Coupled nitrification‐denitrification in autotrophic and heterotrophic estuarine sediments: On the influence of benthic microalgae

Abstract

Field data obtained from 18 European estuaries using the isotope pairing technique were analyzed for trends in relationship between activity of benthic microalgae and coupled nitrification-denitrification. Kruskal-Wallis tests and analyses of covariance performed on the field dataset showed strong statistical evidence for the hypothesis that sediments colonized by microalgae whose activity exceeds community respiration display lower rates of coupled nitrification-denitrification than do heterotrophic sediments. In fully heterotrophic sediments, 90% of the measurements fell within the range 0-92 mol N m Ϫ2 h Ϫ1 with a median of 20.3 mol N m Ϫ2 h Ϫ1. In highly autotrophic sediments, 90% of the measurements fell within the range 0-34 mol N m Ϫ2 h Ϫ1 , and the median was 4.2 mol N m Ϫ2 h Ϫ1 . The hypothesis was tested experimentally using 15 N and microsensor (NO ) techniques in prepared Ϫ 3 microcosms with and without algal activity. The results of the experimental studies were consistent with the hypothesis derived from the field data analysis. For the 15 N study, coupled nitrification-denitrification in alga-colonized sediments was between 4 and 51% of the activity in sediments without algae activity, depending on the N load. For the microsensor study, there was no indication of net NO production in alga-colonized sediments before furthermore showed that compared to heterotrophic sediment, the presence of active microalgae might reduce the population of nitrifying bacteria capable of having an active metabolism. These bacterial populations could display diurnal variations in activity correlated with the diurnal variations in O 2 penetration depth, however. The results showed that induction of nitrogen limitation of the nitrifying bacteria population is a major controlling mechanism of coupled nitrification-denitrification in alga-colonized sediments.

Quantifying photosynthetic rates of microphytobenthos using the triple isotope composition of dissolved oxygen

“…These producers may account for greater than 50% of gross primary productivity, i.e., the total photosynthetic flux, in estuaries (Underwood and Kromkamp 1999). Microphytobenthos have been implicated as a major, and in some cases dominant, controlling factor in estuarine nitrogen cycling (Engelsen et al 2008;Risgaard-Petersen 2003;Tyler et al 2003). Because of their role in moving nitrogen from the overlying water column into the sediments, it is hypothesized that MPB act to buffer estuaries from the effects of eutrophication (McGlathery et al 2004;Meyercordt and Meyer-Reil 1999).…”

“…Humans have heavily impacted coastal zones, and many estuaries show signs of eutrophication (Bricker et al 2007;Cloern 2001;de Jonge et al 2002;Nixon 1995) with low water quality, seasonal harmful algal blooms (Paerl 1988), hypoxia (Diaz 2001;Diaz and Rosenberg 1995;Kemp et al 2009;Rabalais et al 1996;Turner and Rabalais 1994;Vaquer-Sunyer and Duarte 2008), and fish kills (Thronson and Quigg 2008). Microphytobenthos (MPB), i.e., unicellular benthic photosynthesizers such as diatoms and cyanobacteria, are important mediators of nutrient and carbon fluxes in these shallow environments (Eyre andFerguson 2002, 2005;McGlathery et al 2001;McGlathery et al 2004;Risgaard-Petersen 2003;Rysgaard et al 1995;Sundbäck et al 1991). These producers may account for greater than 50% of gross primary productivity, i.e., the total photosynthetic flux, in estuaries (Underwood and Kromkamp 1999).…”

“…Furthermore, there has been some debate as to whether radiocarbon-based productivity estimates are actually measuring gross or net productivity or something in between (e.g., Dring and Jewson 1982). Oxygen fluxes from incubations of cores in light and dark conditions in labo-ratories (Hopkinson et al 1999;Risgaard-Petersen 2003;Sundbäck et al 1991), in benthic flux chambers (Cebrian et al 2008;Jahnke et al 2000;Jahnke et al 2008), or from eddy correlation technique (Berg et al 2003;Glud et al 2010;Lorrai et al 2010;McGinnis et al 2008) are also used to estimate gross and net productivity. However these approaches require the assumption that light and dark respiration are similar, when in fact MPB light respiration appears to be greater than dark respiration by a factor of 1.5 to 2.5 (Epping and Jorgensen 1996;Fenchel and Glud 2000).…”

Nutrient and herbivore alterations cause uncoupled changes in producer diversity, biomass and ecosystem function, but not in overall multifunctionality

“…Cyanobacteria, another relevant component of benthic microalgal assemblages, commonly use atmospheric N 2 as a source of N 30 . Although benthic microalgae do not directly perform denitrifiaction, in high densities benthic microalgae can outcompete nitrifying bacteria, decreasing coupled nitrification-denitrification rates 31 . Additionally, higher abundance of benthic microalgae can also be associated with higher sediment organic matter, particularly in the upper layer 32 , and thus also to sediment water content, given that sediment water content usually follows similar patterns as organic matter 33, 34 .…”

Connecting the dots: linking nitrogen cycle gene expression to nitrogen fluxes in marine sediment mesocosms

“…When estuarine bottom waters are oxic, some portion of NH + 4 formed in the sediment is oxidized at the sediment water interface to form nitrite (NO − 2 ) and then nitrate (NO − 3 ) through the microbially mediated nitrification pathway. This oxidized NO − 3 is then lost as nitrogen gas from the adjoining suboxic sediments through a coupling of the nitrification and denitrification pathways (Jenkins and Kemp, 1984; An and Joye, 2001; Risgaard-Petersen, 2003). In estuaries that have frequent summertime bottom water hypoxia or anoxia, the coupling of nitrification and denitrification can be interrupted as nitrification becomes inhibited by a lack of oxygen and by the accumulation of sulfide (Joye and Hollibaugh, 1995).…”