Warming Shapes nirS- and nosZ-Type Denitrifier Communities and Stimulates N2O Emission in Acidic Paddy Soil

Appl Environ Microbiol. 2021 May 26;87(12):e0296520. doi: 10.1128/AEM.02965-20. Epub 2021 May 26.

Abstract

Warming strongly stimulates soil nitrous oxide (N2O) emission, contributing to the global warming trend. Submerged paddy soils exhibit huge N2O emission potential; however, the N2O emission pathway and underlying mechanisms for warming are not clearly understood. We conducted an incubation experiment using 15N to investigate the dynamics of N2O emission at controlled temperatures (5, 15, 25, and 35°C) in 125% water-filled pore space. The community structures of nitrifiers and denitrifiers were determined via high-throughput sequencing of functional genes. Our results showed that elevated temperature sharply enhanced soil N2O emission from submerged paddy soil. Denitrification was the main contributor, accounting for more than 90% of total N2O emission at all treatment temperatures. N2O flux was coordinatively regulated by nirK-, nirS-, and nosZ-containing denitrifiers but not ammonia-oxidizing archaea or ammonia-oxidizing bacteria. The nirS-containing denitrifiers were more sensitive to temperature shifts, especially at a lower temperature range (5 to 25°C), and showed a stronger correlation with N2O flux than that of nirK-containing denitrifiers. In contrast, nosZ-containing denitrifiers exhibited substantial variation at higher temperatures (15 to 35°C), thereby playing an important role in N2O consumption. Certain taxa of nirS- and nosZ-containing denitrifiers regulated N2O flux, including nirS-containing denitrifiers affiliated with Rhodanobacter and Cupriavidus as well as nosZ-containing denitrifiers affiliated with Azoarcus and Azospirillum. Together, these findings suggest that elevated temperature can significantly increase N2O emission from denitrification in submerged paddy soils by shifting the overall community structures and enriching some indigenous taxa of nirS- and nosZ-containing denitrifiers. IMPORTANCE The interdependence between global warming and greenhouse gas N2O has always been the hot spot. However, information on factors contributing to N2O and temperature-dependent community structure changes is scarce. This study demonstrated high-temperature-induced N2O emission from submerged paddy soils, mainly via stimulating denitrification. Further, we speculate that key functional denitrifiers drive N2O emission. This study showed that denitrifiers were more sensitive to temperature rise than nitrifiers, and the temperature sensitivity differed among denitrifier communities. N2O-consuming denitrifiers (nosZ-containing denitrifiers) were more sensitive at a higher temperature range than N2O-producing denitrifiers (nirS-containing denitrifiers). This study's findings help predict N2O fluxes under different degrees of warming and develop strategies to mitigate N2O emissions from paddy fields based on microbial community regulation.

Keywords: N2O emission; key regulating taxa; relative contribution; submerged paddy soils; temperature sensitivity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Air Pollutants / analysis*
  • Denitrification*
  • Global Warming
  • Hydrogen-Ion Concentration
  • Nitrification
  • Nitrous Oxide / analysis*
  • Oryza
  • Soil / chemistry
  • Soil Microbiology*
  • Soil Pollutants / analysis*
  • Temperature

Substances

  • Air Pollutants
  • Soil
  • Soil Pollutants
  • Nitrous Oxide