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Symbiosis Revisited: Phosphorus and Acid Buffering Stimulate N2 Fixation but Not Sphagnum Growth

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Symbiosis Revisited: Phosphorus and Acid Buffering Stimulate N2 Fixation but Not Sphagnum Growth Biogeosciences, 14, 1111–1122, 2017 www.biogeosciences.net/14/1111/2017/ doi:10.5194/bg-14-1111-2017 © Author(s) 2017. CC Attribution 3.0 License. Symbiosis revisited: phosphorus and acid buffering stimulate N2 fixation but not Sphagnum growth Eva van den Elzen1, Martine A. R. Kox2, Sarah F. Harpenslager3, Geert Hensgens4, Christian Fritz1,5,6, Mike S. M. Jetten2, Katharina F. Ettwig2, and Leon P. M. Lamers1,7 1Department of Aquatic Ecology & Environmental Biology, Institute for Water and Wetland Research, Radboud University, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands 2Department of Microbiology, Institute for Water and Wetland Research, Radboud University, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands 3School of Biological and Chemical Sciences, Queen Mary University, Mile End Road, E1 4NS, London, UK 4Department of Physical Geography and Ecosystem Science, Lund University, Sölvegatan 12, 223 62 Lund, Sweden 5Centre for Energy and Environmental Studies, University of Groningen, Nijenborgh 6Sustainable Agriculture, Rhein-Waal University for Applied Science, Wiesenstraße 5, 47575 Kleve, Germany 7B-Ware Research Centre, Toernooiveld 1, 6525 ED Nijmegen, the Netherlands Correspondence to: Eva van den Elzen ([email protected]) Received: 9 September 2016 – Discussion started: 20 October 2016 Revised: 18 January 2017 – Accepted: 3 February 2017 – Published: 9 March 2017 Abstract. In pristine Sphagnum-dominated peatlands, the higher nitrogen fixation rates reported for minerotrophic (di)nitrogen (N2/ fixing (diazotrophic) microbial communi- and more nutrient-rich peatlands. In addition, nitrogen fix- ties associated with Sphagnum mosses contribute substan- ation was found to strongly depend on light, with rates 10 tially to the total nitrogen input, increasing carbon seques- times higher in light conditions suggesting high reliance on tration. The rates of symbiotic nitrogen fixation reported for phototrophic organisms for carbon. The contrasting effects Sphagnum peatlands, are, however, highly variable, and ex- of phosphorus and bicarbonate on Sphagnum spp. and their perimental work on regulating factors that can mechanisti- diazotrophic communities reveal strong differences in the op- cally explain this variation is largely lacking. For two com- timal niche for both partners with respect to conditions and mon fen species (Sphagnum palustre and S. squarrosum) resources. This suggests a trade-off for the symbiosis of ni- from a high nitrogen deposition area (25 kg N ha−1 yr−1/, we trogen fixing microorganisms with their Sphagnum hosts, in 15−15 found that diazotrophic activity (as measured by N2 la- which a sheltered environment apparently outweighs the less beling) was still present at a rate of 40 nmol N gDW−1 h−1. favorable environmental conditions. We conclude that micro- This was surprising, given that nitrogen fixation is a costly bial activity is still nitrogen limited under eutrophic condi- process. We tested the effects of phosphorus availability and tions because dissolved nitrogen is being monopolized by buffering capacity by bicarbonate-rich water, mimicking a Sphagnum. Moreover, the fact that diazotrophic activity can field situation in fens with stronger groundwater or surface significantly be upregulated by increased phosphorus addi- water influence, as potential regulators of nitrogen fixation tion and acid buffering, while Sphagnum spp. do not bene- rates and Sphagnum performance. We expected that the addi- fit, reveals remarkable differences in optimal conditions for tion of phosphorus, being a limiting nutrient, would stimulate both symbiotic partners and calls into question the regula- both diazotrophic activity and Sphagnum growth. We indeed tion of nitrogen fixation by Sphagnum under these eutrophic found that nitrogen fixation rates were doubled. Plant per- conditions. The high nitrogen fixation rates result in high ad- formance, in contrast, did not increase. Raised bicarbonate ditional nitrogen loading of 6 kg ha−1 yr−1 on top of the high levels also enhanced nitrogen fixation, but had a strong nega- nitrogen deposition in these ecosystems. tive impact on Sphagnum performance. These results explain Published by Copernicus Publications on behalf of the European Geosciences Union. 1112 E. van den Elzen et al.: Symbiosis revisited: phosphorus and acid buffering stimulate N2 fixation 1 Introduction exact nature of the Sphagnum-microorganism symbiosis re- mains unknown, i.e., a direct mutualism or an indirect inter- Nitrogen (N) availability is considered to limit or co-limit action, N fixed by cyanobacteria associated with Sphagnum primary production in pristine Sphagnum-dominated ecosys- was found to enhance Sphagnum growth (Berg et al., 2013). tems (Aerts et al., 1992; Lamers et al., 2000; Limpens and A high variation in rates of N2 fixation has been found not Berendse, 2003). Peat mosses (Sphagnum spp.) function as only for different species and different systems, but also for a filter that very effectively absorbs particularly ammonium similar ecosystem types at different locations. To our knowl- C − (NH4 / but also nitrate (NO3 / from atmospheric deposition, edge, the mechanistic explanation for this high variation of leading to N limitation in the rhizosphere of vascular plants symbiotic N2 fixation rates in Sphagnum peatlands is still (Lamers et al., 2000; Bragazza et al., 2004; Fritz et al., 2014). lacking. Since the availability of N determines primary production, In areas with high N deposition like in our field site in there appears to be a close link between the N and C cy- the Netherlands, the necessity for microorganisms with dia- cles (Hungate et al., 2003; Vitousek et al., 2013). This link zotrophic capacity to actually fix N2 can be expected to di- C is especially important in peatlands, which, by storing sub- minish, as NH4 availability usually leads to down-regulation stantial amounts of C, play an important role in global C cy- of the expression of the nitrogenase enzyme responsible cling (Ruesch and Gibbs, 2008; Clymo and Hayward, 1982). for N2 fixation (Dixon and Kahn, 2004). Nutrients other Being ecosystem engineers in peatlands, Sphagnum spp. pro- than N have been suggested to influence N2 fixation, es- duce recalcitrant litter, rich in phenolic compounds (Verho- pecially phosphorus (P) (Vitousek and Field, 1999), which even and Toth, 1995), and actively acidify their environment is generally the second nutrient limiting primary production (Clymo and Hayward, 1982). This, combined with moist, (Bieleski, 1973; Vance, 2001). P limitation has been shown to anaerobic conditions results in the accumulation of peat with play an important role in biomass growth and functioning of a high C content (Van Breemen, 1995). Recently, it has been peatlands (Larmola et al., 2013; Hill et al., 2014; Fritz et al., shown that the high N2 fixation activity of the Sphagnum mi- 2012) and appeared to control N2 fixation rates (Toberman crobiome could explain the discrepancy between low inputs et al., 2015; Vitousek et al., 2002; Chapin et al., 1991). Be- of atmospheric N and high N accumulation rates in the peat sides, isolated cyanobacteria were shown to be directly stim- of pristine Sphagnum peatlands (Vile et al., 2014), confirm- ulated by P (Mulholland and Bernhardt, 2005) and, in Azolla ing the strong link between C and N accumulation. On the spp., a fern species with symbiotic cyanobacteria within its other end, high atmospheric N deposition may compromise leaves, P was shown to drastically increase plant growth and the C sequestration function of peatlands by stimulating mi- N content (Cheng et al., 2010). In peat mosses from N-rich crobial processes such as overall decomposition (Bragazza et sites, increased P availability can be expected to complement al., 2006) and denitrification (Gruber and Galloway, 2008). the high N supply (Limpens et al., 2004) and lead to an in- N2 fixing microorganisms (diazotrophs) live on the sur- crease in photosynthesis (by 14 %) (Fritz et al., 2012) and face and inside dead hyaline cells of Sphagnum (Opelt et moss growth (by 42 %) (Carfrae et al., 2007). It is therefore al., 2007; Bragina et al., 2012; Larmola et al., 2014), form- expected that the addition of P will improve the performance ing a symbiosis with their host. A highly diverse micro- of the Sphagnum-microorganism association in high N depo- bial community, including Proteobacteria, Verrucomicrobia sition areas. and Cyanobacteria, has been found to colonize peat mosses Next to nutrient availability, the alkalinity and pH of the (Bragina et al., 2014), and many of these microorganisms environment is known to be a key biogeochemical factor af- have the capacity to fix N2 (Bragina et al., 2013; Kox et fecting Sphagnum presence and performance in peatlands − al., 2016). Also, in other bryophytes, like Hylocomiaceae (mires). Higher concentrations of bicarbonate (HCO3 / and (feather mosses), such a symbiotic relationship can be found concomitantly higher pH values (from 7.5 and upwards), with N2 fixing cyanobacteria, supplying up to 50 % of the through the influence of minerotrophic groundwater or sur- total N input in boreal forests (Rousk et al., 2013). These face water in rich fens, have been shown to hamper Sphag- phototrophic diazotrophs provide N to their host in exchange num growth (Clymo, 1973; Lamers et al., 1999). While for C compounds (Bay et al., 2013; Leppänen et al., 2013), the effect of environmental factors such as pH and nutrient a process that we refer to as a direct mutualism, with ref- availability
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