Shifts in the relative abundance of ammonia‐oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary

Abstract

Submarine groundwater discharge to coastal waters can be a significant source of both contaminants and biologically limiting nutrients. Nitrogen cycling across steep gradients in salinity, oxygen and dissolved inorganic nitrogen in sandy 'subterranean estuaries' controls both the amount and form of nitrogen discharged to the coastal ocean. We determined the effect of these gradients on betaproteobacterial ammonia-oxidizing bacteria (beta-AOB) and ammonia-oxidizing archaea (AOA) in a subterranean estuary using the functional gene encoding ammonia monooxygenase subunit A (amoA). The abundance of beta-AOB was dramatically lower in the freshwater stations compared with saline stations, while AOA abundance remained nearly constant across the study site. This differing response to salinity altered the ratio of beta-AOB to AOA such that bacterial amoA was 30 times more abundant than crenarchaeal amoA at the oxic marine station, but nearly 10 times less abundant at the low-oxygen fresh and brackish stations. As the location of the brackish mixing zone within the aquifer shifted from landward in winter to oceanward in summer, the location of the transition from a beta-AOB-dominated to an AOA-dominated community also shifted, demonstrating the intimate link between microbial communities and coastal hydrology. Analysis of ammonia-oxidizing enrichment cultures at a range of salinities revealed that AOA persisted solely in the freshwater enrichments where they actively express amoA. Diversity (as measured by total richness) of crenarchaeal amoA was high at all stations and time points, in sharp contrast to betaproteobacterial amoA for which only two sequence types were found. These results offer new insights into the ecology of AOA and beta-AOB by elucidating conditions that may favour the numerical dominance of beta-AOB over AOA in coastal sediments.

Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest

“…Based on these contradictory results, we suggest further experiments under field conditions to substantiate that decreasing soil temperature promotes AOA abundance. Our results suggested a potential dependence of AOA on ammonia availability, which was supported by recent studies (He et al, 2007;Santoro et al, 2008). Because of the negative correlation between AOA and ammonia concentrations, we conclude that the ammonia decrease may have been the consequence of pronounced ammonia oxidation activity in the assayed temperate soils, whereas Valentine, (2007) proposed that AOA seem to be better adapted to low ammonia concentrations in soil.…”

Metatranscriptomic analysis of ammonia-oxidizing organisms in an estuarine bacterioplankton assemblage

“…From these studies, it appears that the relative abundance of ammonia-oxidizing bacteria (AOB) increases in estuaries relative to coastal waters or the open ocean. The environmental factors responsible for the success of AOB vs AOA in estuarine and coastal waters are not known, but the shift correlates with salinity in some systems (Caffrey et al, 2007;Mosier and Francis, 2008;Santoro et al, 2008;Magalhaes et al, 2009;Bernhard et al, 2010). However, the success of one group over the other is not likely to be directly based on salinity, as AOA can be dominant in the oligohaline reaches of some estuaries (Mosier and Francis, 2008) and in soils (Prosser and Nicol, 2008).…”

“…Most studies of AOA populations in estuaries (Francis et al, 2005;Beman and Francis, 2006;Caffrey et al, 2007;Mosier and Francis, 2008;Santoro et al, 2008;Magalhaes et al, 2009;Bernhard et al, 2010) have focused on sediments. From these studies, it appears that the relative abundance of ammonia-oxidizing bacteria (AOB) increases in estuaries relative to coastal waters or the open ocean.…”

Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation

“…Phylogenetic analysis of 16S rRNA and amoA genes DNA was extracted and purified from 25 ml of culture after vacuum filtration onto 25 mm diameter, 0.2 mm pore size Supor membrane filters (Pall, Port Washington, NY, USA) using DNeasy columns (Qiagen, Valencia, CA, USA) as previously described (Santoro et al, 2008). Genes encoding for the 16S ribosomal RNA (rRNA) and the a subunit of ammonia monooxygenase (amoA), believed to contain the catalytic site for ammonia oxidation (Hyman and Wood, 1985), were amplified using PCR.…”