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Biogeosciences An interactive open-access journal of the European Geosciences Union
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© Author(s) 2019. This work is distributed under
the Creative Commons Attribution 4.0 License.
© Author(s) 2019. This work is distributed under
the Creative Commons Attribution 4.0 License.

Research article 08 Mar 2019

Research article | 08 Mar 2019

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This discussion paper is a preprint. It is a manuscript under review for the journal Biogeosciences (BG).

Physical constraints for respiration in microbial hotspots in soil and their importance for denitrification

Steffen Schlüter1, Jan Zawallich2, Hans-Jörg Vogel1, and Peter Dörsch3 Steffen Schlüter et al.
  • 1Department Soil System Sciences, Helmholtz-Centre for Environmental Research - UFZ, Theodor-Lieser-Str. 4, 06120 Halle, Germany
  • 2Institute of Mathematics, TU Clausthal, Erzweg 3, Clausthal-Zellerfeld, Germany
  • 3Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, NMBU, Aas, Norway

Abstract. Soil denitrification is the most important terrestrial process returning reactive nitrogen to the atmosphere, but remains poorly understood. In upland soils, denitrification occurs in hotspots of enhanced microbial activity, even under well-aerated conditions, and causes harmful emissions of nitric (NO) and nitrous oxide (N2O). Timing and magnitude of such emissions are difficult to predict due to the delicate balance of oxygen (O2) consumption and diffusion in soil. To study how spatial distribution of hotspots affects O2 exchange and denitrification, we embedded porous glass beads inoculated with either Agrobacterium tumefaciens (a denitrifier lacking N2O reductase) or Paracoccus denitrificans (a complete denitrifier) in different architectures (random vs. layered) in sterile sand adjusted to different water saturations (30 %, 60 %, 90 %) and measured gas kinetics (O2, CO2, NO, N2O and N2) at high temporal resolution. Air connectivity, air distance and air tortuosity were determined by X-ray tomography after the experiment. The hotspot architecture exerted strong control on microbial growth and timing of denitrification at low and intermediate saturations, because the separation distance between the microbial hotspots governed local oxygen supply. Electron flow diverted to denitrification in anoxic hotspot centers was low (2–7 %) but increased markedly (17–27 %) at high water saturation. X-ray analysis revealed that the air phase around most of the hotspots remained connected to the headspace even at 90 % saturation, suggesting that the threshold response of denitrification to soil moisture could be ascribed solely to increasing tortuosity of air-filled pores. Our findings suggest that denitrification and its gaseous product stoichiometry do not only depend on the amount of microbial hotspots in aerated soil, but also on their spatial distribution. We demonstrate that combining measurements of microbial activity with quantitative analysis of diffusion lengths using X-ray tomography provides unprecedented insights into physical constraints regulating soil microbial respiration in general and denitrification in particular. This opens new avenues to use observable soil structural attributes to predict denitrification and to parameterize models. Further experiments with natural soil structure, carbon substrates and microbial communities are required to demonstrate this under realistic conditions.

Steffen Schlüter et al.
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Status: final response (author comments only)
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Steffen Schlüter et al.
Steffen Schlüter et al.
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Short summary
A combination of gas chromatography and X-ray CT reveals the microscale processes that govern soil respiration. Aerobic and anaerobic respiration in microbial hotspots not only depends on the quality and quantity of soil organic matter, but also on the spatial distribution of hotspots. Denitrification kinetics are mainly governed by hotspot architecture due to local competition for oxygen during growth. Cumulative behavior is mainly governed by water saturation due to the overall supply with O2.
A combination of gas chromatography and X-ray CT reveals the microscale processes that govern...