amoA Gene Abundances and Nitrification Potential Rates Suggest that Benthic Ammonia-Oxidizing Bacteria and Not Archaea Dominate N Cycling in the Colne Estuary, United Kingdom

Abstract

bNitrification, mediated by ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA), is important in global nitrogen cycling. In estuaries where gradients of salinity and ammonia concentrations occur, there may be differential selections for ammonia-oxidizer populations. The aim of this study was to examine the activity, abundance, and diversity of AOA and AOB in surface oxic sediments of a highly nutrified estuary that exhibits gradients of salinity and ammonium. AOB and AOA communities were investigated by measuring ammonia monooxygenase (amoA) gene abundance and nitrification potentials both spatially and temporally. Nitrification potentials differed along the estuary and over time, with the greatest nitrification potentials occurring mid-estuary (8.2 mol N grams dry weight [gdw] ؊1 day ؊1 in June, increasing to 37.4 mol N gdw ؊1 day ؊1 in January). At the estuary head, the nitrification potential was 4.3 mol N gdw ؊1 day ؊1 in June, increasing to 11.7 mol N gdw ؊1 day ؊1 in January. At the estuary head and mouth, nitrification potentials fluctuated throughout the year. AOB amoA gene abundances were significantly greater (by 100-fold) than those of AOA both spatially and temporally. Nitrosomonas spp. were detected along the estuary by denaturing gradient gel electrophoresis (DGGE) band sequence analysis. In conclusion, AOB dominated over AOA in the estuarine sediments, with the ratio of AOB/AOA amoA gene abundance increasing from the upper (freshwater) to lower (marine) regions of the Colne estuary. These findings suggest that in this nutrified estuary, AOB (possibly Nitrosomonas spp.) were of major significance in nitrification. N itrification is central to the global nitrogen cycle, coupling ammonia production from mineralization of organic matter with denitrification. In estuaries, discharge of domestic and industrial waste as well as runoff from mineral fertilizers and nitrogen fixation may contribute to ammonium enrichment. Ammonia oxidation is considered to be the rate-limiting step of nitrification and is catalyzed by ammonia monooxygenase (AMO), which is encoded by the amoA gene. It was previously considered that autotrophic ammonia oxidation is carried out solely by ammonia-oxidizing bacteria (AOB). However, the discovery of a marine archaeon belonging to the thaumarchaea which also oxidizes ammonia showed that this is not the case (1, 2). Ammonia-oxidizing archaea (AOA) belonging to the phylum Thaumarchaeota (AOA) are widely distributed in terrestrial and aquatic environments (2, 3) and thus may be more important contributors to nitrification than was previously considered. While previous studies of marine sediments showed different patterns of either AOA or AOB dominance, in estuarine environments where gradients of salinity and ammonia concentrations occur, there may be a differential selection for ammonia-oxidizer populations along these gradients (4-9). It has been previously suggested that AOA are significant in estuarine nitrogen cycling (6) and that AOA were more abundant than ...

Recommendations for the Next Generation of Global Freshwater Biological Monitoring Tools

“…Yet despite the functional importance of these groups, and established NGS and qPCR approaches for quantifying them (e.g. Papaspyrou et al 2014;Li et al 2015;Lansdown et al 2016;Thompson et al 2016), they are still rarely included in monitoring of diversity change. Combining information on functionally important groups of microbes with eDNA based assessments of biodiversity could provide a new paradigm in monitoring, as it provides direct insights into the functional capacity and health of ecosystems.…”

Nanosilver inhibits nitrification and reduces ammonia‐oxidising bacterial but not archaeal amoA gene abundance in estuarine sediments

“…Exposure to 50 mg L −1 AgNPs resulted in significant decreases in AOB amoA gene abundance in both the low‐salinity (Hythe) and mesohaline (Wivenhoe) sediments, whilst AOA amoA gene abundances (although much lower than AOB), were not significantly affected. Whilst amoA gene copy numbers are an ideal indicator for AOB and AOA abundance, they cannot directly infer nitrifying activity (Wuchter et al ., ; Li et al ., ). Our findings, therefore, suggest that AgNPs may have a detrimental impact on AOB driven ammonia oxidation in estuarine environments.…”

“…Our study and that of Li et al . (), found greater AOB amoA gene abundance compared to AOA along the Colne estuary, suggesting that AOB may have a greater contribution to ammonia‐oxidation in this estuary. Our findings suggest that the accumulation of high levels of AgNPs may pose an immediate environmental risk to estuarine nitrification, and a further delayed risk to AOB abundance, especially where ammonia‐oxidation is potentially predominantly driven by AOB, like in the Colne estuary.…”

“…The focus of the current study is the River Colne estuary (Fig. ), a macrotidal, hypernutrified estuary in the United Kingdom, which demonstrates a gradient of salinity from the estuary head at the Hythe, through to the estuary mouth at Brightlingsea (Papaspyrou et al ., ; Li et al ., ). The estuary also has very high inorganic nitrogen levels in the upper estuary from inputs from the River Colne and a major sewage treatment works (Ogilvie et al ., ; Papaspyrou et al ., ; Li et al ., ).…”

“…Previously, Li et al . () found greater AOB amoA gene abundance compared to AOA along the Colne estuary, suggesting that AOB are proportionally more important contributors to ammonia‐oxidation in this estuary. In the Colne estuary, as Cl − concentrations increase downstream, we hypothesize that AgNP toxicity will be greater towards the estuary mouth compared to the estuary head.…”