Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone
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1 SUPPLEMENTARY INFORMATION DOI: /NGEO1739 Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone Tim Kalvelage, Gaute Lavik, Phyllis Lam, Sergio Contreras, Lionel Arteaga, Caroline Löscher, Andreas Oschlies, Aurélien Paulmier, Lothar Stramma and Marcel M. M. Kuypers Data interpolation Depth-integrated nutrient concentrations and N-cycling rates (calculated from mid-point averages) and modelled export production rates were interpolated using Ocean Data View 1. Bathymetry data were obtained from the National Geophysical Data Center ( Fluxes of N org The export of N org out of the OMZ to the deep ocean (depth >600 m) was calculated from modelled export production using a Martin-curve 2 : F = F 100 x (z/100) b. Here F is the flux of organic matter at the lower OMZ boundary (z) and F 100 is the flux at 100 m, which was assumed to equal the modelled export production rates. We adopted an attenuation coefficient (b) of 0.82 (ref. 3 ). Benthic N org -flux and -burial rates (depth 600 m) were derived from modelled NPP and estimates of organic matter sedimentation for the Peruvian upwelling system 4. The benthic N org -flux (N org -burial) was calculated as 22% (6%) and 11% (2%) of NPP for 300 m and m water depth, respectively. Remineralization of N org Ammonification of N org in the OMZ via NO reduction to NO 2 was calculated using the following stoichiometry: (CH 2 O) 106 (NH 3 ) 16 H 3 PO NO H + à 106 CO NH NO H 2 O + H 3 PO 4. Any N org remineralization that could not be attributed to NO - 3 reduction was assumed to occur via aerobic respiration: (CH 2 O) 106 (NH 3 ) 16 H 3 PO O H + à 106 CO NH H 2 O + H 3 PO 4. NATURE GEOSCIENCE 1
2 For our sampled area (~1.2x10 6 km²) we estimate aerobic remineralization of 5.2 Tg N org y -1. If we conservatively assume aerobic organic matter degradation to be restricted to the upper 10 m of the OMZ, heterotrophic oxic respiration of on average 0.58 µmol L -1 d -1 would be sufficient to remineralize those 5.2 Tg N org y -1. In accordance, Revsbech et al. 5 recently measured oxic microbial respiration of ~2 µmol L -1 d -1 (which can be largely attributed to heterotrophic activity) in the upper Peruvian OMZ. Oxygen consumption rates on the same order of magnitude were determined during M77-3 (Kalvelage et al. in prep.). We note that the amount of N org available for aerobic respiration in our budget is sensitive to the choice of the attenuation coefficient. Others have suggested a smaller b-value of ~0.36 for O 2 -deficient systems 6,7, which would result in an increased export of organic matter out of the OMZ and reduce our estimate of oxic N org remineralization in the OMZ by ~50%. Benthic N-flux estimates Sedimentary NH + 4, NO x and N 2 fluxes for the shelf and upper continental slope sediments ( 600 m) were calculated from benthic NO x fluxes measured off the coast of Peru and estimates of NO x partitioning between sedimentary denitrification, anammox and DNRA 8. Using reaction-diffusion modelling, Bohlen et al. 8 estimated roughly the following relative contributions to benthic NO x consumption in the shallow shelf ( 300 m) and upper slope ( m) sediments, respectively, at 11 S: DNRA: 70% and 30%; denitrification: 30% and 65%; anammox: 0% and 5%. The sediments from ~10-16 S are particularly C org -rich 9, which favour SO 2-4 reduction and thus DNRA by filamentous large sulphur bacteria 8. Hence, DNRA is likely of less importance in the sediments to the north and south of there. For the wider region, we assumed an average contribution of 50% ( 300 m) and 20% ( m) of DNRA to benthic NO x consumption and increased benthic denitrification accordingly. We adopted a flux of 3 mmol NO x m -2 d -1 ( 300 m) and 2 mmol NO x m -2 d -1 ( m) into the sediment to calculate the net release of NH + 4 (via DNRA and N org ammonification) and N 2 -production due to anammox and denitrification. We
3 recognize that our estimates bear large uncertainties and further investigation on the northsouth variability of benthic NO x uptake and the partitioning between anammox, denitrification and DNRA is required to better constrain sedimentary N-fluxes off the coast of Peru. Nevertheless, our calculated sedimentary NO x flux of 1.7 Tg y -1 compares well with an earlier estimate (2 Tg N y -1 ) for a somewhat larger coastal area (0-25 S) 10. Lateral NO 3 - supply The lateral net transport of NO 3 - into the OMZ volume sampled was calculated from measured NO 3 - concentrations and shipboard ADCP (Acoustic Doppler Current Profiler) data obtained for the 3.58 S, 14 S and 85.83W sections. Water-column denitrification The sulfidic event on the Peruvian shelf, covered an area of ~10,000 km² at the time of our sampling. Chemolitotrophic denitrifiers achieve maximum energy yield when oxidizing H 2 S all the way to sulphate (SO 2-4 ) with NO - 3 : 8 NO HS H + à 4 N SO H 2 O Assuming a 100 m-thick H 2 S-containing layer above the shelf and a H 2 S concentration of on average 1 µmol L -1, results in a loss of ~0.02 Tg N due to chemolitotrophic denitrification. As part of the H 2 S is only partially oxidized (e.g. to S 0 ) or oxidized with NO - 2, O 2 and via DNRA (Schunk et al. in prep.), this should be considered an upper estimate. Even if we did not sample the prime of this sulfidic event and considering that accumulations of H 2 S remain often undetected, the associated annual N-losses are likely only a fraction of those due to anammox activity in the ETSP. Following pages: Supplementary Figure 1a-i Vertical distributions of O 2, nutrients and N-deficits.
4 Supplementary Figure 1a Zonal section at 3.58 S. 4
5 Supplementary Figure 1b Zonal section at 6 S. 5
6 Supplementary Figure 1c Zonal section at 10 S. 6
7 Supplementary Figure 1d Zonal section at 12 S. 7
8 Supplementary Figure 1e Zonal section at 14 S. 8
9 Supplementary Figure 1f Zonal section at 16 S. 9
10 Supplementary Figure 1g Cross-shelf section at ~18 S. 10
11 Supplementary Figure 1h Meridional section at W. 11
12 Supplementary Figure 1i Along-shore section on the central shelf. 12
13 Supplementary Figure 2 Extent and intensity of the ETSP OMZ. a,b, depth of upper and lower OMZ boundary (defined by O 2 15 µmol L -1 ). c, minimum O 2 concentrations measured throughout the cruise (Seabird O 2 sensor data corrected for an observed offset of ~2 µmol L -1 between Seabird- and STOX sensor measurements). Over the Peruvian shelf, O 2 concentrations 15 µmol L -1 were detected at depths as shallow as ~10 m. In the offshore region south of 3 S, the upper and lower OMZ boundaries were located at m (σ t ~26.25 kg m -3 ) and m (σ t ~27.1 kg m -3 ), respectively. To the north of this region, the OMZ was found deeper and less pronounced (~200 m thickness). Here, a depression of the upper OMZ boundary is likely caused by the eastward flowing Equatorial Undercurrent 11. Oxygen was undetectable ( 50 nmol L -1 ) in the subsurface shelf waters as well as in the core of the offshore OMZ by STOX measurements 12. Minimum O 2 concentrations were generally below 1.5 µmol L -1 south of 1 S, centered on a density (σ t ) of ~26.6 kg m -3. Higher minimum O 2 concentrations (>3 µmol L -1 ) were measured at the northernmost stations as well as a few stations off the northwestern tip of the Peruvian coast. 13
14 Supplementary Figure 3 Oxygen sensitivity of NO 2 - oxidation to NO 3 -. Rates of NO 2 - oxidation rates were only moderately affected by decreasing O 2 concentrations. Compared to incubations at >10 µmol L -1 of O 2, still 44-57% activity was measured at 1 µmol L -1. Similar O 2 sensitivities of NO 2 - oxidation (36-59% activity at O 2 1µmol L -1 ) were recently reported for the Namibian OMZ 13. The experimental procedure of the O 2 -sensitivity essay is described in Kalvelage et al. 12. Supplementary Figure 4 Anammox as a function of export of organic nitrogen (N org ). Grey symbols were measured anammox rates with error bars representing standard errors. Solid line shows the linear regression, while dotted lines denote 95% confidence intervals of the regression. Please note the increasing uncertainty associated with increasing export production. 14
15 Supplementary Table 1 Sampling locations and corresponding depth-integrated nutrient concentrations as well as N-fluxes. Station Lat / N Lon / E Bottom depth / m Extent of OMZ / m NH 4 + / mol m - ² NO 2 - / mol m - ² N* / mol m - ² H 2S / mol m - ² NH 3 oxidation to NO 2 - * NO 2 - oxidation to NO 3 - * NO 3 - reduction to NO 2 - * Anammox * Denitrification with H 2S * 119 (3) (±0.02) 4.03 (±0.33) 5.08 (±0.34) 0.82 (±0.22) (4) N.D (±0.19) 3.91 (±0.61) 0.28 (±0.05) (4) (±0.29) 11.5 (±1.53) 9.61 (±1.34) 2.49 (±0.33) (4) (±0.00) 5.24 (±1.58) 13.1 (±2.45) 2.93 (±0.29) (5) N.D (±0.43) 5.45 (±0.45) 0.47 (±0.12) (6) (±0.10) 16.1 (±4.30) 76.7 (±20.0) 12.3 (±1.42) (6) (±0.11) 6.40 (±0.51) 6.00 (±1.07) 1.50 (±0.25) (6) (±0.10) 2.63 (±0.30) 2.62 (±0.89) 1.39 (±0.29) (6) (±0.03) 8.46 (±1.27) 3.89 (±0.69) 0.94 (±0.05) (5) N.D (±0.07) 3.80 (±0.39) N.D (6) (±0.06) 5.11 (±1.25) 18.2 (±1.39) 5.26 (±0.73) (6) (±0.01) 2.36 (±0.27) 5.79 (±0.73) 1.00 (±0.22) (4) (±9.62) 65 (4) (±15.9) 62 (6) (±0.08) 24.1 (±1.27) 15.8 (±1.15) 8.08 (±0.73) (6) (±0.05) 11.0 (±1.72) 22.4 (±0.87) 6.28 (±1.04) (5) (±0.00) 2.92 (±0.35) 8.22 (±1.50) 0.76 (±0.12) (5) N.D. N.D (±0.37) N.D (3) (±0.18) 72.4 (±9.12) 20.0 (±1.64) 9.52 (±0.69) (6) (±0.16) 22.1 (±1.70) 9.99 (±1.60) 2.94 (±0.83) (6) (±0.06) 2.85 (±0.57) No data 1.35 (±0.36) (6) (±0.14) 8.86 (±0.91) 20.0 (±3.10) 3.08 (±0.35) 2.08 N org export to OMZ * In parenthesis: depths sampled for 15 N-labelling experiments. Vertical extent for O 2 15 µmol L -1. * In mmol N m - ² d -1. N.D.: non-detectable. Grey shading: sulfidic stations. 15
16 2 of 2 Supplementary Table 2. Volumetric N-cycling rates at various depths and stations in the ETSP OMZ onboard Meteor M77/3-4. Coastal OMZ ( 600 m) Offshore OMZ (>600m) Cruise Station Lat [ N] Lon [ E] Depth [m] Inc. depth [m] O2 [µm] NH4+ [µm] NO2- [µm] NO3- [µm] N* [µm] NH4+ ox. to NO2-* NO2- ox. to NO3-* NO3- red. to NO2-* M M M M M M M M M M M M M M M no data no data no data no data no data M M M M M M M M M M M M M M M no data no data no data M no data M no data all M no data M M M M no data no data M M M M M M all M M M M M all M M M M M M all M M M M M M M all M M all M M no data M no data M no data M no data M no data M no data M M M all M M M all M M M M M M anammox* exp DNRA* autotr. denitr.* heterotr. denitr.*
17 2 of 2 Supplementary Table 2. Volumetric N-cycling rates at various depths and stations in the ETSP OMZ onboard Meteor M77/3-4. Cruise Station Lat [ N] Lon [ E] Depth [m] Inc. depth [m] O2 [µm] NH4+ [µm] NO2- [µm] NO3- [µm] N* [µm] NH4+ ox. to NO2-* NO2- ox. to NO3-* NO3- red. to NO2-* M all M M M M all M all M all M all M all M all M all M all M all M all M all M M M M all M M all M M M M M M M all M all M all M all *all rates are net potential rates corrected for the labeling percentage of the respective N pool; =standard error N* = DIN - 16x PO µmol kg-1 x density M77-3: St. 805 CTD data; St & St. 3-8 µ-sensor data (downcast); St STOX - M77-4: CTD data Shown here are maximum potential anammox rates calculated from the respective 15 N-labeling experiments indicated: 1= 15 NH + 4, 2= 15 NO - 2, 3= 15 NH + 4 / 14 NO - 2, 4= 15 NO - 2 / 14 NH + 4, 5= 15 NO - 3, 6= 15 NO - 3 / 14 + NH 4 CTD oxygen data were corrected for an offset of ~2µM. anammox* exp DNRA* autotr. denitr.* heterotr. denitr.*
18 1 of 2 Supplmentary Table 3 N- cycling Biomarker Functional Gene Abundances (x10 2 copies ml - 1 ) at Different Sampling Stations in the ETSP OMZ. Station Water Sampled depth depth Latitude Longitude [m] [m] [ N] [ E] Archaeal amoa β- proteobacterial amoa γ- proteobacterial amoa denitrifier nirs Anammox hzo1 Amammox hzo2 nrfa Coastal OMZ ( 600 m)
19 Supplmentary Table 3 N- cycling Biomarker Functional Gene Abundances (x10 2 copies ml - 1 ) at Different Sampling Stations in the ETSP OMZ(Cont'd). 2 of 2 Offshore OMZ (>600m) Water depth Sampled depth Latitude Longitude Archaeal amoa β- proteobacterial amoa γ- proteobacterial amoa denitrifier nirs Anammox hzo1 Amammox hzo2 Station nrfa [m] [m] [ N] [ E]
20 References 1. Schlitzer, R. Ocean Data View, (2011). 2. Martin, J.H. et al. VERTEX: carbon cycling in the northeast Pacific. Deep-Sea Research 34, (1987). 3. Berelson, W.M. The Flux of Particulate Organic Carbon Into the Ocean Interior : A Comparison of Four U.S. JGOFS Regional Studies. Oceanography 14, (2001). 4. Suess, E., D, K.L. & Killingley, J.S. Marine Petroleum Source Rocks. Geologial Society Special Publication No (1987). 5. Revsbech, N.P. et al. Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor. Limnology and Oceanography: Methods 7, (2009). 6. Van Mooy, B.A., Keil, R.G. & Devol, A.H. Impact of suboxia on sinking particulate organic carbon: Enhanced carbon flux and preferential degradation of amino acids via denitrification. Geochimica et Cosmochimica Acta 66, (2002). 7. Hartnett, H.E. & Devol, A.H. Role of a strong oxygen-deficient zone in the preservation and degradation of organic matter: A carbon budget for the continental margins of northwest Mexico and Washington State. Geochimica et Chosmochimca Acta 67, (2003). 8. Bohlen, L. et al. Benthic nitrogen cycling traversing the Peruvian oxygen minimum zone. Geochimica et Cosmochimica Acta 75, (2011). 9. Reimers, C.E. & Suess, E. Spatial and temporal patterns of organic matter accumulation on the Peru continental margin. Coastal Upwelling: Its Sediment Record (1983). 10. Codispoti, L.A. & Packard, T.T. Denitrification Rates in the Eastern Tropical South- Pacific. Journal of Marine Research 38, (1980). 11. Helly, J.J. & Levin, L.A. Global distribution of naturally occurring marine hypoxia on continental margins. Deep-Sea Research 51, (2004). 12. Kalvelage, T. et al. Oxygen Sensitivity of Anammox and Coupled N-Cycle Processes in Oxygen Minimum Zones. PLoS ONE 6, e29299 (2011). 13. Füssel, J. et al. Nitrite oxidation in the Namibian oxygen minimum zone. The ISME Journal 6, (2011). 20
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