryotes

The deep-sea is the largest biome of the biosphere, and contains more than half of the whole ocean''s microbes. Uncovering their general patterns of diversity and community structure at a global scale remains a great challenge, as only fragmentary information of deep-sea microbial diversity exists based on regional-scale studies. Here we report the first globally comprehensive survey of the prokaryotic communities inhabiting the bathypelagic ocean using high-throughput sequencing of the 16S rRNA gene. This work identifies the dominant prokaryotes in the pelagic deep ocean and reveals that 50% of the operational taxonomic units (OTUs) belong to previously unknown prokaryotic taxa, most of which are rare and appear in just a few samples. We show that whereas the local richness of communities is comparable to that observed in previous regional studies, the global pool of prokaryotic taxa detected is modest (~3600 OTUs), as a high proportion of OTUs are shared among samples. The water masses appear to act as clear drivers of the geographical distribution of both particle-attached and free-living prokaryotes. In addition, we show that the deep-oceanic basins in which the bathypelagic realm is divided contain different particle-attached (but not free-living) microbial communities. The combination of the aging of the water masses and a lack of complete dispersal are identified as the main drivers for this biogeographical pattern. All together, we identify the potential of the deep ocean as a reservoir of still unknown biological diversity with a higher degree of spatial complexity than hitherto considered.     

Biodiversity in deep-sea sites located near the south part of Japan

We obtained 100 isolates of bacteria from deep-sea mud samples collected at various depths (1050–10 897 m). Various types of bacteria such as alkaliphiles, thermophiles, psychrophiles, and halophiles were recovered on agar plates at a frequency of 0.8 × 10² to 2.3 × 10⁴/g of dry sea mud. No acidophiles were recovered. These extremophilic bacteria were widely distributed, being detected at each deep-sea site, and the frequency of isolation of such extremophiles from the deep-sea mud was not directly influenced by the depth of the sampling sites. Phylogenetic analysis of deep-sea isolates based on 16S rDNA sequences revealed that a wide range of taxa were represented in the deep-sea environments. Growth patterns under high hydrostatic pressure were determined for the deep-sea isolates obtained in this study. No extremophilic strains isolated in this study showed growth at 60 MPa, although a few of the other isolates grew slightly at this hydrostatic pressure. Received: August 3, 1998 / Accepted: October 20, 1998     

Shell nacre ultrastructure and depressurisation dissolution in the deep-sea hydrothermal vent mussel <Emphasis Type="Italic">Bathymodiolus azoricus</Emphasis>

This study describes the micro-morphological features of the shell nacre in the vent mytilid Bathymodiolus azoricus collected along a bathymetric gradient of deep-sea hydrothermal vents of the mid-Atlantic ridge (MAR). Pressure-dependent crystallisation patterns were detected in animals subjected to post-capture hydrostatic simulations. We provide evidence for the following: (1) shell micro morphology in B. azoricus is similar to that of several vent and cold-seep species, but the prismatic shell layers may vary among bathymodiolids; (2) nacre micro-morphology of mussels from three vent sites of the MAR did not differ significantly; minor differences do not appear to be related to hydrostatic pressure, but rather to calcium ion availability; (3) decompression stress may cause drop off in pH of the pallial fluid that damages nascent crystals, and in a more advanced phase, the aragonite tablets as well as the continuous layer of mature nacre; and (4) adverse effects of decompression on calcium salt deposition in shells was diminished by re-pressurisation of specimens. The implications of the putative influence of hydrostatic pressure on biomineralisation processes in molluscs are discussed.     

Using Species-Area Relationships to Inform Baseline Conservation Targets for the Deep North East Atlantic

Demands on the resources of the deep-sea have increased in recent years. Consequently, the need to create and implement a comprehensive network of Marine Protected Areas (MPAs) to help manage and protect these resources has become a global political priority. Efforts are currently underway to implement MPA networks in the deep North East Atlantic. To ensure these networks are effective, it is essential that baseline information be available to inform the conservation planning process. Using empirical data, we calculated conservation targets for sessile benthic invertebrates in the deep North East Atlantic for consideration during the planning process. We assessed Species-Area Relationships across two depth bands (200–1100 m and 1100–1800 m) and nine substrata. Conservation targets were predicted for each substratum within each depth band using z-values obtained from fitting a power model to the Species-Area Relationships of observed and estimated species richness (Chao1). Results suggest an MPA network incorporating 10% of the North East Atlantic’s deep-sea area would protect approximately 58% and 49% of sessile benthic species for the depth bands 200–1100 m and 1100–1800 m, respectively. Species richness was shown to vary with substratum type indicating that, along with depth, substratum information needs to be incorporated into the conservation planning process to ensure the most effective MPA network is implemented in the deep North East Atlantic.