深海氨氧化古菌的环境适应基础及生态功能

氨氧化古菌是地球上丰度最高的微生物类群之一,驱动氮循环。尤其在深海,其相对丰度可达原核生物的20%-40%。然而,纯培养的缺乏严重阻碍了我们全面认知深海氨氧化古菌的生理特性和生态贡献。本文系统性地分析了深海环境特征与微生物适应性之间的关系,聚焦深海氨氧化古菌的潜在生存策略和代谢偏好。这些信息将有助于我们设计适用于深海氨氧化古菌的培养技术。此外,从系统发育和生理特性来看,深海氨氧化古菌与土壤或表层海洋来源的氨氧化古菌有显著区别,提示我们需要根据其特性重新估算全球海洋氮通量。     

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.     

Neutrophilic Iron-Oxidizing Bacteria in the Ocean: Their Habitats,Diversity, and Roles in Mineral Deposition,Rock Alteration,and Biomass Production in the Deep-Sea

The importance of metals to life has long been appreciated. Iron (Fe) is the fourth most abundant element overall, and the second most abundant element that is redox-active in near-surface aqueous habitats, rendering it the most important environmental metal. While it has long been recognized that microorganisms participate in the global iron cycle, appreciation for the pivotal role that redox cycling of iron plays in energy conservation among diverse prokaryotes has grown substantially in the past decade. In addition, redox reactions involving Fe are linked to several other biogeochemical cycles (e.g., carbon), with significant ecological ramifications. The increasing appreciation for the role of microbes in redox transformations of Fe is reflected in a recent surge in biological and environmental studies of microorganisms that conserve energy for growth from redox cycling of Fe compounds, particularly in the deep ocean. Here we highlight some of the key habitats where microbial Fe-oxidation plays significant ecological and biogeochemical roles in the oceanic regime, and provide a synthesis of recent studies concerning this important physiological group. We also provide the first evidence that microbial Fe-oxidizing bacteria are a critical factor in the kinetics of mineral dissolution at the seafloor, by accelerating dissolution by 6–8 times over abiotic rates. We assert that these recent studies, which indicate that microbial Fe-oxidation is widespread in the deep-sea, combined with the apparent role that this group play in promoting rock and mineral weathering, indicate that a great deal more attention to these microorganisms is warranted in order to elucidate the full physiological and phylogenetic diversity and activity of the neutrophilic Fe-oxidizing bacteria in the oceans.     

海洋奇古菌门认知的拓展：从新类群到新功能

奇古菌门是全球海洋中的重要微生物类群,在海洋原核浮游生物中的比例可达20%–40%。作为一类化能无机自养微生物,奇古菌门成员可通过氧化氨获得能量,实现不依赖光照的无机碳固定,在碳、氮等元素的地球化学循环中起关键作用。奇古菌门是海洋中氨氧化反应的主要执行者,其化能合成的有机质是海洋特别是深海环境中微生物的重要能量来源。随着研究的逐步深入,有关该类群生理代谢特性的认知不断被拓展,包括奇古菌门异养代谢的揭示、不具氨氧化能力类群在深海中的发现,以及最新报道的奇古菌门在厌氧条件下介导氧气、氧化亚氮和氮气的产生等。这些研究揭示了奇古菌门参与海洋生物地球化学循环和气候变化调节的新机制,为围绕该类群的深入探究和培养提供了新的思路和方向。本文从群落组成、环境适应、生态功能、进化历史和培养现状等方面综述了近年来有关海洋奇古菌门的新发现和新认识,以期增进对该类群的了解。     

Environmental variables and evolution of xenobiotic catabolism in Bacteria

The use of microorganisms for remediation of contaminated soil and groundwater has been limited by our incomplete understanding of how environmental variables influence the activities of microorganisms. Recent research has increased our knowledge of the mechanisms whereby environmental variables can regulate microbial processes, including gene transfer and expression. This review examines factors that influence transfer of genetic material between bacteria in the environmental (evolution of genotypes) and utilization of genetic capabilities (expression of phenotypes).     

When Pasteurian Science Went to Sea: The Birth of Marine Microbiology

In the late nineteenth century, French naturalists were global leaders in microbial research. Louis Pasteur advanced sterilization techniques and demonstrated that dust particles in the air could contaminate a putrefiable liquid. Pasteur’s discoveries prompted a new research program for the naturalists of the Talisman and Travailleur expeditions: to recover uncontaminated water and mud samples from the deep sea. French naturalists Adrien Certes and Paul Regnard both independently conducted experiments to address the question of whether microorganisms inhabited the oceans and whether organic material in the deep sea was subject to decomposition. The experiments of Certes and Regnard have largely been omitted from histories of microbiology and marine science. However, an examination of their work is crucial for understanding the context in which marine microbiology first developed. At the end of the nineteenth century, marine microbiology emerged from the disciplinary melding of terrestrial microbial ecology, experimental physiology, and the then-nascent field of deep-sea biology.     

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.     

Microbial diversity and biogeochemistry of the Guaymas Basin deep‐sea hydrothermal plume

Hydrothermal plumes are hot spots of microbial biogeochemistry in the deep ocean, yet little is known about the diversity or ecology of microorganisms inhabiting plumes. Recent biogeochemical evidence shows that Mn(II) oxidation in the Guaymas Basin (GB) hydrothermal plume is microbially mediated and suggests that the plume microbial community is distinct from deep‐sea communities. Here we use a molecular approach to compare microbial diversity in the GB plume and in background deep seawater communities, and cultivation to identify Mn(II)‐oxidizing bacteria from plumes and sediments. Despite dramatic differences in Mn(II) oxidation rates between plumes and background seawater, microbial diversity and membership were remarkably similar. All bacterial clone libraries were dominated by Gammaproteobacteria and archaeal clone libraries were dominated by Crenarchaeota. Two lineages, both phylogenetically related to methanotrophs and/or methylotrophs, were consistently over‐represented in the plume. Eight Mn(II)‐oxidizing bacteria were isolated, but none of these or previously identified Mn(II) oxidizers were abundant in clone libraries. Taken together with Mn(II) oxidation rates measured in laboratory cultures and in the field, these results suggest that Mn(II) oxidation in the GB hydrothermal plume is mediated by genome‐level dynamics (gene content and/or expression) of microorganisms that are indigenous and abundant in the deep sea but have yet to be unidentified as Mn(II) oxidizers.     

微塑料附着微生物研究进展

近年来,微塑料引起的环境污染已经成为一个全球性的问题,在海洋环境中,微生物可以附着于微塑料表面形成生物被膜。已有研究表明生物被膜可以为生活在其内部的细菌提供保护,被膜中可能富集了对人体或者水生生物有害的致病菌,且频繁的基因交流可能产生更多耐药菌。微塑料表面附着的微生物,能借助大洋环流随微塑料在海洋中迁徙,进而可能引起微生物入侵事件的发生。主要对微塑料与生物被膜之间的相互作用、微塑料与附着在其表面的塑料降解菌、微塑料与致病菌、微塑料对微生物迁徙的影响,以及微塑料表面生物被膜中耐药基因的扩散进行综述,对微塑料附着微生物未来研究方向进行了展望,为更好地了解海洋微塑料污染提供参考。     

The changing face of the deep: Colonization of the Early Ordovician deep-sea floor, Puna, northwest Argentina

An Upper Tremadocian deep-sea ichnofauna from the Chiquero Formation of Puna, northwest Argentina, represents a link between Ediacaran and Cambrian microbial-mat dominated ecosystems and younger Ordovician deep-marine trace-fossil assemblages. This ichnofauna is preserved at the base of thin-bedded turbidites formed in the lobe fringe of a back-arc deep-sea fan. While Ediacaran–Cambrian deep-marine trace fossils are typically linked to matground grazing and feeding, microbial textures in the Chiquero Formation are rare and not associated with trace fossils. Morphologic patterns (e.g. radial trace fossils and networks) of the Chiquero ichnofauna indicate the onset of novel trophic types, recording trapping of microorganisms and bacterial farming. However, in comparison with younger Ordovician deep-sea ichnofaunas, graphoglyptids are relatively rare, poorly diverse, and geometrically simpler. This study indicates that the Early Ordovician was a pivotal point in the ecology of deep-sea infaunal communities. This Upper Tremadocian ichnofauna records the arrival of the Agronomic Revolution to the deep sea. Comparisons with slightly older and younger deep-sea ichnofaunas demonstrate that the colonization of the deep sea was a protracted process spanning the Early Paleozoic, lagging behind colonization of nearshore and offshore substrates.     

Highly Similar Prokaryotic Communities of Sunken Wood at Shallow and Deep-Sea Sites Across the Oceans

With an increased appreciation of the frequency of their occurrence, large organic falls such as sunken wood and whale carcasses have become important to consider in the ecology of the oceans. Organic-rich deep-sea falls may play a major role in the dispersal and evolution of chemoautotrophic communities at the ocean floor, and chemosynthetic symbiotic, free-living, and attached microorganisms may drive the primary production at these communities. However, little is known about the microbiota thriving in and around organic falls. Our aim was to investigate and compare free-living and attached communities of bacteria and archaea from artificially immersed and naturally sunken wood logs with varying characteristics at several sites in the deep sea and in shallow water to address basic questions on the microbial ecology of sunken wood. Multivariate indirect ordination analyses of capillary electrophoresis single-stranded conformation polymorphisms (CE-SSCP) fingerprinting profiles demonstrated high similarity of bacterial and archaeal assemblages present in timbers and logs situated at geographically distant sites and at different depths of immersion. This similarity implies that wood falls harbor a specialized microbiota as observed in other ecosystems when the same environmental conditions reoccur. Scanning and transmission electron microscopy observations combined with multivariate direct gradient analysis of Bacteria CE-SSCP profiles demonstrate that type of wood (hard vs. softwood), and time of immersion are important in structuring sunken wood bacterial communities. Archaeal populations were present only in samples with substantial signs of decay, which were also more similar in their bacterial assemblages, providing indirect evidence of temporal succession in the microbial communities that develop in and around wood falls.     

Bacteria dominate the ammonia-oxidizing community in a hydrothermal vent site at the Mid-Atlantic Ridge of the South Atlantic Ocean

Ammonia oxidation is the first and rate-limiting step of nitrification, which is carried out by two groups of microorganisms: ammonia-oxidizing bacteria (AOB) and the recently discovered ammonia-oxidizing archaea (AOA). In this study, diversity and abundance of AOB and AOA were investigated in five rock samples from a deep-sea hydrothermal vent site at the Mid-Atlantic Ridge (MAR) of the South Atlantic Ocean. Both bacterial and archaeal ammonia monooxygenase subunit A (amoA) gene sequences obtained in this study were closely related to the sequences retrieved from deep-sea environments, indicating that AOB and AOA in this hydrothermal vent site showed typical deep ocean features. AOA were more diverse but less abundant than AOB. The ratios of AOA/AOB amoA gene abundance ranged from 1/3893 to 1/242 in all investigate samples, indicating that bacteria may be the major members responding to the aerobic ammonia oxidation in this hydrothermal vent site. Furthermore, diversity and abundance of AOA and AOB were significantly correlated with the contents of total nitrogen and total sulfur in investigated samples, suggesting that these two environmental factors exert strong influences on distribution of ammonia oxidizers in deep-sea hydrothermal vent environment.     

Major environmental drivers determining life and death of cold-water corals through time

Cold-water corals (CWCs) are the engineers of complex ecosystems forming unique biodiversity hotspots in the deep sea. They are expected to suffer dramatically from future environmental changes in the oceans such as ocean warming, food depletion, deoxygenation, and acidification. However, over the last decades of intense deep-sea research, no extinction event of a CWC ecosystem is documented, leaving quite some uncertainty on their sensitivity to these environmental parameters. Paleoceanographic reconstructions offer the opportunity to align the on- and offsets of CWC proliferation to environmental parameters. Here, we present the synthesis of 6 case studies from the North Atlantic Ocean and the Mediterranean Sea, revealing that food supply controlled by export production and turbulent hydrodynamics at the seabed exerted the strongest impact on coral vitality during the past 20,000 years, whereas locally low oxygen concentrations in the bottom water can act as an additional relevant stressor. The fate of CWCs in a changing ocean will largely depend on how these oceanographic processes will be modulated. Future ocean deoxygenation may be compensated regionally where the food delivery and food quality are optimal.

Cold-water corals are the engineers of complex ecosystems forming unique biodiversity hot spots in the deep sea, but there is substantial uncertainty regarding their sensitivity to environmental parameters. A synthesis of six paleoceanographic reconstructions reveals that food supply exerted the strongest impact on coral vitality during the past 20,000 years, whereas locally low oxygen concentrations can act as a stressor.     

Microbial life in ridge flank crustal fluids

To determine the microbial community diversity within old oceanic crust, a novel sampling strategy was used to collect crustal fluids at Baby Bare Seamount, a 3.5 Ma old outcrop located in the north-east Pacific Ocean on the eastern flank of the Juan de Fuca Ridge. Stainless steel probes were driven directly into the igneous ocean crust to obtain samples of ridge flank crustal fluids. Genetic signatures and enrichment cultures of microorganisms demonstrate that these crustal fluids host a microbial community composed of species indigenous to the subseafloor, including anaerobic thermophiles, and species from other deep-sea habitats, such as seawater and sediments. Evidence using molecular techniques indicates the presence of a relatively small but active microbial population, dominated by bacteria. The microbial community diversity found in the crustal fluids may indicate habitat variability in old oceanic crust, with inputs of nutrients from seawater, sediment pore-water fluids and possibly hydrothermal sources. This report further supports the presence of an indigenous microbial community in ridge flank crustal fluids and advances our understanding of the potential physiological and phylogenetic diversity of this community.     

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.     

Submarine canyons: hotspots of benthic biomass and productivity in the deep sea

Submarine canyons are dramatic and widespread topographic features crossing continental and island margins in all oceans. Canyons can be sites of enhanced organic-matter flux and deposition through entrainment of coastal detrital export, dense shelf-water cascade, channelling of resuspended particulate material and focusing of sediment deposition. Despite their unusual ecological characteristics and global distribution along oceanic continental margins, only scattered information is available about the influence of submarine canyons on deep-sea ecosystem structure and productivity. Here, we show that deep-sea canyons such as the Kaikoura Canyon on the eastern New Zealand margin (42°01′ S, 173°03′ E) can sustain enormous biomasses of infaunal megabenthic invertebrates over large areas. Our reported biomass values are 100-fold higher than those previously reported for deep-sea (non-chemosynthetic) habitats below 500 m in the ocean. We also present evidence from deep-sea-towed camera images that areas in the canyon that have the extraordinary benthic biomass also harbour high abundances of macrourid (rattail) fishes likely to be feeding on the macro- and megabenthos. Bottom-trawl catch data also indicate that the Kaikoura Canyon has dramatically higher abundances of benthic-feeding fishes than adjacent slopes. Our results demonstrate that the Kaikoura Canyon is one of the most productive habitats described so far in the deep sea. A new global inventory suggests there are at least 660 submarine canyons worldwide, approximately 100 of which could be biomass hotspots similar to the Kaikoura Canyon. The importance of such deep-sea canyons as potential hotspots of production and commercial fisheries yields merits substantial further study.     

Single Cells within the Puerto Rico Trench Suggest Hadal Adaptation of Microbial Lineages

Hadal ecosystems are found at a depth of 6,000 m below sea level and below, occupying less than 1% of the total area of the ocean. The microbial communities and metabolic potential in these ecosystems are largely uncharacterized. Here, we present four single amplified genomes (SAGs) obtained from 8,219 m below the sea surface within the hadal ecosystem of the Puerto Rico Trench (PRT). These SAGs are derived from members of deep-sea clades, including the Thaumarchaeota and SAR11 clade, and two are related to previously isolated piezophilic (high-pressure-adapted) microorganisms. In order to identify genes that might play a role in adaptation to deep-sea environments, comparative analyses were performed with genomes from closely related shallow-water microbes. The archaeal SAG possesses genes associated with mixotrophy, including lipoylation and the glycine cleavage pathway. The SAR11 SAG encodes glycolytic enzymes previously reported to be missing from this abundant and cosmopolitan group. The other SAGs, which are related to piezophilic isolates, possess genes that may supplement energy demands through the oxidation of hydrogen or the reduction of nitrous oxide. We found evidence for potential trench-specific gene distributions, as several SAG genes were observed only in a PRT metagenome and not in shallower deep-sea metagenomes. These results illustrate new ecotype features that might perform important roles in the adaptation of microorganisms to life in hadal environments.     

Causal analysis of the temperature impact on deep-sea biodiversity

The deep sea comprises more than 90% of the ocean; therefore, understanding the controlling factors of biodiversity in the deep sea is of great importance for predicting future changes in the functioning of the ocean system. Consensus has recently been increasing on two plausible factors that have often been discussed as the drivers of deep‐sea species richness in the contexts of the species‐energy and physiological tolerance hypotheses: (i) seafloor particulate organic carbon (POC) derived from primary production in the euphotic zone and (ii) temperature. Nonetheless, factors that drive deep-sea biodiversity are still actively debated potentially owing to a mirage of correlations (sign and magnitude are generally time dependent), which are often found in nonlinear, complex ecological systems, making the characterization of causalities difficult. Here, we tested the causal influences of POC flux and temperature on species richness using long-term palaeoecological datasets derived from sediment core samples and convergent cross mapping, a numerical method for characterizing causal relationships in complex systems. The results showed that temperature, but not POC flux, influenced species richness over 10³–10⁴-year time scales. The temperature–richness relationship in the deep sea suggests that human-induced future climate change may, under some conditions, affect deep-sea ecosystems through deep-water circulation changes rather than surface productivity changes.     

Reproduction in marine invertebrates in “stable” environments: the deep sea model

Summary

Studies over the last 15 years have revealed that deep-sea benthic megainvertebrates show a variety of reproductive patterns that are adapted to the deep-sea, an environment in which the fauna occurs at low densities and resources are sparse. In the NE Atlantic the majority of species reproduce year round whilst a limited number of species reproduce on a seasonal basis believed to be entrained by the deposition of surface derived organic material on the deep-sea bed. A third pattern of rapid growth and early reproduction is found in a limited number of species that utilize unpredictable and ephemeral resources in the deep sea. Examination of the fertilization and behavioural biology of species from the bathyal depths suggest some species enhance fertilization success by forming pairs during their breeding season. However, the same concentration of sperm, as seen in shallow water invertebrates, is required for successful fertilization. At least one deep-sea species of echinoid requires high pressure for successful embryogenesis suggesting a depth-related segregation of deep-sea fauna. The origin of megafaunal populations of deep-sea invertebrates in the N. Atlantic is discussed in the light of these new data in relation to varying reproductive patterns and the environmental changes that have occurred during the last deglaciation.