Genetic and environmental controls on nitrous oxide accumulation in lakes.

Jatta Saarenheimo,Marja Tiirola,Lauri Arvola,Antti J Rissanen,Moritz F Lehmann,Hannu Nykänen,Yiguo Hong

doi:10.1371/journal.pone.0121201

Jatta Saarenheimo, Marja Tiirola + Show 5 more

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https://doi.org/10.1371/journal.pone.0121201

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Abstract

We studied potential links between environmental factors, nitrous oxide (N2O) accumulation, and genetic indicators of nitrite and N2O reducing bacteria in 12 boreal lakes. Denitrifying bacteria were investigated by quantifying genes encoding nitrite and N2O reductases (nirS/nirK and nosZ, respectively, including the two phylogenetically distinct clades nosZ I and nosZ II) in lake sediments. Summertime N2O accumulation and hypolimnetic nitrate concentrations were positively correlated both at the inter-lake scale and within a depth transect of an individual lake (Lake Vanajavesi). The variability in the individual nirS, nirK, nosZ I, and nosZ II gene abundances was high (up to tenfold) among the lakes, which allowed us to study the expected links between the ecosystem’s nir-vs-nos gene inventories and N2O accumulation. Inter-lake variation in N2O accumulation was indeed connected to the relative abundance of nitrite versus N2O reductase genes, i.e. the (nirS+nirK)/nosZ I gene ratio. In addition, the ratios of (nirS+nirK)/nosZ I at the inter-lake scale and (nirS+nirK)/nosZ I+II within Lake Vanajavesi correlated positively with nitrate availability. The results suggest that ambient nitrate concentration can be an important modulator of the N2O accumulation in lake ecosystems, either directly by increasing the overall rate of denitrification or indirectly by controlling the balance of nitrite versus N2O reductase carrying organisms.

Highlights

Nitrous oxide (N2O) is an important greenhouse gas and the single most important ozone destroying chemical [1]
Neither environmental factors nor N2O accumulation showed any significant correlation with the gene abundance, gene copy numbers, or with nirS/nirK or nosZI/nosZII gene ratios (Pearson correlations, p values >0.05)
A negative correlation was observed with respect to the oxygen concentration (r = -0.90 and p = 0.002) and temperature (r = -0.95 and p < 0.001). This is the first study combining N2O measurements and molecular analyses of denitrification genes in lake ecosystems. This is the first time that the abundance of nirS and nirK genes together with both clades of nosZ genes were investigated in freshwater sediments

Summary

Introduction

Nitrous oxide (N2O) is an important greenhouse gas and the single most important ozone destroying chemical [1]. Since denitrifier community structure is likely to have an effect on net N2O production and emission [11, 12], denitrifier communities have been studied through the analysis of sequence variation and/or the abundance of nirS, nirK, and nosZ genes in many ecosystems [13, 14, 15, 16, 17]. High availability of nitrate and nitrite has been shown to be conducive to N2O accumulation [18, 19], fostering the increase the N2O/(N2O+N2) ratio in the gaseous denitrification products [20, 21]. We evaluated genetic and environmental factors that likely modulate N2O production and accumulation in lake ecosystems, especially focusing on the benthic abundance of nirS, nirK, nosZI, and nosZII genes during the summertime N2O accumulation period. High-nitrate lakes Mean (±SE) Low-nitrate lakes Mean (±SE) Pairwise test results High vs. low nitrate

Results

Discussion

Experimental Procedures