Skip to main content

Advertisement

Log in

Submicromolar Oxygen Profiles at the Oxic–Anoxic Boundary of Temperate Lakes

  • Original Paper
  • Published:
Aquatic Geochemistry Aims and scope Submit manuscript

Abstract

Elements involved in biogeochemical cycles undergo rapid turnover at the oxic–anoxic interface of stratified lakes. Here, the presence or absence of oxygen governs abiotic and biotic processes and rates. However, achieving a detailed sampling resolution to precisely locate the oxic–anoxic interface is difficult due to a lack of fast, drift-free sensors in the working range of 10 to a few 1,000 nmol O2 L−1. Here, we demonstrate that conventional amperometric and optical microsensors can be used to resolve submicromolar oxygen concentrations in a continuous profiling mode. The amperometric drift was drastically reduced by anoxic preconditioning. In situ offset correction in the anoxic layer and a high amplification scheme allowed for an excellent detection limit of < 10 nmol L−1. The optical microsensors also showed a similar performance with a detection limit of < 20 nmol L−1. Their drift stability allowed for a laboratory calibration in combination with a minor in situ anoxic offset correction. The two different sensor systems showed virtually identical profiles during parallel use in stratified lakes. Both sensors were able to resolve the fine-scale structure at the oxic–anoxic interface and revealed hitherto unnoticed extended zones of submicromolar oxygen concentrations even below a steep oxycline. The zones extended up to several meters and showed substantial vertical variability. These results underline the need of a precise localization of the oxic–anoxic interface on a submicromolar scale in order to constrain the relevant aerobic and anaerobic redox processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Balcke GU, Wegener S, Kiesel B, Benndorf D, Schlomann M, Vogt C (2008) Kinetics of chlorobenzene biodegradation under reduced oxygen levels. Biodegradation 19(4):507–518. doi:10.1007/s10532-007-9156-0

    Article  Google Scholar 

  • Barbieri A, Polli B (1992) Description of Lake Lugano. Aquat Sci 54(3–4):181–183. doi:10.1007/BF00878135

    Article  Google Scholar 

  • Benson BB, Krause D (1984) The concentration and isotopic fractionation of oxygen dissolved in fresh-water and seawater in equilibrium with the atmosphere. Limnol Oceanogr 29(3):620–632. doi:10.4319/lo.1984.29.3.0620

    Article  Google Scholar 

  • Berg P, Roy H, Janssen F, Meyer V, Jorgensen BB, Huettel M, de Beer D (2003) Oxygen uptake by aquatic sediments measured with a novel non-invasive eddy-correlation technique. Mar Ecol Prog Ser 261:75–83. doi:10.3354/Meps261075

    Article  Google Scholar 

  • Berner RA (1981) A new geochemical classification of sedimentary environments. J Sediment Petrol 51(2):359–365. doi:10.1306/212F7C7F-2B24-11D7-8648000102C1865D

    Google Scholar 

  • Brand A, McGinnis DF, Wehrli B, Wüest A (2008) Intermittent oxygen flux from the interior into the bottom boundary of lakes as observed by eddy correlation. Limnol Oceanogr 53(5):1997–2006. doi:10.4319/lo.2008.53.5.1997

    Article  Google Scholar 

  • Canfield DE, Thamdrup B (2009) Towards a consistent classification scheme for geochemical environments, or, why we wish the term ‘suboxic’ would go away. Geobiology 7(4):385–392. doi:10.1111/j.1472-4669.2009.00214.x

    Article  Google Scholar 

  • Chipman L, Huettel M, Berg P, Meyer V, Klimant I, Glud R, Wenzhoefer F (2012) Oxygen optodes as fast sensors for eddy correlation measurements in aquatic systems. Limnol Oceanogr Methods 10:304–316. doi:10.4319/lom.2012.10.304

    Article  Google Scholar 

  • Clark LC, Wolf R, Granger D, Taylor Z (1953) Continuous recording of blood oxygen tensions by polarography. J Appl Physiol 6(3):189–193

    Google Scholar 

  • Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458

    Article  Google Scholar 

  • Dellwig O, Leipe T, Marz C, Glockzin M, Pollehne F, Schnetger B, Yakushev EV, Bottcher ME, Brumsack HJ (2010) A new particulate Mn–Fe–P-shuttle at the redoxcline of anoxic basins. Geochim Cosmochim Acta 74(24):7100–7115. doi:10.1016/j.gca.2010.09.017

    Article  Google Scholar 

  • Garcia HE, Gordon LI (1992) Oxygen solubility in seawater—better fitting equations. Limnol Oceanogr 37(6):1307–1312. doi:10.4319/lo.1992.37.6.1307

    Article  Google Scholar 

  • Goudsmit GH, Peeters F, Gloor M, Wüest A (1997) Boundary versus internal diapycnal mixing in stratified natural waters. J Geophys Res Oceans 102(C13):27903–27914. doi:10.1029/97JC01861

    Article  Google Scholar 

  • Gundersen JK, Ramsing NB, Glud RN (1998) Predicting the signal of O2 microsensors from physical dimensions, temperature, salinity, and O2 concentration. Limnol Oceanogr 43(8):1932–1937

    Google Scholar 

  • Hofmann AF, Peltzer ET, Walz PM, Brewer PG (2011) Hypoxia by degrees: establishing definitions for a changing ocean. Deep Sea Res Part I 58(12):1212–1226. doi:10.1016/j.dsr.2011.09.004

    Article  Google Scholar 

  • Holst GA, Kuehl M, Klimant I (1995) Novel measuring system for oxygen micro-optodes based on a phase modulation technique. Proc SPIE 2508:387–398. doi:10.1117/12.221754

    Article  Google Scholar 

  • Holst G, Klimant I, Kühl M, Kohls O (2000) Optical microsensors and microprobes. In: Varney MS (ed) Chemical sensors in oceanography, vol 1. Gordon and Breach Science Publishers, London

    Google Scholar 

  • Imboden DM, Wüest A (1995) Physics and chemistry of lakes, 2nd edn. Springer, Berlin

    Google Scholar 

  • Kalvelage T, Jensen MM, Contreras S, Revsbech NP, Lam P, Gunter M, LaRoche J, Lavik G, Kuypers MMM et al (2011) Oxygen sensitivity of anammox and coupled N-cycle processes in oxygen minimum zones. Plos One 6(12). doi:10.1371/journal.pone.0029299

  • Klimant I, Meyer V, Kuhl M (1995) Fiber-optic oxygen microsensors, a new tool in aquatic biology. Limnol Oceanogr 40(6):1159–1165. doi:0.4319/lo.1995.40.6.1159

    Article  Google Scholar 

  • Kohler HP, Ahring B, Albella C (1984) Bacteriological studies on the sulfur cycle in the anaerobic part of the hypolimnion and in the surface sediments of Rotsee in Switzerland. FEMS Microbiol Lett 21(3):279–286. doi:10.1111/j.1574-6968.1984.tb00322.x

    Google Scholar 

  • Konovalov SK, Luther GW, Friederich GE, Nuzzio DB, Tebo BM, Murray JW, Oguz T, Glazer B, Trouwborst RE, Clement B, Murray KJ, Romanov AS (2003) Lateral injection of oxygen with the Bosporus plume—fingers of oxidizing potential in the Black Sea. Limnol Oceanogr 48(6):2369–2376

    Article  Google Scholar 

  • Lam P, Kuypers MMM (2011) Microbial nitrogen cycling processes in oxygen minimum zones. Annu Rev Mar Sci 3:317–345. doi:10.1146/annurev-marine-120709-142814

    Article  Google Scholar 

  • Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Dimitri G, Amann R, Jetten MSM, Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA 106(12):4752–4757. doi:10.1073/pnas.0812444106

    Article  Google Scholar 

  • Lippitsch ME, Pusterhofer J, Leiner MJP, Wolfbeis OS (1988) Fibre-optic oxygen sensor with the fluorescence decay time as the information carrier. Anal Chim Acta 205(1–2):1–6. doi:10.1016/S0003-2670(00)82310-7

    Article  Google Scholar 

  • Lopes F, Viollier E, Thiam A, Michard G, Abril G, Groleau A, Prevot F, Carrias JF, Alberic P, Jezequel D (2011) Biogeochemical modelling of anaerobic vs. aerobic methane oxidation in a meromictic crater lake (Lake Pavin, France). Appl Geochem 26(12):1919–1932. doi:10.1016/j.apgeochem.2011.06.021

    Article  Google Scholar 

  • Lorke A, Müller B, Maerki M, Wüest A (2003) Breathing sediments: the control of diffusive transport across the sediment-water interface by periodic boundary-layer turbulence. Limnol Oceanogr 48(6):2077–2085. doi:10.4319/lo.2003.48.6.2077

    Article  Google Scholar 

  • Maerki M, Müller B, Dinkel C, Wehrli B (2009) Mineralization pathways in lake sediments with different oxygen and organic carbon supply. Limnol Oceanogr 54(2):428–438. doi:10.4319/lo.2009.54.2.0428

    Article  Google Scholar 

  • Mayr T, Borisov SM, Abel T, Enko B, Waich K, Mistlberger G, Klimant I (2009) Light harvesting as a simple and versatile way to enhance brightness of luminescent sensors. Anal Chem 81(15):6541–6545. doi:10.1021/Ac900662x

    Article  Google Scholar 

  • Morrison JM, Codispoti LA, Smith SL, Wishner K, Flagg C, Gardner WD, Gaurin S, Naqvi SWA, Manghnani V, Prosperie L, Gundersen JS (1999) The oxygen minimum zone in the Arabian Sea during 1995. Deep Sea Res Part II 46(8–9):1903–1931. doi:10.1016/S0967-0645(99)00048-X

    Article  Google Scholar 

  • Müller B, Bryant LD, Matzinger A, Wüest A (2012) Hypolimnetic oxygen depletion in eutrophic lakes. Environ Sci Technol 46(18):9964–9971. doi:10.1021/es301422r

    Google Scholar 

  • Murray JW, Codispoti LA, Friederich GE et al (1995) Oxidation-reduction environments—the suboxic zone in the Black Sea. In: Huang CP, O’Melia CR, Morgan JJ (eds) Aquatic chemistry: interfacial and interspecies processes, vol 244. American Chemical Society: Washington, DC, pp 157–176. doi:10.1021/ba-1995-0244.ch007

  • Nestler H, Kiesel B, Kaschabek SR, Mau M, Schlomann M, Balcke GU (2007) Biodegradation of chlorobenzene under hypoxic and mixed hypoxic-denitrifying conditions. Biodegradation 18(6):755–767. doi:10.1007/s10532-007-9104-z

    Article  Google Scholar 

  • Peeters F, Wüest A, Piepke G, Imboden DM et al (1996) Horizontal mixing in lakes. J Geophys Res Oceans 101(C8):18361–18375. doi:10.1029/96JC01145

    Article  Google Scholar 

  • Reimers CE (1987) An in situ microprofiling instrument for measuring interfacial pore water gradients—methods and oxygen profiles from the North Pacific Ocean. Deep Sea Res Part A 34(12):2019–2035. doi:10.1016/0198-0149(87)90096-3

    Article  Google Scholar 

  • Revsbech NP (1989) An oxygen microsensor with a guard cathode. Limnol Oceanogr 34(2):474–478. doi:10.4319/lo.1989.34.2.0474

    Article  Google Scholar 

  • Revsbech NP, Jørgensen BB (1986) Microelectrodes: their use in microbial ecology. Adv Microb Ecol 9:293–352

    Article  Google Scholar 

  • Revsbech NP, Larsen LH, Gundersen J, Dalsgaard T, Ulloa O, Thamdrup B (2009) Determination of ultra-low oxygen concentrations in oxygen minimum zones by the STOX sensor. Limnol Oceanogr Methods 7:371–381. doi:10.4319/lom.2009.7.371

    Article  Google Scholar 

  • Revsbech NP, Thamdrup B, Dalsgaard T, Canfield DE (2011) Construction of STOX oxygen sensors and their application for determination of O2 concentrations in oxygen minimum zones. Methods Enzymol 486:325–341. doi:10.1016/B978-0-12-381294-0.00014-6

    Article  Google Scholar 

  • Schubert CJ, Durisch-Kaiser E, Wehrli B, Thamdrup B, Lam P, Kuypers MMM (2006) Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ Microbiol 8(10):1857–1863. doi:10.1111/j.1462-2920.2006.001074.x

    Article  Google Scholar 

  • Schubert CJ, Lucas FS, Durisch-Kaiser E, Stierli R, Diem T, Scheidegger O, Vazquez F, Müller B (2010) Oxidation and emission of methane in a monomictic lake (Rotsee, Switzerland). Aquat Sci 72(4):455–466. doi:10.1007/s00027-010-0148-5

    Article  Google Scholar 

  • Stolper DA, Revsbech NP, Canfield DE (2010) Aerobic growth at nanomolar oxygen concentrations. Proc Natl Acad Sci USA 107(44):18755–18760. doi:10.1073/pnas.1013435107

    Article  Google Scholar 

  • Tengberg A, Hovdenes J, Andersson HJ, Brocandel O, Diaz R, Hebert D, Arnerich T, Huber C, Kortzinger A, Khripounoff A, Rey F, Ronning C, Schimanski J, Sommer S, Stangelmayer A (2006) Evaluation of a lifetime-based optode to measure oxygen in aquatic systems. Limnol Oceanogr Methods 4:7–17. doi:10.4319/lom.2006.4.7

    Article  Google Scholar 

  • Thamdrup B, Dalsgaard T, Revsbech NP (2012) Widespread functional anoxia in the oxygen minimum zone of the Eastern South Pacific. Deep Sea Res Part I 65:36–45. doi:10.1016/j.dsr.2012.03.001

    Article  Google Scholar 

  • Tonolla M, Peduzzi S, Demarta A, Peduzzi R, Hahn D (2004) Phototropic sulfur and sulfate-reducing bacteria in the chemocline of meromictic Lake Cadagno, Switzerland. J Limnol 63(2):161–170. doi:10.4081/jlimnol.2004.161

    Google Scholar 

  • Ulloa O, Canfield DE, DeLong EF, Letelier RM, Stewart FJ (2012) Microbial oceanography of anoxic oxygen minimum zones. Proc Natl Acad Sci USA 109(40):15996–16003. doi:10.1073/pnas.1205009109

    Article  Google Scholar 

  • Winkler LW (1888) Die Bestimmung des im Wasser gelösten Sauerstoffes. Ber Dtsch Chem Ges 21(2):2843–2854. doi:10.1002/cber.188802102122

    Article  Google Scholar 

  • Wright JJ, Konwar KM, Hallam SJ (2012) Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol 10(6):381–394. doi:10.1038/Nrmicro2778

    Google Scholar 

  • Wüest A, Lorke A (2003) Small-scale hydrodynamics in lakes. Annu Rev Fluid Mech 35:373–412. doi:10.1146/annurev.fluid.35.101101.161220

    Article  Google Scholar 

Download references

Acknowledgments

For fruitful discussions, we thank Eric Epping, Jan Fischer, Volker Meyer and Hans Røy. We thank Dörte Carstens, Alois Zwyssig and Ruth Stierli for help in the laboratory and in the field. Hans Røy, Alfred Wüest, B. Bohnenbuck, Moritz Holtappels, Jan Fischer, Andreas Brand and Helmut Bürgmann commented on the previous version of the manuscript. The project was funded by Eawag and benefitted from the interaction with team members of the EU-project “HYPOX” (EC Grant # 226213).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mathias K. Kirf.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kirf, M.K., Dinkel, C., Schubert, C.J. et al. Submicromolar Oxygen Profiles at the Oxic–Anoxic Boundary of Temperate Lakes. Aquat Geochem 20, 39–57 (2014). https://doi.org/10.1007/s10498-013-9206-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10498-013-9206-7

Keywords

Navigation