Contributions of Vertically Migrating Metazoans to Sinking and Suspended Particulate Matter Fuel N2 Production in the Eastern Tropical North Pacific Oxygen Deficient Zone

Organic complexation of iron by strong ligands and siderophores in the eastern tropical North Pacific oxygen deficient zone

Iron (Fe) and copper (Cu) are essential cofactors for microbial metalloenzymes, but little is known about the metalloenyzme inventory of anaerobic marine microbial communities despite their importance to the nitrogen cycle. We compared dissolved O2, NO, NO, Fe and Cu concentrations with nucleic acid sequences encoding Fe and Cu-binding proteins in 21 metagenomes and 9 metatranscriptomes from Eastern Tropical North and South Pacific oxygen minimum zones and 7 metagenomes from the Bermuda Atlantic Time-series Station. Dissolved Fe concentrations increased sharply at upper oxic-anoxic transition zones, with the highest Fe:Cu molar ratio (1.8) occurring at the anoxic core of the Eastern Tropical North Pacific oxygen minimum zone and matching the predicted maximum ratio based on data from diverse ocean sites. The relative abundance of genes encoding Fe-binding proteins was negatively correlated with O2, driven by significant increases in genes encoding Fe-proteins involved in dissimilatory nitrogen metabolisms under anoxia. Transcripts encoding cytochrome c oxidase, the Fe- and Cu-containing terminal reductase in aerobic respiration, were positively correlated with O2 content. A comparison of the taxonomy of genes encoding Fe- and Cu-binding vs. bulk proteins in OMZs revealed that Planctomycetes represented a higher percentage of Fe genes while Thaumarchaeota represented a higher percentage of Cu genes, particularly at oxyclines. These results are broadly consistent with higher relative abundance of genes encoding Fe-proteins in the genome of a marine planctomycete vs. higher relative abundance of genes encoding Cu-proteins in the genome of a marine thaumarchaeote. These findings highlight the importance of metalloenzymes for microbial processes in oxygen minimum zones and suggest preferential Cu use in oxic habitats with Cu > Fe vs. preferential Fe use in anoxic niches with Fe > Cu.

Iron and manganese accumulation within the Eastern Tropical North Pacific oxygen deficient zone

Up to half of marine N losses occur in oxygen-deficient zones (ODZs). Organic matter flux from productive surface waters is considered a primary control on N2 production. Here we investigate the offshore Eastern Tropical North Pacific (ETNP) where a secondary chlorophyll a maximum resides within the ODZ. Rates of primary production and carbon export from the mixed layer and productivity in the primary chlorophyll a maximum were consistent with oligotrophic waters. However, sediment trap carbon and nitrogen fluxes increased between 105 and 150 m, indicating organic matter production within the ODZ. Metagenomic and metaproteomic characterization indicated that the secondary chlorophyll a maximum was attributable to the cyanobacterium Prochlorococcus, and numerous photosynthesis and carbon fixation proteins were detected. The presence of chemoautotrophic ammonia-oxidizing archaea and the nitrite oxidizer Nitrospina and detection of nitrate oxidoreductase was consistent with cyanobacterial oxygen production within the ODZ. Cyanobacteria and cyanophage were also present on large (>30 μm) particles and in sediment trap material. Particle cyanophage-to-host ratio exceeded 50, suggesting that viruses help convert cyanobacteria into sinking organic matter. Nitrate reduction and anammox proteins were detected, congruent with previously reported N2 production. We suggest that autochthonous organic matter production within the ODZ contributes to N2 production in the offshore ETNP.

An N isotopic mass balance of the Eastern Tropical North Pacific oxygen deficient zone

ABSTRACTOxygen deficient zones (ODZs) are subsurface marine systems that harbour distinct microbial communities, including populations of the picocyanobacteria Prochlorococcus that can form a secondary chlorophyll maximum (SCM), and low‐oxygen tolerant strains of the globally abundant heterotroph Pelagibacter (SAR11). Yet, the small labile molecules (metabolites) responsible for maintaining these ODZ communities are unknown. Here, we compared the metabolome of an ODZ to that of an oxygenated site by quantifying 87 metabolites across depth profiles in the eastern tropical North Pacific ODZ and the oxygenated waters of the North Pacific Gyre. Metabolomes were largely consistent between anoxic and oxic water columns. However, the osmolyte glycine betaine (GBT) was enriched in the oxycline and SCM of the ETNP, comprising as much as 1.2% of particulate organic carbon. Transcriptomes revealed two active GBT production pathways, glycine methylation (SDMT/bsmB) expressed by Prochlorococcus and choline oxidation (betB) expressed by Gammaproteobacteria. GBT consumption through demethylation involved diverse microbial taxa, with SAR11 contributing nearly half of the transcripts for the initial step of GBT demethylation (BHMT), which is predicted to convert GBT and homocysteine into dimethylglycine and methionine, a compound SAR11 cannot otherwise produce. Thus, GBT connects the metabolisms of the dominant phototroph and heterotroph in the oceans.

Lack of redox cycling for nickel in the water column of the Eastern tropical north pacific oxygen deficient zone: Insight from dissolved and particulate nickel isotopes

Naturally existing stable carbon and nitrogen isotopes are important in the study of sedimentary organic matter sources. To identify the sources of sedimentary organic matter in Sanggou Bay and its adjacent areas, which is characterized by high-density shellfish and seaweed aquaculture, the grain size, organic carbon (OC), total nitrogen (TN), carbon and nitrogen isotopic composition (δ13C and δ15N) of organic matter in the surface sediment were determined. The results showed that, in August, sedimentary OC and TN ranged from 0.17% to 0.76% and 0.04% to 0.14%, respectively. In November, OC and TN ranged from 0.23% to 0.87% and 0.05% to 0.14%, respectively. There was a significant positive correlation between OC and TN (R=0.98, P<0.0001), indicating that OC and TN were homologous. In August, the δ13C and δ15N of organic matter varied from −23.06‰ to −21.59‰ and 5.10‰ to 6.31‰, respectively. In November, δ13C and δ15N ranged from −22.87‰ to −21.34‰ and 5.13‰ to 7.31‰, respectively. This study found that the major sources of sedimentary organic matter were marine shellfish biodeposition, seaweed farming, and soil organic matter. Using a three-end-member mixed model, we estimated that the dominant source of sedimentary organic matter was shellfish biodeposition, with an average contribution rate of 65.53% in August and 43.00% in November. Thus, shellfish farming had a significant influence on the coastal carbon cycle.

Changes in the intensity of the oxygen minimum zone (OMZ) in the eastern tropical North Pacific over the past 140 kyr are recorded as enrichments and depletions of redox‐sensitive metals in sediments of two piston cores, one within and one below the modern OMZ, from the continental margin off Mazatlán, Mexico (22°41′N, 106°28′W). Concentrations of Al (7.7 ± 0.6%), Ti (0.37 ± 0.03%), Fe (3.1 ± 0.25%), Mn (320 ± 31 ppm), and Ba (560 ± 82 ppm) in core NH15P (within the OMZ at 420 m water depth) were relatively constant over the last 110 kyr. In contrast, concentrations of Cd (4.8 ± 2 ppm), Cu (29.8 ± 9.1 ppm), U (9.1 ± 3.7 ppm), Mo (12.1 ± 5.0 ppm), V (138.2 ± 51.9 ppm), and Re (45.8 ± 25.5 ppb) were all at least 30% higher in interglacial stages compared to glacial stages. Concentrations of Al (7.4 ± 0.3%), Ti (0.35 ± 0.03%), Fe (3.5 ± 0.4%), and Mn (385 ± 77 ppm) in core NH22P (below the OMZ at 2025 m water depth) were comparable to those in core NH15P, while concentrations of Ba (1662 ± 292 ppm) were about a factor of three higher. In contrast, concentrations of Cd (0.9 ± 0.3 ppm), U (6.6 ± 0.9 ppm), Mo (3.2 ± 1.2 ppm), V (81.8 ± 10.1 ppm), and Re (25.4 ± 12 ppb) were lower in sediments of comparable age than the concentrations of these same metals in the OMZ core, and the differences in their concentrations over glacial‐interglacial cycles were less pronounced than those in shallower core. Comparison of the nonlithogenic fraction of metals in the sediments with their estimated contribution from plankton suggests that organic matter is probably the major source of Cu, Ba, and perhaps Cd to the sediment, whereas the indirect effects of organic carbon and low bottom water oxygen concentrations on sediment redox state appear to be more important controls on the distributions U, Re, Mo, and V. Changes in the depth at which Re and Mo precipitated in the sediments and in the Re/Mo ratio suggest that the redox state of the surface sediment and overlying water at both core depths varied over time. Re and Mo removal depths were shallower and Re/Mo ratios were lower at the OMZ site than in deeper water, suggesting that a more reducing environment prevailed over time at the shallower site. Although the redox state of the waters and sediment at both sites varied over glacial‐interglacial cycles, the OMZ likely was never anoxic in the last 140 kyr. This variability in redox state could be attributed to changes in regional export productivity, changes in ocean circulation, or a combination of both processes. A paleoproductivity reconstruction from biogenic Ba data suggests that glacial productivity was considerable lower than it was during interglacial stages. Model results suggest that the oxygen penetration depth, an indicator of sediment redox state, changed less than 1 cm as a result of the change in productivity. Changes in oxygen penetration depth estimated from Re and U removal depths are significantly larger, suggesting that changes in ventilation are a more important control on sediment redox state. Overall, trace metal results confirm the tight coupling between ocean circulation, marine productivity, and global change.

Previous work estimating the N2excess above background due to denitrification has suggested that nitrate deficit‐type methods may be an underestimate of fixed nitrogen (N) loss in the major oxygen deficient zones of the ocean. The N2excess approach has the advantage over nitrate deficit‐type methods in that it does not depend on stoichiometric assumptions of fixed N to phosphate or oxygen utilization and avoids any uncertainly regarding the pathway of N loss. Measurements of N2:Ar from two stations within the eastern tropical North Pacific and from one station within the Arabian Sea oxygen deficient zones were used to determine the N2 excess due to denitrification. In both of the regions, the N2 excess was comparable in shape and magnitude to the concurrent fixed nitrogen deficit. In the eastern tropical North Pacific oxygen deficient zone, the N2 excess was near zero at the surface and rose to maxima of 13.7 ± 1.8 and 10.8 ± 1.9 μM N, compared to maximum fixed N deficits of 13.5 ± 1.5 and 12.3 ± 1.5 μM N, respectively. In the Arabian Sea oxygen deficient zone, the maximum N2 excess was 11.1 ± 1.5 μM N, compared to a maximum deficit of 12.5 ± 1.0 μM N. These results suggests that previous estimates of fixed N loss based on fixed N deficit calculations in these regions are likely reasonable, given the same considerations of volume and residence time of the water of the oxygen deficient zone.

Limited iodate reduction in shipboard seawater incubations from the Eastern Tropical North Pacific oxygen deficient zone

Carbon and nitrogen stable isotope compositions (δ13C and δ15N) of organic matter (OM) and total organic carbon to total nitrogen ratio (Corg/TN) in a sediment core collected in Sagua estuary (Cuba), were investigated to elucidate the origin of the Sedimentary OM (SOM) and changes in its main sources, over the last 100 years. Results showed almost constant values in the elemental and isotope composition of SOM from 1908 to 1970 with an abrupt change after 1970. From 1970 to 2005, δ13C increased from -21.2 up to -19.3 ‰, while δ15N declined from 1.5 to values close to 0 ‰. The output of the mass-balance model for the identification of OM sources indicated that δ13C and Corg/TN values are generally influenced by marine Particulate OM (POM) sources. Between 1900 and 1970, the main OM source in sediments was marine POM (>85 %), with freshwater POM contributing ca. 15%. Since 1970, the establishment of the Alacranes Dam determined drastic environmental changes influencing the OM sources in the area. Mixing models pointed to seagrasses (79 %) as the main contributors to SOM in the first period, while since 1973 onward, the contribution of human-derived sources such as fertilizers and urban discharges became greater. This information can provide baseline data for the environmental management of the Sagua watershed.

Distribution and sources of particulate organic matter in a mesoscale eddy dipole in the Mozambique Channel (south-western Indian Ocean): Insight from C and N stable isotopes

BackgroundCyanophages, viruses that infect cyanobacteria, are globally abundant in the ocean’s euphotic zone and are a potentially important cause of mortality for marine picocyanobacteria. Viral host genes are thought to increase viral fitness by either increasing numbers of genes for synthesizing nucleotides for virus replication, or by mitigating direct stresses imposed by the environment. The encoding of host genes in viral genomes through horizontal gene transfer is a form of evolution that links viruses, hosts, and the environment. We previously examined depth profiles of the proportion of cyanophage containing various host genes in the Eastern Tropical North Pacific Oxygen Deficient Zone (ODZ) and at the subtropical North Atlantic (BATS). However, cyanophage host genes have not been previously examined in environmental depth profiles across the oceans.MethodologyWe examined geographical and depth distributions of picocyanobacterial ecotypes, cyanophage, and their viral-host genes across ocean basins including the North Atlantic, Mediterranean Sea, North Pacific, South Pacific, and Eastern Tropical North and South Pacific ODZs using phylogenetic metagenomic read placement. We determined the proportion of myo and podo-cyanophage containing a range of host genes by comparing to cyanophage single copy core gene terminase (terL). With this large dataset (22 stations), network analysis identified statistical links between 12 of the 14 cyanophage host genes examined here with their picocyanobacteria host ecotypes.ResultsPicyanobacterial ecotypes, and the composition and proportion of cyanophage host genes, shifted dramatically and predictably with depth. For most of the cyanophage host genes examined here, we found that the composition of host ecotypes predicted the proportion of viral host genes harbored by the cyanophage community. Terminase is too conserved to illuminate the myo-cyanophage community structure. Cyanophage cobS was present in almost all myo-cyanophage and did not vary in proportion with depth. We used the composition of cobS phylotypes to track changes in myo-cyanophage composition.ConclusionsPicocyanobacteria ecotypes shift with changes in light, temperature, and oxygen and many common cyanophage host genes shift concomitantly. However, cyanophage phosphate transporter gene pstS appeared to instead vary with ocean basin and was most abundant in low phosphate regions. Abundances of cyanophage host genes related to nutrient acquisition may diverge from host ecotype constraints as the same host can live in varying nutrient concentrations. Myo-cyanophage community in the anoxic ODZ had reduced diversity. By comparison to the oxic ocean, we can see which cyanophage host genes are especially abundant (nirA, nirC, and purS) or not abundant (myo psbA) in ODZs, highlighting both the stability of conditions in the ODZ and the importance of nitrite as an N source to ODZ endemic LLV Prochlorococcus.

Cyanophages encode host-derived genes that may increase their fitness. We examined the relative abundance of 18 host-derived cyanophages genes in metagenomes and viromes along depth profiles from the Eastern Tropical North Pacific Oxygen Deficient Zone (ETNP ODZ) where Prochlorococcus dominates a secondary chlorophyll maximum within the ODZ. Cyanophages at the oxic primary chlorophyll maximum encoded genes related to light and phosphate stress (psbA, psbD and pstS in T4-like and psbA in T7-like), but the proportion of cyanophage with these genes decreased with depth. The proportion of cyanophage with purine biosynthesis genes increased with depth in T4-like, but not T7-like cyanophages. No additional host-derived genes were found in deep T7-like cyanophages, suggesting that T4-like and T7-like cyanophages have different host-derived gene acquisition strategies, possibly linked to their different genome packaging mechanisms. In contrast to the ETNP, in the oxic North Atlantic T4-like cyanophages encoded psbA and pstS throughout the euphotic zone. Differences in pstS between the ETNP and the North Atlantic stations were consistent with differences in phosphate concentrations in those regimes. We suggest that the low proportion of cyanophage with psbA within the ODZ reflects the stably stratified low-light conditions occupied by their hosts, a Prochlorococcus ecotype endemic to ODZs.