Denitrification by sulfur-oxidizing bacteria in a eutrophic lake

Abstract

Understanding the mechanistic controls of microbial denitrification is of central importance to both environmental microbiology and ecosystem ecology. Loss of nitrate (NO 3 − ) is often attributed to carbon-driven (heterotrophic) denitrification. However, denitrification can also be coupled to sulfur (S) oxidation by chemolithoautotrophic bacteria. In the present study, we used an in situ stable isotope ( 15 NO 3 − ) tracer addition in combination with molecular approaches to understand the contribution of sulfur-oxidizing bacteria to the reduction of NO 3 − in a eutrophic lake. Samples were incubated across a total dissolved sulfide (H 2 S) gradient (2 to 95 µM) between the lower epilimnion and the upper hypolimnion. Denitrification rates were low at the top of the chemocline (4.5 m) but increased in the deeper waters (5.0 and 5.5 m), where H 2 S was abundant. Concomitant with increased denitrification at depths with high sulfide was the production of sulfate (SO 4 2− ), suggesting that the added NO 3 − was used to oxidize H 2 S to SO 4 2− . Alternative nitrate removal pathways, including dissimilatory nitrate reduction to ammonium (DNRA) and anaerobic ammonium oxidation (anammox), did not systematically change with depth and accounted for 1 to 15% of the overall nitrate loss. Quantitative PCR revealed that bacteria of the Sulfurimonas genus that are known denitrifiers increased in abundance in response to NO 3 − addition in the treatments with higher H 2 S. Stoichiometric estimates suggest that H 2 S oxidation accounted for more than half of the denitrification at the depth with the highest sulfide concentration. The present study provides evidence that microbial coupling of S and nitrogen (N) cycling is likely to be important in eutrophic freshwater ecosystems.KEY WORDS: Denitrification · Nitrate reduction · Sulfur oxidation · Sulfur-driven denitrification · Sulfurimonas denitrificans · Sulfide · Wintergreen Lake Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 66: [283][284][285][286][287][288][289][290][291][292][293] 2012 Anaerobic sediments and biofilms of aquatic ecosystems are conducive to NO 3 − reduction; however, 15 N tracer studies often show that less than half of the total NO 3 − disappearance is attributable to direct denitrification (e.g. Mulholland et al. 2008). Such findings suggest that other microbial processes may be important for removing NO 3 − in freshwater ecosystems (Gardner et al. 2006, Burgin & Hamilton 2007, Gardner & McCarthy 2009. NO 3 − can also be reduced via dissimilatory nitrate reduction (DNRA) to ammonium (NH 4 + ) by fermentative bacteria as well as via denitrification or DNRA coupled to the chemolithoautotrophic oxidation of either sulfur (Brunet & Garcia-Gil 1996, Otte et al. 1999 or iron (Weber et al. 2006). The relative importance of DNRA and denitrification is germane to understanding the fate of NO 3 − because the NH 4 + produced by DNRA is biologically available, while N 2 , the predominant end-produc...

Buried particulate organic carbon stimulates denitrification and nitrate retention in stream sediments at the groundwater–surface water interface

“…In this mechanism, sulfide oxidation is coupled with NO 3 − reduction to NH 4 + or N 2 (Burgin and Hamilton 2007). If sulfide-driven NO 3 − reduction had been important, we would have expected NO 3 − loss along flow paths in the mesocosms to be coupled with SO 4 2-production (Burgin et al 2012). Instead, SO 4 2-concentrations decreased between 25 and 5 cm during the experiment, particularly on day 16 (RSS, unpublished data).…”

“…An additional possible mechanism for NO 3 − removal is immobilization of NO 2 − , produced from NO 3 − reduction, on organic matter surfaces in the sediments (Lewis and Kaye 2012). One alternative mechanism for NO 3 − removal, sulfurdriven NO 3 − reduction (Burgin et al 2012), probably was not important in our study. In this mechanism, sulfide oxidation is coupled with NO 3 − reduction to NH 4 + or N 2 (Burgin and Hamilton 2007).…”

Effect of Temperature on Oxygen Profiles and Denitrification Rates in Freshwater Sediments

“…Denitrification is carried out by a wide range of microorganisms, most of which are facultative anaerobes, which will only denitrify once oxygen becomes limiting (Knowles 1982). Denitrifiers use organic carbon (canonical heterotrophic denitrification), sulphide, or hydrogen (chemolithoautotrophic denitrification) as an electron donor (Burgin et al 2012). Or, in the special case of methane-oxidation dependent denitrification, methane reduction and oxidation are coupled to nitrite dismutation (Ettwig et al 2010;Stein and Klotz 2016).…”

A global perspective on wetland salinization: ecological consequences of a growing threat to freshwater wetlands

“…Increased ionic strength can also interfere with the enzymes associated with denitrification (Glass and Silverstein 1999 as cited in Laverman et al 2007). Substantial denitrification can also be driven by the use of H 2 S and FeS as electron donors, but only in the presence of sufficient NO 3 À thus, if nitrification is inhibited, no increase in denitrification would be expected (Brettar and Rheinheimer 1991, Haaijer et al 2006, Burgin and Hamilton 2007, Burgin et al 2012. High Cl À concentrations can also inhibit both nitrification and denitrification, but microbial communities appear to be able to adapt to high concentrations over time (Hale and Groffman 2006).…”