N2-fixation by methanotrophs sustains carbon and nitrogen accumulation in pristine peatlands

Abstract

Symbiotic relationships between N 2 -fixing prokaryotes and their autotrophic hosts are essential in nitrogen (N)-limited ecosystems, yet the importance of this association in pristine boreal peatlands, which store 25 % of the world's soil (C), has been overlooked. External inputs of N to bogs are predominantly atmospheric, and given that regions of boreal Canada anchor some of the lowest rates found globally (*1 kg N ha -1 year -1), biomass production is thought to be limited primarily by N. Despite historically low N deposition, we show that boreal bogs have accumulated approximately 12-25 times more N than can be explained by atmospheric inputs.Here we demonstrate high rates of biological N 2 -fixation in prokaryotes associated with Sphagnum mosses that can fully account for the missing input of N needed to sustain high rates of C sequestration. Additionally, N amendment experiments in the field did not increase Sphagnum production, indicating that mosses are not limited by N. Lastly, by examining the composition and abundance of N 2 -fixing prokaryotes by quantifying gene expression of 16S rRNA and nitrogenase-encoding nifH, we show that rates of N 2 -fixation are driven by the substantial contribution from methanotrophs, and not from cyanobacteria. We conclude biological N 2 -fixation drives high sequestration of C in pristine peatlands, and may play an important role in moderating fluxes of methane, one of the most important greenhouse gases produced in peatlands. Understanding the mechanistic controls on biological N 2 -fixation is crucial for assessing the fate Responsible Editor: Matthew Wallenstein.Electronic supplementary material The online version of this article (doi:10.1007/s10533-014-0019-6) contains supplementary material, which is available to authorized users. Biogeochemistry (2014) 121:317-328 DOI 10.1007 of peatland carbon stocks under scenarios of climate change and enhanced anthropogenic N deposition.

Long-term macronutrient stoichiometry of UK ombrotrophic peatlands

“…If we assume that N:P for preindustrial atmospheric deposition is 10:1 (rounded average of dust - Lawrence and Neff, 2009;vegetation and litter -Wang et al, 2015; forest fire smoke - Zhang et al, 2002), then based on the long-term mean atmospheric P loading calculated above we can expect 0.38 gN m −2-year −1 from atmosphere. This leaves 0.8 g m −2 year −1 to be supplied through biological N fixation, rather lower than has been measured in Alberta peat bogs (Vile et al, 2014;1.7 to 3.4 g m − 2 year − 1 ). If denitrification was active in peat bogs prior to modern N deposition, then our estimate for average long-term N fixation would be proportionately higher.…”

“…As with P, plant cycling has been shown to transport mineralised N to the bog surface (Vile et al, 2014) contributing to surface enrichment. However, it is generally regarded that differences in decay rates of C and N in peat have a greater influence over the N concentration.…”

Effects of nitrogen fertilization on diazotrophic activity of microorganisms associated with Sphagnum magellanicum

“…Therefore, deprivation of methane during the complete experimental phase might have contributed to the observed decrease in N 2 fixation activity. Especially for mosses from the low N-deposition site, where the strongest decrease in N 2 fixation activity was observed, since for similar pristine sites methanotrophic diazotrophs have been shown to contribute to N 2 fixation significantly (Vile et al 2014).…”

“…Similarly, along a natural gradient of N deposition levels, the diazotrophic activity (mainly of cyanobacteria) associated with the forest mosses Hylocomium splendens and P. schreberi was shown to decrease with increasing N deposition levels (Leppänen et al 2013). Studies on the effect of N fertilization on S. fuscum and S. angustifolium-associated diazotrophs in a pristine peat bog showed that the diazotrophic activity was negatively affected by high N input, although moss productivity did not change (Vile et al 2014). The difference in response pattern to N deposition between the study of Rousk et al (2013b) and the others indicates that increased N deposition may not have a uniform effect on diazotrophs in all moss species.…”

“…In a Canadian ombrotrophic bog, investigation of the active diazotrophic community showed higher relative abundance of nifH transcripts originating from methanotrophs than those from cyanobacteria (Vile et al 2014). Nevertheless, many questions on the relative importance of different diazotrophic microorganisms in peat mosses remain and in contrast to plant communities, the effect of N deposition on microbial assemblages in peatlands has been less well explored (Bodelier 2011;Andersen et al 2012;Ho and Bodelier 2015).…”