Date Published: March 20, 2019
Publisher: Public Library of Science
Author(s): Stéphanie Massé, Morgan Botrel, David A. Walsh, Roxane Maranger, Iddya Karunasagar.
We investigated the variability in ammonia oxidation (AO) rates and the presence of ammonia-oxidizing archaea and bacteria (AOB and AOA) over an annual cycle in the water column of a small, seasonnally ice covered, temperate shield lake. AO, the first step of nitrification, was measured in situ using 15N-labelled ammonium (NH4+) at 1% and 10% of photosynthetic active radiation during day and at the same depths during night. AO was active across seasons and light levels, ranging from undetectable to 333 nmol L-1 d-1 with peak activity in winter under ice cover. NH4+ concentration was the single most important positive predictor of AO rates. High NH4+ concentrations and reduced chlorophyll a concentrations under ice, which favoured AO, were coherent with high nitrate concentrations and super saturation in nitrous oxide. When targeting the ammonia monooxygenase (amoA) gene in samples from the photic zone, we found AOA to be omnipresent throughout the year while AOB were observed predominantly during winter. Our results demonstrate that AO is an ongoing process in sunlit surface waters of temperate lakes and at all seasons with pronounced nitrification activity observed during winter under ice. The combination of high NH4+ concentrations due to fall overturn, reduced light availability that limited phytoplankton competition, and the presence of AOB together with AOA apparently favoured these elevated rates under ice. We suggest that lake ice could be a control point for nitrification in oligotrophic temperate shield lakes, characterized as a moment and place that exerts disproportionate influence on the biogeochemical behaviour of ecosystems.
Nitrification is a two-step microbial process that plays a pivotal role in the nitrogen (N) cycle, yet our understanding of the relative importance of nitrification in aquatic systems is currently heavily biased to marine systems as compared to lakes . Ammonia oxidation (AO), typically considered the rate-limiting transformation  and the most frequently measured proxy of nitrification, first converts ammonium (NH4+) to nitrite (NO2-) and is performed by ammonia-oxidizing bacteria (AOB) or ammonia-oxidizing archaea (AOA). AO is also a chemoautotrophic process that uses dissolved oxygen as the electron acceptor. In step two of nitrification, the resulting NO2- is converted to nitrate (NO3-) by nitrite-oxidizing bacteria. Thus, nitrification controls the relative availability of different N forms. In aquatic systems, this influences phytoplankton growth and community structure , but also the supply of nitrate (NO3-) for denitrification, the main N loss pathway that can mitigate eutrophication  (Fig 1). Furthermore, and on a global scale, nitrification has a direct effect on climate change since nitrous oxide (N2O) is a potent greenhouse gas and is a by-product of the AO reaction [5, 6].
This study is the first to our knowledge to simultaneously quantify the in situ AO rates and assess the presence and the diversity of AOA and AOB across seasons in a small ice-covered temperate, oligotrophic lake. Four major outcomes were identified: (1) AO was observed at 10% and 1% of surface PAR and throughout all seasons; (2) NH4+ concentrations exerted the strongest influence on rates; (3) AOA were observed throughout the year and likely play a dominant role in nitrification in oligotrophic lakes and (4) lake ice appears to act as a control point for AO. This is likely due to the highest availability of NH4+ under ice, the presence of both AOA and AOB and reduced competition with phytoplankton for this critical substrate as a function of light limitation.