Vascular Plant Success in a Warming Antarctic May Be Due to Efficient Nitrogen Acquisition

LETTERS PUBLISHED ONLINE: 29 MARCH 2011 | DOI: 10.1038/NCLIMATE1060 Vascular plant success in a warming Antarctic may be due to efficient nitrogen acquisition Paul W. Hill1*, John Farrar1, Paula Roberts1, Mark Farrell1,2(, Helen Grant3, Kevin K. Newsham4, David W. Hopkins5,6(, Richard D. Bardgett2 and Davey L. Jones1 For the past 50 years there has been rapid warming in the maritime Antarctic1–3, with concurrent, and probably temperature-mediated, proliferation of the two native plants, Antarctic pearlwort (Colobanthus quitensis) and especially Antarctic hair grass (Deschampsia antarctica)4–10. In many terrestrial ecosystems at high latitudes, nitrogen (N) supply regulates primary productivity11–13. Although the predominant view is that only inorganic and amino acid N are important sources of N for angiosperms, most N enters soil as protein. Maritime Antarctic soils have large stocks of proteinaceous N, which is released slowly as decomposition is limited by low temperatures. Consequently, an ability to acquire N at an early stage of availability is key to the success of photosynthetic organisms. Here we show that D. antarctica can acquire N through its roots as short peptides, produced at an early stage of protein decomposition, acquiring N over three times faster than as amino acid, nitrate or ammonium, and more than 160 times faster than the mosses with which it competes. Efficient Figure 1 j D. antarctica growing in competition with moss at Moss Braes, acquisition of the N released in faster decomposition of soil Signy Island. organic matter as temperatures rise14 may give D. antarctica an advantage over competing mosses that has facilitated its animal faeces, plants are largely dependent on N which enters recent proliferation in the maritime Antarctic. the soil as protein. Thus growth is limited by the rate at which Over the past 50 years some areas of the maritime Antarctic have protein is decomposed to a form in which plants are able to warmed at rates almost an order of magnitude greater than the acquire and use it. Historically, it was thought that plants were 1 − C global mean . Although bryophytes still dominate the vegetation, wholly dependent on inorganic N (NO3 and NH4 ) for their during this period there have typically been order of magnitude nitrogen. Consequently, primary productivity in N-limited systems increases in the size of most populations of Deschampsia antarctica was thought to be controlled by the rates of protein cleavage to Desv.4,5,9,15. In the maritime Antarctic, D. antarctica is most fre- amino acids and subsequent mineralization to ammonium and quently found growing either where moss has been present and has nitrate by soil microbes. However, microbial N mineralization in died, or with living moss, particularly Sanionia uncinata (Hedw.) polar soils is often too slow to meet plant N requirements13,24. We Loeske, which is a primary colonist16–21 (Fig. 1). Prior colonization now know that some Arctic vascular plants can avoid N limitation by other organisms increases the availability of nutrients (Table 1; from slow N mineralization by using amino acid N directly13,25. Supplementary Table S1), but in the presence of living moss, Acquisition of this organic N requires plants to compete successfully D. antarctica must compete for both light and nutrients. The upright with soil microbes. Recently, it has been shown that in the absence leaves of D. antarctica penetrate through moss and enable it to of soil, plants are able to use protein N when cleaved only to intercept light efficiently even when occupying little ground area short-chain peptides26 (Fig. 2; Supplementary Fig. S1), and here we relative to competing moss (Fig. 1). Although both D. antarctica and demonstrate that this process has real ecological significance. We S. uncinata have temperature optima for photosynthesis above cur- show that short peptides are an important component of the N cycle rent summer mean temperatures in the maritime Antarctic22,23, suc- of the maritime Antarctic. We further show that D. antarctica can cessful competition for nutrients is essential if the beneficial effects both acquire organic N in the presence of soil microbes, and is much of warming on carbon fixation are to be exploited. better adapted to access the N, which becomes available as stored Neither species of Antarctic angiosperm has a N2-fixing proteinaceous soil organic matter breaks down, than are the mosses symbiosis. Consequently, in areas where there are low inputs of with which it competes. 1Environment Centre Wales, Bangor University, Bangor, Gwynedd LL57 2UW, UK, 2Soil and Ecosystem Ecology, Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK, 3Life Sciences Mass Spectrometry Facility, Lancaster Environment Centre, Lancaster LA1 4AP, UK, 4Ecosystems Programme, British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 OET, UK, 5Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, UK, 6School of Biological and Environmental Sciences, University of Stirling, Stirling FK9 4LA, UK. (Present address: CSIRO Land and Water, PMB2, Glen Osmond, SA, 5064, Australia (M.F.); School of Life Sciences, Heriot-Watt University, Riccarton, Edinburgh EH14 4AS, UK (D.W.H.). *e-mail: [email protected]. 50 NATURE CLIMATE CHANGE j VOL 1 j APRIL 2011 j www.nature.com/natureclimatechange © 2011 Macmillan Publishers Limited. All rights reserved. NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1060 LETTERS Table 1 j Total, inorganic, peptide and amino acid N in soil Protein solution. Protease Soil Concentration Per cent of total Root microbes Soil particle (µmol N l−1) soluble N All moss and grass sites sampled (n D 39) Peptides Total soluble N 346±42 C Peptidase NH4 12±2 4±0:6 − NO3 238±37 63±4 Free amino acids 0:9±0:2 0:3±0:03 Amino Peptides <1 kDa 52±11 22±4 acids D. antarctica (n D 20) Deaminase Total soluble N 428±75 C NH4 11±2 4±1 − NO3 336±63 72±5 ± ± Free amino acids 1:3 0:3 0:3 0:05 + 4 Peptides <1 kDa 44±10 21±5 + NH4 NH S. uncinata (n D 11) Total soluble N 262±16 C NH4 14±2 5±0:8 − NO3 124±20 50±9 ¬ Free amino acids 0:6±0:08 0:2±0:03 NO3 Peptides <1 kDa 77±32 29±12 Mixed moss and grass (n D 8) Figure 2 j Schematic showing soil N transformations before uptake by Total soluble N 255±59 plant roots. C NH4 10±5 3±1 − NO3 151±42 56±8 (C12H22N4O5) was faster (P ≤ 0:02) than as alanine, dialanine ± ± − Free amino acids 0:7 0:4 0:2 0:07 (C6H12N2O3) or NO3 . Despite the higher N content of peptides, Peptides <1 kDa 35±7 15±3 uptake of 15N by D. antarctica was 60–600% faster (P ≤ 0:006) C Fellfield (n D 6) as NH4 than in any other form. Roots of D. antarctica were Total soluble N 54±9 soil-free, but not sterile. Consequently, although D. antarctica is C NH4 9±5 13±5 not mycorrhizal, it is possible that N uptake by D. antarctica − 27 NO3 18±5 35±10 roots was mediated by association with dark septate fungi . Free amino acids 0:9±0:3 2±0:8 We evaluated the likelihood of this route of uptake based on 13 Peptides <1 kDa 27±8 46±9 the location of recovered C and measurement of extracellular peptidase activity. In both soils and plants, 15N and 13C were Solutions were extracted from underneath D. antarctica, S. uncinata, and mostly bare lichen- co-located and we found no extracellular peptide cleavage in Andreaea spp. (fellfield) vegetation on Signy Island. Fellfield represents tundra with no higher plants present. Values are mean±s:e:m: soil solution (Supplementary Table S2; Supplementary Fig. S3). Further, microscopic examination revealed no evidence of fungal colonization of roots (D. Murphy, personal communication). This We carried out experimental work on Signy Island (60◦ 430 S, strongly suggests that amino acid and peptides were taken up intact 45◦ 360 W) in the South Orkney Islands. Signy has recently been without prior cleavage or mineralization. As would be expected subject to rapid warming2 and has an expanding population of D. from the rapid respiration of peptide and amino acid C following antarctica9 (S. Favero-Longo, personal communication, February uptake by plants28 (Supplementary Fig. S1), less of the added 2009). We determined the size of the pool of soluble peptides and 13C was recovered than 15N. We used the difference between 13C amino acids likely to be available to plants by sampling soil solution and 15N recovery to determine respiratory losses of peptide and from 10 locations around Signy in early December 2008. In soils amino acid C. As a proportion of that taken up during 30 min of dominated by D. antarctica, S. uncinata or mixed communities exposure to substrates, plants respired approximately twice as much of the two species, the pool of small (<1 kDa) soluble peptides 13C as soil microbes (17 ± 2 and 33 ± 2% of uptake, respectively; was about 22% of total soluble N. Free amino acids constituted P < 0:001; mean±s:e:m:; n D 12; Supplementary Table S2). Using about 0.3% of total soluble N (Table 1). Solute concentrations the respiration rate of peptide and amino acid C as an indicator of were spatially variable, but did not differ significantly between D. minimal N assimilation, N assimilation by D. antarctica was faster antarctica, S. uncinata or mixed communities. (P ≤0:03) as trialanine (C9H17N3O4) and tetraalanine (92 and 97%, We supplied 13C- and 15N-labelled inorganic, amino acid and respectively) than as the amino acid monomer, but the rate of N peptidic forms of N to both soil and D.

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