Photoinhibition on natural ammonia oxidizers biofilm populations and implications for nitrogen uptake in stream biofilms

Abstract

We investigated photoinhibition on natural communities of ammonia oxidizing (AO) archaea (AOA) and bacteria (AOB) embedded in complex stream biofilms, and its implications on nitrogen uptake at biofilm scale. Based on the strong photoinhibition previously exhibited by free living and cultured AOA and AOB, we expected AO activity to decrease in biofilms experimentally exposed to light, reducing the contribution of microbial nitrification to ammonium uptake. To test it, we conducted light manipulation experiments in mesocosms using biofilms naturally developed on stream cobbles sides both exposed to light (light‐side) and facing the sediment (dark‐side). We observed a strong AO photoinhibition in dark‐side biofilms, accompanied by either biofilm‐scale decreases in nitrification or increases in nitrogen uptake likely by heterotrophic activity. Conversely, in light‐side biofilms photoinhibition was not observed suggesting that photoautotrophic layers may protect AO in situ by a sunshade effect. Experimental light and dark alternation cycles stimulated AO, enhancing both nitrification and ammonium uptake. These results support photoinhibition effects on natural AO communities, especially in biofilms developed under ambient dark conditions, whereas this effect seems to be buffered in biofilms developed under light conditions. Therefore, the contribution of nitrification to ammonium uptake at biofilm scale should consider not only the physiological study of AOA and AOB, but also the environmental conditions and community structure at the habitat microscale, since they may counterbalance, among others, the damaging light effects under natural conditions.

Day–night ammonium oxidation in an urban stream: the influence of irradiance on ammonia oxidizers

“…AOA and AOB were present in similar abundance even in light-side epilithic biofilms that were more exposed to light and thus, more susceptible to photoinhibition. The failure of light to prevent ammonia oxidizers from colonizing light-exposed biofilms could be partially explained by the 3-dimensional structure of the biofilm matrix that may provide particular self-shading (Boston and Hill 1991, Guasch and Sabater 1995, Merbt et al 2016). This idea is further supported by the nonlinear relationship between the abundance of ammonia oxidizers and biofilm AFDM, which shows that a minimal critical biomass (AFDM > 0.17 g/cm 2 ) is needed for successful development of ammonia oxidizers in light-side epilithic biofilms.…”

“…1 (Smith et al 2014) or high susceptibility to light (Merbt et al 2016). In streams, AOA and AOB are part of benthic microbial biofilm assemblages growing on submerged substrata and within the sediment (Merbt et al 2011, Sonthiphand et al 2013.…”

“…In streams, AOA and AOB are part of benthic microbial biofilm assemblages growing on submerged substrata and within the sediment (Merbt et al 2011, Sonthiphand et al 2013. Those ammonia-oxidizing communities can experience photoinhibition when biofilms developed naturally in the dark are experimentally exposed to light (Merbt et al 2016). Thus, we hypothesized that irradiance could determine the spatial distribution of ammonia oxidizers and diel rates of NH 4 1 oxidation in stream ecosystems and, ultimately, could dictate in-stream NH 4 1 oxidation at the reach scale.…”

Differences in ammonium oxidizer abundance and N uptake capacity between epilithic and epipsammic biofilms in an urban stream

“…However, the degree to which algae contributes to NH 4 1 uptake in this type of experiment depends on the specific light conditions set during the incubations. For instance, in a previous study, assimilatory NH 4 1 uptake increased when epilithic biofilms were exposed to experimental dark and light alternation cycles, though no changes were detected under full light conditions, probably because some other element became limiting (Merbt et al 2017).…”

“…Water was recirculated continuously with a submerged peristaltic pump (12 V) and water temperature and DO were constant during the experiments (21 ± 1.67C, 8.6 ± 0.6 mg O 2 /L). We ran the incubations under dark conditions to ensure optimal conditions for nitrification and to avoid confounding effects associated with photoinhibition (Merbt et al 2017). Running the experiments in darkness might have led us to underestimate NH 4 1 uptake to some extent because we did not account for photoautotrophic NH 4…”