Physical mixing in coastal waters controls and decouples nitrification via biomass dilution

Proc Natl Acad Sci U S A. 2021 May 4;118(18):e2004877118. doi: 10.1073/pnas.2004877118.

Abstract

Nitrification is a central process of the aquatic nitrogen cycle that controls the supply of nitrate used in other key processes, such as phytoplankton growth and denitrification. Through time series observation and modeling of a seasonally stratified, eutrophic coastal basin, we demonstrate that physical dilution of nitrifying microorganisms by water column mixing can delay and decouple nitrification. The findings are based on a 4-y, weekly time series in the subsurface water of Bedford Basin, Nova Scotia, Canada, that included measurement of functional (amoA) and phylogenetic (16S rRNA) marker genes. In years with colder winters, more intense winter mixing resulted in strong dilution of resident nitrifiers in subsurface water, delaying nitrification for weeks to months despite availability of ammonium and oxygen. Delayed regrowth of nitrifiers also led to transient accumulation of nitrite (3 to 8 μmol · kgsw-1) due to decoupling of ammonia and nitrite oxidation. Nitrite accumulation was enhanced by ammonia-oxidizing bacteria (Nitrosomonadaceae) with fast enzyme kinetics, which temporarily outcompeted the ammonia-oxidizing archaea (Nitrosopumilus) that dominated under more stable conditions. The study reveals how physical mixing can drive seasonal and interannual variations in nitrification through control of microbial biomass and diversity. Variable, mixing-induced effects on functionally specialized microbial communities are likely relevant to biogeochemical transformation rates in other seasonally stratified water columns. The detailed study reveals a complex mechanism through which weather and climate variability impacts nitrogen speciation, with implications for coastal ecosystem productivity. It also emphasizes the value of high-frequency, multiparameter time series for identifying complex controls of biogeochemical processes in aquatic systems.

Keywords: Thaumarchaeota; aquatic nitrogen biogeochemistry; nitrifier diversity; nitrite accumulation; time series.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ammonia / metabolism
  • Ammonium Compounds / metabolism
  • Archaea / genetics
  • Archaea / metabolism
  • Biomass
  • Canada
  • Denitrification / genetics
  • Ecosystem
  • Humans
  • Kinetics
  • Nitrates
  • Nitrification / genetics*
  • Nitrites / metabolism
  • Nitrogen / metabolism
  • Nitrogen Cycle / genetics*
  • Nitrosomonadaceae / genetics*
  • Nitrosomonadaceae / pathogenicity
  • Oxidation-Reduction
  • Phylogeny
  • Phytoplankton / genetics
  • Phytoplankton / metabolism
  • RNA, Ribosomal, 16S / genetics
  • Seasons
  • Water / metabolism*

Substances

  • Ammonium Compounds
  • Nitrates
  • Nitrites
  • RNA, Ribosomal, 16S
  • Water
  • Ammonia
  • Nitrogen