Dark Ocean Research Articles

Dynamic prokaryotic communities in the dark western Mediterranean Sea

Dark ocean microbial dynamics are fundamental to understand ecosystem metabolism and ocean biogeochemical processes. Yet, the ecological response of deep ocean communities to environmental perturbations remains largely unknown. Temporal and spatial dynamics of the meso- and bathypelagic prokaryotic communities were assessed throughout a 2-year seasonal sampling across the western Mediterranean Sea. A common pattern of prokaryotic communities’ depth stratification was observed across the different regions and throughout the seasons. However, sporadic and drastic alterations of the community composition and diversity occurred either at specific water masses or throughout the aphotic zone and at a basin scale. Environmental changes resulted in a major increase in the abundance of rare or low abundant phylotypes and a profound change of the community composition. Our study evidences the temporal dynamism of dark ocean prokaryotic communities, exhibiting long periods of stability but also drastic changes, with implications in community metabolism and carbon fluxes. Taken together, the results highlight the importance of monitoring the temporal patterns of dark ocean prokaryotic communities.

The redox fate of hydrogen peroxide in the marine water column

AbstractMarine microbes produce extracellular reactive oxygen species (ROS) such as superoxide and hydrogen peroxide (H2O2) as a result of regulated and nonregulated physiological and metabolic reactions. ROS production can be a sink and cryptic recycling flux of dissolved oxygen that may rival other key fluxes in the global oxygen cycle; however, the low abundance and high turnover rate of ROS makes this figure difficult to constrain. One key step in determining the disparity between the gross production of ROS and the net sink of dissolved oxygen lies in understanding the degradation pathways of H2O2 in the marine water column. In this study, we use isotope‐labeling techniques to determine the redox fate of H2O2 in a range of marine environments off the West Coast of California. We find that H2O2 reduction is greater than or equal to H2O2 oxidation at most sampled depths, with notable exceptions in some surface and intermediate water depths. The observation that H2O2 oxidation can exceed reduction in the dark ocean indicates the presence of an oxidizing decay pathway that is not among the known suite of microbially mediated enzymatic pathways (i.e., catalase and peroxidase), pointing to an abiotic and/or a nonenzymatic decay pathway at intermediate water depths. These results highlight the complexity and heterogeneity of ROS decay pathways in natural waters and their unconstrained regulation of oxygen levels within the ocean.

Vertical community patterns of Labyrinthulomycetes protists reveal their potential importance in the oceanic biological pump.

The biological pump plays a vital role in exporting organic particles into the deep ocean for long-term carbon sequestration. However, much remains unknown about some of its key microbial players. In this study, Labyrinthulomycetes protists (LP) were used to understand the significance of heterotrophic microeukaryotes in the transport of particulate organic matter from the surface to the dark ocean. Unlike the sharp vertical decrease of prokaryotic biomass, the LP biomass only slightly decreased with depth and eventually exceeded prokaryotic biomass in the bathypelagic layer. Sequencing identified high diversity of the LP communities with a dominance of Aplanochytrium at all depths. Notably, ASVs that were observed in the surface layer comprised ~20% of ASVs and ~60% of sequences in each of the deeper (including bathypelagic) layers, suggesting potential vertical export of the LP populations to the deep ocean. Further analyses of the vertical patterns of the 50 most abundant ASVs revealed niche partitioning of LP phylotypes in the pelagic ocean, including those that could decompose organic detritus and/or facilitate the formation of fast-sinking particles. Overall, this study presents several lines of evidence that the LP can be an important component of the biological pump through their multiple ecotypes in the pelagic ocean.

Metapangenomics reveals depth-dependent shifts in metabolic potential for the ubiquitous marine bacterial SAR324 lineage

BackgroundOceanic microbiomes play a pivotal role in the global carbon cycle and are central to the transformation and recycling of carbon and energy in the ocean’s interior. SAR324 is a ubiquitous but poorly understood uncultivated clade of Deltaproteobacteria that inhabits the entire water column, from ocean surface waters to its deep interior. Although some progress has been made in elucidating potential metabolic traits of SAR324 in the dark ocean, very little is known about the ecology and the metabolic capabilities of this group in the euphotic and twilight zones. To investigate the comparative genomics, ecology, and physiological potential of the SAR324 clade, we examined the distribution and variability of key genomic features and metabolic pathways in this group from surface waters to the abyss in the North Pacific Subtropical Gyre, one of the largest biomes on Earth.ResultsWe leveraged a pangenomic ecological approach, combining spatio-temporally resolved single-amplified genome, metagenomic, and metatranscriptomic datasets. The data revealed substantial genomic diversity throughout the SAR324 clade, with distinct depth and temporal distributions that clearly differentiated ecotypes. Phylogenomic subclade delineation, environmental distributions, genomic feature similarities, and metabolic capacities revealed strong congruence. The four SAR324 ecotypes delineated in this study revealed striking divergence from one another with respect to their habitat-specific metabolic potentials. The ecotypes living in the dark or twilight oceans shared genomic features and metabolic capabilities consistent with a sulfur-based chemolithoautotrophic lifestyle. In contrast, those inhabiting the sunlit ocean displayed higher plasticity energy-related metabolic pathways, supporting a presumptive photoheterotrophic lifestyle. In epipelagic SAR324 ecotypes, we observed the presence of two types of proton-pumping rhodopsins, as well as genomic, transcriptomic, and ecological evidence for active photoheterotrophy, based on xanthorhodopsin-like light-harvesting proteins.ConclusionsCombining pangenomic and both metagenomic and metatranscriptomic profiling revealed a striking divergence in the vertical distribution, genomic composition, metabolic potential, and predicted lifestyle strategies of geographically co-located members of the SAR324 bacterial clade. The results highlight the utility of metapangenomic approaches employed across environmental gradients, to decipher the properties and variation in function and ecological traits of specific phylogenetic clades within complex microbiomes.AbL6i64VtV696aBPsu8M5wVideo abstract

Precipitable Water Vapor Variation in the Clear-Cloud Transition Zone From the ARM Shortwave Spectrometer

A new technique to retrieve precipitable water vapor (PWV) amount in the clear-cloud transition zone using ground-based zenith spectral radiance is developed. The method uses zenith radiances at the water vapor band at 720 nm and at the adjacent nonadsorbing band at 750 nm. Radiative transfer calculations show that the relative difference in zenith radiance between the two bands depends on PWV and the variations in cloud optical depth introduce a small change in the relative difference which is independent of PWV amount. This allows us to retrieve PWV variations in the clear-cloud transition zone for clouds over dark ocean surface. We applied this method to a Cu cloud case with zenith radiance observations by Shortwave Array Spectroradiometer-Zenith (SASZe) during the Marine ARM GPCI Investigation of Clouds (MAGIC) field campaign. We found that there is about 10% change in PWV amount from the known-cloudy region to known-clear sky in the cloud edges.

Determining the Distribution of Fluorescent Organic Matter in the Indian Ocean Using in situ Fluorometry.

In order to determine the dynamics of marine fluorescent organic matter (FOM) using high-resolution spatial data, in situ fluorometers have been used in the open ocean. In this study, we measured FOM during the Global Ocean Ship-based Hydrographic Investigations Program (GO-SHIP) expedition from early December 2019 to early February 2020, using an in situ fluorometer at 148 stations along the two meridional transects (at ∼80 and ∼57°E) in the Indian Ocean, covering latitudinal ranges from ∼6°N to ∼20°S and ∼30 to ∼65°S, respectively. The FOM data obtained from the fluorometer were corrected for known temperature dependence and calibrated using FOM data measured onboard by a benchtop fluorometer. Using the relative water mass proportions estimated from water mass analyses, we determined the intrinsic values of FOM and apparent oxygen utilization (AOU) for each of the 12 water masses observed. We then estimated the basin-scale relationship between the intrinsic FOM and the AOU, as well as the turnover time for FOM in the Indian Ocean (410 ± 19 years) in combination with the microbial respiration rate in the dark ocean (>200 m). Consistent to previous estimates in the global tropical and subtropical ocean, the FOM turnover time obtained is of the same order of magnitude as the circulation age of the Indian Ocean, indicating that the FOM is refractory and is a sink for reduced carbon in the dark ocean. A decoupling of FOM and AOU from the basin-scale relationship was also observed in the abyssal waters of the northern Indian Ocean. The local variability may be explained by the effect of sinking organic matter altered by denitrification through the oxygen-deficient zone on enhanced abyssal FOM production relative to oxygen consumption.

Dark Ocean: Maritime Disasters in the Modern Age

In the past decade, a trio of violent storms in the North Atlantic has led to terrifying and tragic encounters between large oceangoing vessels and extreme weather (Figure 1). In an era of technolo...

Potential virus-mediated nitrogen cycling in oxygen-depleted oceanic waters

Viruses play an important role in the ecology and biogeochemistry of marine ecosystems. Beyond mortality and gene transfer, viruses can reprogram microbial metabolism during infection by expressing auxiliary metabolic genes (AMGs) involved in photosynthesis, central carbon metabolism, and nutrient cycling. While previous studies have focused on AMG diversity in the sunlit and dark ocean, less is known about the role of viruses in shaping metabolic networks along redox gradients associated with marine oxygen minimum zones (OMZs). Here, we analyzed relatively quantitative viral metagenomic datasets that profiled the oxygen gradient across Eastern Tropical South Pacific (ETSP) OMZ waters, assessing whether OMZ viruses might impact nitrogen (N) cycling via AMGs. Identified viral genomes encoded six N-cycle AMGs associated with denitrification, nitrification, assimilatory nitrate reduction, and nitrite transport. The majority of these AMGs (80%) were identified in T4-like Myoviridae phages, predicted to infect Cyanobacteria and Proteobacteria, or in unclassified archaeal viruses predicted to infect Thaumarchaeota. Four AMGs were exclusive to anoxic waters and had distributions that paralleled homologous microbial genes. Together, these findings suggest viruses modulate N-cycling processes within the ETSP OMZ and may contribute to nitrogen loss throughout the global oceans thus providing a baseline for their inclusion in the ecosystem and geochemical models.

Relative Importance of Phosphodiesterase vs. Phosphomonoesterase (Alkaline Phosphatase) Activities for Dissolved Organic Phosphorus Hydrolysis in Epi- and Mesopelagic Waters

Marine microbes use extracellular phosphatases to hydrolyse phosphate from organic matter. Dissolved organic phosphorus (DOP) is typically present in higher concentrations than phosphate in oceanic surface waters. Yet, the fate and role of different DOP components, such as phosphomonoester and phosphodiester, are poorly understood. Most of the investigations on extracellular enzymatic hydrolysis of marine DOP have focused on phosphomonoesterase (MEA) activity (i.e., alkaline phosphatase), whereas phosphodiesterase (DEA) measurements are scarce. This limits our understanding of the ecological and biogeochemical role of DOP sources other than P-monoesters in the sea. We determined extracellular MEA and DEA activities including their cell-free fractions on a bimonthly basis over 14 months in surface and mesopelagic subantarctic waters, thus covering a wide range of phosphate availability levels (from <0.5 to 2.3 µM). We found that DEA and MEA exhibit similar hydrolysis rates in surface as well as in mesopelagic waters. The MEA : DEA ratio varied between 0.38 and 5.42 during the study period, indicating potential differences in function and/or expression among the two enzyme groups, potentially reflecting differences in the availability and/or utilization of P-monoester and P-diester pools. Interestingly, the MEA : DEA was negatively correlated to phosphate (r=-0.82, p=0.02, R2=0.67) and positively with N:P (r=0.84, p=0.02, R2=0.67), suggesting that the relative importance of DEA versus MEA is linked to inorganic P availability and the N : P ratio. DEA was also related to the N : P ratio, both at the surface and at depth, suggesting DEA alone is sensitive to changes in the N : P ratio. The majority (>70%) of extracellular MEA and DEA was found in the cell-free fraction which increased with depth. Our results indicated that DOP hydrolysis mediated by DEA in the surface as well as in dark ocean is as important as the frequently measured MEA.

Laterally Transported Particles From Margins Serve as a Major Carbon and Energy Source for Dark Ocean Ecosystems

AbstractDeep ocean microorganisms consume particulate organic matter that is produced in the surface ocean and exported to deeper depths. Such consumption not only enriches inorganic carbon in the deep ocean but also transforms organic carbon into recalcitrant forms, creating an alternative type of carbon sequestration. However, estimates of deep microbial carbon demand substantially exceed the available particulate organic carbon exported from the euphotic zone, resulting in an unbalanced dark ocean carbon budget. Here, we combined field‐based microbial activity parameters, integrated multiyear particle export flux data, sinking particle fluxes measured by sediment traps, and optical data from Biogeochemical‐Argo floats to quantify the main sources of organic carbon to the dark ocean. Laterally transported particles (including sinking and suspended particles) serve as a major energy source, which directly provide organic carbon and enhance new organic carbon production by dark carbon fixation, reconciling the mismatch in the regional carbon budget.

Variability in Water-Column Respiration and Its Dependence on Organic Carbon Sources in the Canary Current Upwelling Region

Plankton respiration (R) is a key factor governing the ocean carbon cycle. However, although the ocean supports respiratory activity throughout its entire volume, to our knowledge there are no studies that tackle both the spatial and temporal variability of respiration in the dark ocean and its dependence on organic carbon sources. Here, we have studied the variability of epipelagic and mesopelagic R via the enzymatic activity of the electron transport system (ETS) in microbial communities, along two zonal sections (21°N and 26°N) extending from the northwest African coastal upwelling to the open-ocean waters of the North Atlantic subtropical gyre, during the fall 2002 and the spring 2003. Overall, integrated R in epipelagic (Repi; 0-200 m) waters, was similar during the two periods, while integrated mesopelagic respiration (Rmeso; 200-1000 m) was >25% higher in the fall. The two seasons, however, exhibited contrasting zonal and meridional patterns of ETS distribution in the water column, largely influenced by upwelling effects and associated mesoscale variability. Multiple linear regression between average R and average concentrations of dissolved organic carbon (DOC) and slow-sinking (suspended) particulate organic carbon (POCsus) indicates that POCsus is the main contributor to Rmeso, supporting previous results in the same area. Rmeso exceeded satellite-derived net primary production (NPP) at all stations except at the most coastal ones, with the imbalance increasing offshore. Moreover, the export flux of sinking POC collected at 200 m with sediment traps, represented on average less than 6% of the NPP. All this indicates that Rmeso depends largely on small particles with low sinking rates, which would be laterally advected at mid water depths from the continental margin towards the open ocean, or transported by mesoscale features from the surface to the mesopelagic ocean, providing support to inferences from modeling studies in the region.

Particulate Organic Carbon Deconstructed: Molecular and Chemical Composition of Particulate Organic Carbon in the Ocean

The dynamics of the particulate organic carbon (POC) pool in the ocean are central to the marine carbon cycle. POC is the link between surface primary production, the deep ocean, and sediments. The rate at which POC is degraded in the dark ocean can impact atmospheric CO2 concentration. Therefore, a central focus of marine organic geochemistry studies is to improve our understanding of POC distribution, composition, and cycling. The last few decades have seen improvements in analytical techniques that have greatly expanded what we can measure, both in terms of organic compound structural diversity and isotopic composition, and complementary molecular omics studies. Here we provide a brief overview of the autochthonous, allochthonous, and anthropogenic components comprising POC in the ocean. In addition, we highlight key needs for future research that will enable us to more effectively connect diverse data sources and link the identity and structural diversity of POC to its sources and transformation processes.

Mesonia oceanica sp. nov., isolated from oceans during the Tara oceans expedition, with a preference for mesopelagic waters.

Strain ISS653T, isolated from Atlantic seawater, is a yellow pigmented, non-motile, Gram-reaction-negative rod-shaped bacterium, strictly aerobic and chemoorganotrophic, slightly halophilic (1-15 % NaCl) and mesophilic (4-37 °C), oxidase- and catalase-positive and proteolytic. Its major cellular fatty acids are iso-C15 : 0, iso-C15 : 0 2-OH, and iso-C17 : 0 3-OH; the major identified phospholipid is phosphatidylethanolamine and the major respiratory quinone is MK6. Genome size is 4.28 Mbp and DNA G+C content is 34.9 mol%. 16S rRNA gene sequence similarity places the strain among members of the family Flavobacteriaceae, with the type strains of Mesonia phycicola (93.2 %), Salegentibacter mishustinae (93.1 %) and Mesonia mobilis (92.9 %) as closest relatives. Average amino acid identity (AAI) and average nucleotide identity (ANI) indices show highest values with M. mobilis (81 % AAI; 78.9 % ANI), M. phycicola (76 % AAI; 76.3 % ANI), Mesonia maritima (72 % AAI, 74.9 % ANI), Mesonia hippocampi (64 % AAI, 70.8 % ANI) and Mesonia algae (68 % AAI; 72.2 % ANI). Phylogenomic analysis using the Up-to-date-Bacterial Core Gene set (UBCG) merges strain ISS653T in a clade with species of the genus Mesonia. We conclude that strain ISS653T represents a novel species of the genus Mesonia for which we propose the name Mesonia oceanica sp. nov., and strain ISS653T (=CECT 9532T=LMG 31236T) as the type strain. A second strain of the species, ISS1889 (=CECT 30008) was isolated from Pacific Ocean seawater. Data obtained throughout the Tara oceans expedition indicate that the species is more abundant in the mesopelagic dark ocean than in the photic layer and it is more frequent in the South Pacific, Indian and North Atlantic oceans.

Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean.

The Thaumarchaeota is a diverse archaeal phylum comprising numerous lineages that play key roles in global biogeochemical cycling, particularly in the ocean. To date, all genomically characterized marine thaumarchaea are reported to be chemolithoautotrophic ammonia oxidizers. In this study, we report a group of putatively heterotrophic marine thaumarchaea (HMT) with small genome sizes that is globally abundant in the mesopelagic, apparently lacking the ability to oxidize ammonia. We assembled five HMT genomes from metagenomic data and show that they form a deeply branching sister lineage to the ammonia-oxidizing archaea (AOA). We identify this group in metagenomes from mesopelagic waters in all major ocean basins, with abundances reaching up to 6% of that of AOA. Surprisingly, we predict the HMT have small genomes of ∼1 Mbp, and our ancestral state reconstruction indicates this lineage has undergone substantial genome reduction compared to other related archaea. The genomic repertoire of HMT indicates a versatile metabolism for aerobic chemoorganoheterotrophy that includes a divergent form III-a RuBisCO, a 2M respiratory complex I that has been hypothesized to increase energetic efficiency, and a three-subunit heme-copper oxidase complex IV that is absent from AOA. We also identify 21 pyrroloquinoline quinone (PQQ)-dependent dehydrogenases that are predicted to supply reducing equivalents to the electron transport chain and are among the most highly expressed HMT genes, suggesting these enzymes play an important role in the physiology of this group. Our results suggest that heterotrophic members of the Thaumarchaeota are widespread in the ocean and potentially play key roles in global chemical transformations.IMPORTANCE It has been known for many years that marine Thaumarchaeota are abundant constituents of dark ocean microbial communities, where their ability to couple ammonia oxidation and carbon fixation plays a critical role in nutrient dynamics. In this study, we describe an abundant group of putatively heterotrophic marine Thaumarchaeota (HMT) in the ocean with physiology distinct from those of their ammonia-oxidizing relatives. HMT lack the ability to oxidize ammonia and fix carbon via the 3-hydroxypropionate/4-hydroxybutyrate pathway but instead encode a form III-a RuBisCO and diverse PQQ-dependent dehydrogenases that are likely used to conserve energy in the dark ocean. Our work expands the scope of known diversity of Thaumarchaeota in the ocean and provides important insight into a widespread marine lineage.

Characteristics and implications of isoprenoid and hydroxy tetraether lipids in hadal sediments of Mariana and Yap Trenches

As one of the least-explored regions on Earth, the hadal zone remains poorly understood in terms of sedimentary organic geochemistry. This study examined the composition of isoprenoid glycerol dialkyl glycerol tetraethers (Iso-GDGTs) and hydroxy GDGTs (OH-GDGTs) in sediment cores with water depths ranging from 5058 to 10,911 m from the Mariana and Yap Trenches. The results showed a higher proportion of GDGT-0 (25–73%, mean = 49%) in the trench Iso-GDGTs pool than those from shallower ocean counterparts (<5000 m). Properties, including higher values of the [GDGT-2/GDGT-3] ratio (7.17–20.03, mean = 13.02) and the [GDGT-0/Crenarchaeol] ratio (0.49–3.94, mean = 1.48), as well as a dominance of OH-GDGT-0 in the OH-GDGTs, are similar to characteristics observed in other cold deep marine environments rather than tropical shallow ocean. Ring Index decreased with increasing water depth of the sampling sites, corresponding with increased fractional abundance of acyclic Iso-GDGTs and OH-GDGTs. Paleothermometer TEX86 in the surface sediments (>5000 m) revealed a significant negative linear correlation with water depth (TEX86H: R2 = 0.89, p < 0.01; TEX86L: R2 = 0.89, p < 0.01), leading to a bias toward lower proxy-derived temperatures. This is likely due to the increased incorporation of cold- and pressure- adapted species of archaea in dark ocean. Overall, this study provided implications of the extreme water depth effect on the distribution of isoprenoid and hydroxy tetraether lipids, as well as the proxy application in hadal environments.

Prokaryotic Response to Phytodetritus-Derived Organic Material in Epi- and Mesopelagic Antarctic Waters.

Particulate organic matter (POM) export represents the underlying principle of the biological carbon pump, driving the carbon flux from the sunlit to the dark ocean. The efficiency of this process is tightly linked to the prokaryotic community, as >70% of POM respiration is carried out by particle-associated prokaryotes. In the Ross Sea, one of the most productive areas of the Southern Ocean, up to 50% of the surface primary production is exported to the mesopelagic ocean as POM. Recent evidence suggests that a significant fraction of the POM in this area is composed of intact phytoplankton cells. During austral summer 2017, we set up bottle enrichment experiments in which we amended free-living surface and deep prokaryotic communities with organic matter pools generated from native microplankton, mimicking the particle export that may derive from mild (1 μg of Chlorophyll a L–1) and intense (10 μg of Chlorophyll a L–1) phytoplankton bloom. Over a course of 4 days, we followed free-living and particle-attached prokaryotes’ abundance, the degradation rates of polysaccharides, proteins and lipids, heterotrophic production as well as inorganic carbon utilization and prokaryotic community structure dynamics. Our results showed that several rare or undetected taxa in the initial community became dominant during the time course of the incubations and that different phytodetritus-derived organic matter sources induced specific changes in microbial communities, selecting for peculiar degradation and utilization processes spectra. Moreover, the features of the supplied detritus (in terms of microplankton taxa composition) determined different colonization dynamics and organic matter processing modes. Our study provides insights into the mechanisms underlying the prokaryotic utilization of phytodetritus, a significant pool of organic matter in the dark ocean.

Viral infection of prokaryotic plankton during early formation of the North Atlantic Deep Water

Viral abundance was assessed in different water masses of the NW Atlantic, and the development of viral abundance, lytic viral infection and lysogeny was followed for the first ca. 5000 km (corresponding to ca. 50 yr in the oceanic conveyor belt) of the western branch of the North Atlantic Deep Water (NADW). Viral abundance was significantly higher in the 100 m layer than in the NADW (2400-2700 m depth) and the Denmark Strait Overflow Water (2400-3600 m depth). The virus-to-prokaryote ratio (VPR) increased with depth, ranging from 32-43 for different water masses of the bathypelagic ocean, thus corroborating the enigma of high viral abundance in the dark ocean. The O2-minimum layer (250-600 m) also showed high viral abundance and VPRs. Viral abundance, a viral subgroup and VPRs decreased in a non-linear form with distance from the NADW origin. Viral production (range: 0.2-2.4 × 107 viruses l-1) and the fraction of lytically infected cells (range: 1-22%) decreased with increasing distance from the formation site of the NADW. Conservative estimations of virus-mediated mortality of prokaryotes in the NADW averaged 20 ± 12%. The fraction of the prokaryotic community with lysogens (i.e. harboring a functional viral DNA) in the NADW averaged 21 ± 14%. Hence, we conclude that (1) viral abundance and subgroups differ between water masses, (2) virus-mediated mortality of prokaryotes as well as lysogeny are significant in the dark ocean and (3) the lysogenic life strategy became more important than the lytic life style during the early formation of the NADW.

The Dark Ocean Is Full of Lights

The Dark Ocean Is Full of Lights

Coupling Between Carbon and Nitrogen Metabolic Processes Mediated by Coastal Microbes in Synechococcus-Derived Organic Matter Addition Incubations.

Phytoplankton are major contributors to labile organic matter in the upper ocean. Diverse heterotrophic bacteria successively metabolize these labile compounds and drive elemental biogeochemical cycling. We investigated the bioavailability of Synechococcus-derived organic matter (SOM) by estuarine and coastal microbes during 180-day dark incubations. Variations in organic carbon, inorganic nutrients, fluorescent dissolved organic matter (FDOM), and total/active microbial communities were monitored. The entire incubations could be partitioned into three phases (labeled I, II, and III) based on the total organic carbon (TOC) consumption rates of 6.38–7.01, 0.53–0.64, and 0.10–0.13 μmol C L–1 day–1, respectively. This corresponded with accumulation processes of NH4+, NO2–, and NO3–, respectively. One tryptophan-like (C1) and three humic-like (C2, C3, and C4) FDOM components were identified. The intensity variation of C1 followed bacterial growth activities, and C2, C3, and C4 displayed labile, semi-labile, and refractory DOM characteristics, respectively. Alphaproteobacteria, Gammaproteobacteria, Bacteroidetes, and Actinobacteria dominated the quickly consumed process of SOM (phase I) coupled with a substantial amount of NH4+ generation. Thaumarchaeota became an abundant population with the highest activities in phase II, especially in the free-living size-fraction, and these organisms could perform chemoautotroph processes through the ammonia oxidation. Microbial populations frequently found in the dark ocean, even the deep sea, became abundant during phase III, in which Nitrospinae/Nitrospirae obtained energy through nitrite oxidation. Our results shed light on the transformation of different biological availability of organic carbon by coastal microorganisms which coupled with the regeneration of different form of inorganic nitrogen.

Carbon recycling efficiency and phosphate turnover by marine nitrifying archaea.

Thaumarchaeotal nitrifiers are among the most abundant organisms in the ocean, but still unknown is the carbon (C) yield from nitrification and the coupling of these fluxes to phosphorus (P) turnover and release of metabolites from the cell. Using a dual radiotracer approach, we found that Nitrosopumilus maritimus fixed roughly 0.3 mol C, assimilated 2 mmol P, and released ca. 10-2 mol C and 10-5 mol P as dissolved organics (DOC and DOP) per mole ammonia respired. Phosphate turnover may influence assimilation fluxes by nitrifiers in the euphotic zone, which parallel those of the dark ocean. Collectively, marine nitrifiers assimilate up to 2 Pg C year-1 and 0.05 Pg P year-1 and thereby recycle roughly 5% of mineralized C and P into marine biomass. Release of roughly 50 Tg DOC and 0.2 Tg DOP by thaumarchaea each year represents a small but fresh input of reduced substrates throughout the ocean.