Introduction

Most of the DOC in the ocean is produced by marine organisms and removed by abiotic processes, such as photochemical oxidation1,2 and microbial degradation3. DOC is a highly complex mixture of compounds4, each having a different reactivity. Although DOC plays an important role in global carbon cycling5,6,7, the mechanisms underlying the production and removal of DOC have yet to be clarified4. The objective of this study was to examine the degradation rate of DOC in a very cold deep ocean (EJS), which may infer the sensitivity of DOC storage capacity in warming oceans.

The EJS is a semi-enclosed marginal sea and is divided into three major basins (Japan Basin, Ulleung Basin and Yamato Basin), all of which are deeper than 2000 m (Fig. 1). The deep water masses (at depths greater than 1000 m) in the EJS are formed by deep convection or brine rejection in the Japan Basin8,9,10,11. Using salinity and oxygen isotope budgets9, the rate of potential bottom-water formation due to brine rejection (at depths greater than 2500 m) was estimated to be approximately 4 × 1012 m3 yr−1. This brine rejection accounts for 25–35% of the subsurface water formed in the EJS. The turnover time of the EJS deep water mass was determined to be ~100 years by using radionuclides such as 14C and 226Ra12,13 by assuming steady-state conditions.

Figure 1
figure 1

A map showing sampling stations for vertical dissolved organic carbon (DOC) profiles in the East/Japan Sea.

Seawater samples for DOC analysis were collected with a Niskin sampler from 30 stations in the southern area and from 15 stations in the northern area of the EJS. The hydrological and biogeochemical surveys were conducted during four periods: May 8 to 22, 2007, on board the R/V M.A. Gagarinsky of the Pacific Oceanological Institute (POI), Russia; May 28 to June 2, 2007, onboard the R/V Tam-Yang of the Pukyung National University (PKNU), Korea; August 4 to 14, 2008, onboard the R/V HaeYang 2000 of the National Oceanographic Research Institute (NORI), Korea; and July 9 to 18, 2009, on board the R/V M.A. Lavrentyev of the POI, Russia. Map was created using Adobe Illustrator.

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Results and Discussion

Vertical profiles of DOC concentration were determined on several cruises covering the main EJS during the course of three years (Fig. 1). The average DOC concentrations in the surface layer (0–200 m) and in the deep (>200 m) layer over the entire area of the EJS were 68 ± 6 and 58 ± 4 μM, respectively (Fig. 2). In general, the DOC concentrations in the surface layer of EJS were comparable to those in the major world oceans (60–80 μM)14,15,16. However, the DOC concentrations in the deep layer of the EJS are significantly higher than those in the major oceans (34–43 μM)6,17,18 (Fig. 2) and slightly higher than or similar to those in the Arctic Ocean (54 ± 3 μM, up to ~4000 m)19 and the Nordic seas (50 μM, up to ~3500 m)20, where deep water formation occurs. In the Greenland Sea, one of the Nordic seas, the concentrations of DOC decrease from the surface (60 μM) to the deep layer (53 μM, <1500 m depth) and reach a constant DOC concentration (50 μM) in the deeper layer (>1500 m depth)20. Therefore, the concentration of DOC in the deep bottom water of the EJS seems to be the highest reported so far in the world oceans.

Figure 2
figure 2

Vertical profiles of dissolved organic carbon (DOC), potential temperature and δ13C-DOC.

(a–c) Vertical profiles of (a) DOC, (b) potential temperature and (c) δ13C-DOC in the East/Japan Sea (open circle), North Pacific (black lines), North Atlantic (black dotted lines) and Mediterranean Sea (gray dotted lines). Data in the North Pacific, North Atlantic and Mediterranean Sea are from Hawaii Ocean Time-series (HOT), Bermuda Atlantic Time-series (BATS) and Santinelli et al. (ref. 26), respectively. Samples for δ13C-DOC in the East/Japan Sea were collected in station 10 (42 °N). The depth profiles of δ13C-DOC in the major oceans are from the North Central Pacific (31 °N) and the Sargasso Sea (31 °N).

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In the Arctic and Nordic Seas, the elevated concentrations of DOC are related to downwelling of waters that are enriched in terrigenous DOC19,20. However, there is no large river that directly drains into the EJS. In addition, export of DOC in the deep EJS to the Pacific Ocean can be ignored since the EJS is connected to the Pacific Ocean only through the sills which are shallower than 150 m. The δ13C-DOC in the EJS ranged from −20.4 to −21.7% (avg.: −21.3 ± 0.4%), similar to that in the North Pacific (avg.: −21.2 ± 0.2%) and in the North Atlantic (avg.: −21.0 ± 0.3%) oceans21 (Fig. 2). The enriched δ13C values in these oceans are different from terrigenous C3 plant material (−28 to −30%) indicating that the main fraction of the DOM is of marine origin (δ13C values of plankton organic matter = −18 to −20%). However, we cannot exclude the possibility that the Tsushima Current, which brings Yangtze River water into the EJS, may contribute some terrigenous DOC to the EJS. In addition, the DOC production from sinking particulate organic carbon (POC) could result in high DOC in the EJS. However, despite most of the sinking POC (>80%) being generally degraded between 200 and 1600 m22, the DOC profiles were uniform throughout the entire depths, down to 3500 m, indicating that DOC production in the deep ocean is not significant over the time scale of deep water mixing. The total export production (including sinking particles) through 200 m in the EJS has been estimated to be 99 Tg yr−1 (8.25 mol C m−2 yr−1) by using 3H-3He isotopes22, which in general is not unusually higher than in other oceans.

The concentrations of DOC in the deep layer of the EJS in May 2007 decreased slightly from the north (59 ± 3 μM) to the south (55 ± 2 μM) along the deep-sea current flows, which was associated with biological degradation reflected in apparent oxygen utilization (AOU) (Fig. 3). Considering the fact that these DOC profiles include the entire East Sea through several cruises, including the southwestern EJS stations23, over the last 10 years, the DOC concentrations in the deep EJS were remarkably stable and neither systematic nor significant differences were observed among the stations.

Figure 3
figure 3

Transectional contours of dissolved organic carbon (DOC) and apparent oxygen utilization (AOU) in the East/Japan Sea.

Distributions of DOC and AOU in the East/Japan Sea during May 8 to 22, 2007 and May 28 to June 2, 2007. Red lines indicate distributions of DOC reported by Kim and Kim (ref. 23).

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In order to determine the characteristics of DOC degradation in the EJS, it was necessary to compare DOC degradation rates for the same DOM quality and the same age following deep water formation. In this connection, the degradation rate of DOC in the deep EJS was compared with those of the Atlantic Ocean and the Mediterranean Sea, which have similar deep water formation modes (thermohaline circulation). Because the turnover times of the EJS and Mediterranean Sea are about 100 years, we used the DOC difference in the entire regions of these marginal seas. In the case of the Atlantic Ocean, we used the difference in DOC concentration between the Greenland Sea water and the water mass around 50 °N, which was found to be approximately 100 years old based on 14C dating24.

The slopes of DOC concentrations over the time scale of 100 years were obtained from the highest (59, 50 and 48 μM) to the lowest (55, 42 and 34 μM) concentrations in the EJS, Atlantic Ocean25 and Mediterranean Sea26, respectively. A major fraction of the DOC mineralization was assumed to have occurred during downwelling. Then, the degradation rate of DOC was estimated to be 0.04, 0.08 and 0.14 μmol C kg−1 yr−1 in the EJS, Atlantic Ocean, and, Mediterranean Sea respectively. The degradation rate in the EJS is much lower than those of the Mediterranean Sea and the Atlantic Ocean.

In order to determine the contribution of DOC oxidation to oxygen consumption in deep EJS, DOC is plotted against AOU. The plotting was performed after converting AOU to carbon equivalents [AOU-Ceq (μM C) = AOU (μM O2) × 0.72]16. A ΔC/ΔO ratio of 0.72 was derived from the Redfield stoichiometry (C:O:N:P = 106:42:16:1)27. The slope (−0.13) of the linear regression of DOC concentration versus AOU-Ceq in the deep EJS indicates that oxidation of DOC is responsible for 13% of the oxygen utilization in the deep EJS. This value in the deep EJS is similar to that (14 ± 3%) in the North Atlantic Deep Water25, but much higher than that (approximately 32%) in the eastern Mediterranean Sea28.

The reason behind the low degradation rates remains speculative at this point, but it is most likely associated with the difference in water temperature. The water temperature in the EJS is <1 °C (Fig. 2), which is lower than that in the Atlantic Ocean (3 °C, range from 2.2–3.5 °C) and in the Mediterranean Sea (~13 °C, range from 12.8–13.7 °C). Carlson et al. (ref. 25) suggested that the degradation rates of DOC derived from single end-member and multiple linear regression models decrease exponentially as temperature decreases although temperature cannot be the sole control of DOC degradation. DOM quality other than temperature alone might control DOM degradation rates29,30,31.

The water temperature increased by 0.1–0.5 °C in the upper 1000 m and by 0.01 °C below 2000 m from the 1950s to 1996 in the EJS because of the recent slowdown in deep-water formation32. Similarly, the rate of anthropogenic CO2 accumulation in the deep layer of the EJS decreased considerably from 1992 to 2007 owing to the considerable weakening of the overturning circulation33. It is unknown whether this recent small change has resulted in DOC reduction in the deep EJS during the last few decades. However, our results from EJS in comparison with other seas suggest that global carbon cycles could be significantly affected by the warming and slow-down of water overturning in marginal seas.

Methods

The samples for DOC and δ13C-DOC were filtered onboard through a pre-combusted syringe glass-fiber filter (Whatman, 0.7 μm, 25 mm) into pre-combusted glass ampoules (550 °C for 5 h). The samples were then acidified to pH 2 with 6 M HCl and stored at 4 °C for preservation until further analysis. All sampling procedures were performed in a clean bench (class 100). The DOC concentrations were measured using a TOC-VCPH analyzer (Shimadzu, Japan), as described elsewhere34. Briefly, the acidified seawater sample was bubbled with high-purity air gas (purity: 99.999) to completely purge inorganic carbon species in the injection system. Carrier gas was passed at a controlled flow rate of 150 mL min−1. Three to five replicates (100 μL) for each sample were automatically injected into a combustion glass tube filled with a catalyst (Pt-coated Al) at 720 °C in a furnace. The organic matter present in the sample was oxidized on the catalyst to CO2. The evolved CO2 was measured by non-dispersive infrared detection (NDIR) by integrating peak area.

In order to determine DOC concentrations with high accuracy, it is necessary to reduce the system blank as low as possible. The blank run was continued until organic-free distilled water (DIW) was stable within the detection limit (<5 μM) of our DOC method. Six-point calibration curves for acetanilide were used daily for DOC standardization. The reliability of the measurements was verified on a daily basis by comparing the measured values with a DOC-certified seawater sample (DSR: 44–46 μM for DOC, University of Miami) and procedural blanks. Most of our DSR measurement results (n = 34, 92%) were in good agreement with the DSR values (within 2%), although three measured values differed by 3–5% from the DSR values. These DSR measurements were performed for every 10 samples. The average standard deviation value for all DSR measurements was ±1.2 μM, which is similar to the value (±1 μM) suggested by Carlson et al. (ref. 25). An inter-laboratory comparison between the two laboratories involved (Kim and Dittmar) confirmed the accuracy of measurements to be within 5%.

The stable isotope compositions of dissolved organic carbon (δ13C-DOC) were measured by using TOC-IR-MS (Isoprime IR-MS coupled with vario TOC cube), which is commercially available (Isoprime, Elementar). This instrument uses the common high temperature catalytic combustion method, which is the same principle as our DOC method. Briefly, 10 mL of filtered samples, following acidification to pH 2 with 6 M HCL, is placed into an auto-sampler. The instrument is programmed to purge the sample for 20–30 min with O2 gas to completely remove dissolved inorganic carbon species. Then, 1.5 mL of the sample is injected into Pt-impregnated silica spheres in a quartz tube, where DOC is fully converted to CO2 at 750 °C. The CO2 gas flows through a halogen trap and a water trap. After detecting DOC concentrations using an NDIR detector, CO2 gas enters the interface by O2 carrier gas. In the interface, a series of valves are set so that the flow from the TOC and the flow toward the IR-MS system can be separated. The CO2 gas, carried by O2 carrier gas, is trapped by CO2 column in the interface. After switching the valves, the trapped gas is released to IR-MS by helium carrier gas. After passing through a reduction furnace to remove any interfering species, including residual oxygen, CO2 gas is transferred to the IR-MS. The δ13C content of the CO2 is measured using Isoprime IR-MS.

The ion source parameters were fine-tuned every day and the variations of the reference gas were checked to maintain good stability (standard deviation: <0.01%). The blank was determined by running low carbon water (University of Miami), containing a DOC level lower than 2 μM before the analysis of each sample batch. Certified IAEA-CH6 sucrose (International Atomic Energy Agency, −10.45 ± 0.03%) dissolved in the low carbon water was used for standardization. For every 10 samples, one standard sample was measured to check the stability of measurements. The method used for blank determination and corrections followed the previous method35,36. Our measurement result of δ13C-DOC for DSR was –21.5 ± 0.1%, which agree well with previous results reported by Lang et al. (ref. 37) (−21.7%) and by Panetta et al. (ref. 35) (−21.4 ± 0.3%). The samples were measured three times and the values were reproducible within 0.3%.

At all the stations, dissolved oxygen (DO), potential temperature and salinity were measured using a rosette system with a mounted CTD (SBE 911+). All DO data were from a CTD–DO sensor that was calibrated by the data from grab samples (measured on board using the Winkler titration method). AOU, determined from the same bottle as DOC concentration, was obtained by subtracting the measured DO concentration from the saturated DO concentration which is dependent on temperature and salinity. The temperature sensor used was a SBE–3/F thermometer (resolution 0.0003 °C). The probes were calibrated at Sea-Bird Electronics, USA, prior to each cruise. Reported error margins were standard errors. Wherever appropriate, error propagation was applied.

Additional Information

How to cite this article: Kim, T.-H. et al. Extraordinary slow degradation of dissolved organic carbon (DOC) in a cold marginal sea. Sci. Rep. 5, 13808; doi: 10.1038/srep13808 (2015).