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Rising CO2 accelerates phosphorus and molybdenum limitation of N2-fixation in young tropical trees

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Abstract

Background and aims

Nitrogen fixation may be critical for supplying the nitrogen (N) needed to maintain the tropical carbon sink in a world of rising atmospheric CO2. However, we do not know whether increased CO2 acts to exacerbate nutrient limitation on the fixation process itself. We experimentally test this idea by growing N2-fixing plants in pre-Industrial (280 ppm), present-day (400 ppm), and doubled (800 ppm) atmospheric CO2.

Methods

In a greenhouse experiment, we grew tree seedlings from N2-fixing species and a non-fixing species at three CO2 concentrations with control, +P (phosphorus), +Mo (molybdenum), and + P +Mo nutrient treatments.

Results

We found nutrient limitation to be minimal at pre-Industrial CO2, but with increasing CO2 fixer growth and fixation became increasingly limited by P and by a P-by-Mo interaction. At 400 ppm, plants with +P grew ~50% faster and fixed 10-15× more N2 based on nodule mass and nitrogenase activity. At 800 ppm, plants with +P +Mo grew 200% more, and fixed 25× more N2, suggesting Mo-P co-limitation at elevated CO2.

Conclusion

Our findings imply that complex patterns of nutrient limitation can develop as CO2 rises, potentially suppressing tropical N2-fixation and the new inputs of N needed to sustain the tropical carbon sink.

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References

  • Alberty R (2005) Thermodynamics of the mechanism of the nitrogenase reaction. Biophys Chem 114:115–120

    Article  PubMed  CAS  Google Scholar 

  • Arnone JA, Gordon JC (1990) Effect of nodulation, nitrogen fixation and CO2 enrichment on the physiology, growth and dry mass allocation of seedlings of Alnus rubra bong. New Phytol 116:55–66. https://doi.org/10.1111/j.1469-8137.1990.tb00510.x

    Article  CAS  Google Scholar 

  • Barron A, Purves D, Hedin L (2011) Facultative nitrogen fixation by canopy legumes in a lowland tropical forest. Oecologia 165:511–520. https://doi.org/10.1007/s00442-010-1838-3

    Article  PubMed  Google Scholar 

  • Barron AR (2007) Patterns and controls of nitrogen fixation in a lowland tropical forest, Panama. Princeton university

  • Barron AR, Wurzburger N, Bellenger JP, Wright SJ, Kraepiel AML, Hedin LO (2008) Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat Geosci 2:42–45

    Article  CAS  Google Scholar 

  • Batterman SA, Hedin LO, van Breugel M, Ransijn J, Craven DJ, Hall JS (2013a) Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502:224–227. https://doi.org/10.1038/nature12525

    Article  PubMed  CAS  Google Scholar 

  • Batterman SA, Wurzburger N, Hedin LO (2013b) Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J Ecol 101:1400–1408. https://doi.org/10.1111/1365-2745.12138

    Article  CAS  Google Scholar 

  • Boddey RM, Peoples MB, Palmer B, Dart PJ (2000) Use of the 15N natural abundance technique to quantify biological nitrogen fixation by woody perennials. Nutr Cycl Agroecosyst 57:235–270. https://doi.org/10.1023/a:1009890514844

    Article  Google Scholar 

  • Cernusak LA, Winter K, Aranda J, Turner BL, Marshall JD (2007) Transpiration efficiency of a tropical pioneer tree (Ficus insipida) in relation to soil fertility. J Exp Bot 58:3549–3566. https://doi.org/10.1093/jxb/erm201

    Article  PubMed  CAS  Google Scholar 

  • Cernusak LA, Winter K, Martínez C, Correa E, Aranda J, Garcia M, Jaramillo C, Turner BL (2011) Responses of legume versus nonlegume tropical tree seedlings to elevated CO2 concentration. Plant Physiol 157:372–385

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chou CB, Hedin LO, Pacala SW (2018) Functional groups, species and light interact with nutrient limitation during tropical rainforest sapling bottleneck. J Ecol 106:157–167

    Article  CAS  Google Scholar 

  • Coley P, Massa M, Lovelock C, Winter K (2002) Effects of elevated CO2 on foliar chemistry of saplings of nine species of tropical tree. Oecologia 133:62–69

    Article  PubMed  CAS  Google Scholar 

  • Dalling JW, Cernusak LA, Winter K, Aranda J, Garcia M, Virgo A, Cheesman AW, Baresch A, Jaramillo C, Turner BL (2016) Two tropical conifers show strong growth and water-use efficiency responses to altered CO2 concentration. Ann Bot 118:1113–1125. https://doi.org/10.1093/aob/mcw162

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dalling JW, Winter K, Andersen KM, Turner BL (2013) Artefacts of the pot environment on soil nutrient availability: implications for the interpretation of ecological studies. Plant Ecol 214:329–338. https://doi.org/10.1007/s11258-013-0172-3

    Article  Google Scholar 

  • Eady RR (1996) Structure-function relationships of alternative nitrogenases. Chem Rev 96:3013–3030. https://doi.org/10.1002/chin.199710280

    Article  PubMed  CAS  Google Scholar 

  • Finzi A, Moore D, DeLucia E, Lichter J, Hofmockel K, Jackson R, Kim H, Matamala R, McCarthy H, Oren R (2006) Progressive nitrogen limitation of ecosystem processes under elevated CO2 in a warm-temperate forest. Ecology 87:15–25

    Article  PubMed  Google Scholar 

  • Gerber S, Hedin LO, Oppenheimer M, Pacala SW, Shevliakova E (2010) Nitrogen cycling and feedbacks in a global dynamic land model. Glob Biogeochem Cycles 24

  • Gifford RM, Barrett DJ, Lutze JL (2000) The effects of elevated [CO2] on the C: N and C: P mass ratios of plant tissues. Plant Soil 224:1–14

    Article  CAS  Google Scholar 

  • Gutschick V (1981) Evolved strategies in nitrogen acquisition by plants. Am Nat 118:607–637

    Article  CAS  Google Scholar 

  • Hardy R, Holsten R, Jackson E, Burns R (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hedin LO, Brookshire ENJ, Menge DNL, Barron AR (2009) The nitrogen paradox in tropical forest ecosystems. Annual Review of Ecology, Evolution, and Systematics 40:613–635

    Article  Google Scholar 

  • Houlton B, Sigman D, Hedin L (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci 103:8745–8750

    Article  PubMed  CAS  Google Scholar 

  • Houlton BZ, Sigman DM, Schuur EAG, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci 104:8902–8906

    Article  PubMed  CAS  Google Scholar 

  • Huante P, Rincon E, Acosta I (1995) Nutrient availability and growth rate of 34 Woody species from a tropical deciduous Forest in Mexico. Funct Ecol 9:849–858. https://doi.org/10.2307/2389982

    Article  Google Scholar 

  • Hungate B, Stiling P, Dijkstra P, Johnson D, Ketterer M, Hymus G, Hinkle C, Drake B (2004) CO2 elicits long-term decline in nitrogen fixation. Science 304:1291

    Article  PubMed  CAS  Google Scholar 

  • Hungate BA, Dijkstra PL, Johnson DEW, Hinkle CRS, Drake BTG (1999) Elevated CO2 increases nitrogen fixation and decreases soil nitrogen mineralization in Florida scrub oak. Glob Chang Biol 5:781–789

    Article  Google Scholar 

  • Hungate BA, Dukes JS, Shaw MR, Luo Y, Field CB (2003) Nitrogen and climate change. Science 302:1512–1513

    Article  PubMed  CAS  Google Scholar 

  • Le Roux MR, Khan S, Valentine AJ (2008) Organic acid accumulation may inhibit N2 fixation in phosphorus-stressed lupin nodules. New Phytol 177:956–964. https://doi.org/10.1111/j.1469-8137.2007.02305.x

    Article  PubMed  CAS  Google Scholar 

  • Le Roux MR, Ward CL, Botha FC, Valentine AJ (2006) Routes of pyruvate synthesis in phosphorus-deficient lupin roots and nodules. New Phytol 169:399–408. https://doi.org/10.1111/j.1469-8137.2005.01594.x

    Article  PubMed  CAS  Google Scholar 

  • Lovelock C, Virgo A, Popp M, Winter K (1999) Effects of elevated CO2 concentrations on photosynthesis, growth and reproduction of branches of the tropical canopy tree species, Luehea seemannii Tr. & planch. Plant. Cell & Environ 22:49–59

    Article  Google Scholar 

  • LPWG (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny the legume phylogeny working group (LPWG). Taxon 66:44–77. https://doi.org/10.12705/661.3

    Article  Google Scholar 

  • McKey (1994) Legumes and nitrogen: the evolutionary ecology of a nitrogen-demanding lifestyle. In: Sprent J, McKey D (eds) Advances in Legume Systematics, Part 5: The Nitrogen Factor. Royal Botanical Garden, Kew

    Google Scholar 

  • Mendieta-Araica B, Spörndly E, Reyes-Sánchez N, Salmerón-Miranda F, Halling M (2013) Biomass production and chemical composition of Moringa oleifera under different planting densities and levels of nitrogen fertilization. Agrofor Syst 87:81–92. https://doi.org/10.1007/s10457-012-9525-5

    Article  Google Scholar 

  • Minchin FR, Witty JF, Sheehy JE, MÜLler M (1983) A major error in the acetylene reduction assay: decreases in nodular Nitrogenase activity under assay conditions. J Exp Bot 34:641–649. https://doi.org/10.1093/jxb/34.5.641

    Article  CAS  Google Scholar 

  • Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci 107:19368–19373

    Article  PubMed  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Rastetter EB, Vitousek PM, Field C, Shaver GR, Herbert D, gren GI (2001) Resource optimization and symbiotic nitrogen fixation. Ecosystems 4:369–388. https://doi.org/10.1007/s10021-001-0018-z

    Article  CAS  Google Scholar 

  • Sprent JI, Ardley J, James EK (2017) Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol 215:40–56. https://doi.org/10.1111/nph.14474

    Article  PubMed  CAS  Google Scholar 

  • Sprent JI, Ardley JK, James EK (2013) From north to south: a latitudinal look at legume nodulation processes. S Afr J Bot 89:31–41. https://doi.org/10.1016/j.sajb.2013.06.011

    Article  Google Scholar 

  • Thomas R, Bashkin M, Richter D (2000) Nitrogen inhibition of nodulation and N2 fixation of a tropical N2 fixing tree (Gliricidia sepium) grown in elevated atmospheric CO2. New Phytol 145:233–243

    Article  CAS  Google Scholar 

  • Tissue DT, Megonigal JP, Thomas RB (1996) Nitrogenase activity and N2-fixation are stimulated by elevated CO2 in a tropical N2-fixing tree. Oecologia 109:28–33. https://doi.org/10.1007/s004420050054.

    Article  PubMed  CAS  Google Scholar 

  • Turner BL, Engelbrecht BMJ (2011) Soil organic phosphorus in lowland tropical rain forests. Biogeochemistry:1–19

  • van Kessel C, Roskoski J (1983) Nodulation and N2 fixation by Inga jinicuil, a woody legume in coffee plantations. Plant Soil 72:95–105. https://doi.org/10.1007/BF02185099

    Article  Google Scholar 

  • Vance C, Heichel G (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu Rev Plant Biol 42:373–390

    Article  CAS  Google Scholar 

  • Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philosophical Transactions of the Royal Society B: Biological Sciences 368. https://doi.org/10.1098/rstb.2013.0119

  • Winter K, Garcia M, Gottsberger R, Popp M (2001) Marked growth response of communities of two tropical species to elevated CO2 when soil nutrient limitation is removed. Flora 196:47–58

    Article  Google Scholar 

  • Winter K, Garcia M, Lovelock C, Gottsberger R, Popp M (2000) Responses of model communities of two tropical tree species to elevated atmospheric CO2: growth on unfertilized soil. Flora 195:289–302

    Article  Google Scholar 

  • Witty J, Minchin F (1988) Measurement of nitrogen fixation by the acetylene reduction assay; myths and mysteries. Nitrogen fixation by legumes in Mediterranean agriculture. Springer

  • Wurzburger N, Bellenger JP, Kraepiel AML, Hedin LO (2012) Molybdenum and phosphorus interact to constrain Asymbiotic nitrogen fixation in tropical forests. PLoS One 7: e33710

  • Wurzburger N, Hedin LO (2015) Taxonomic identity determines N2 fixation by canopy trees across lowland tropical forests. Ecol Lett

  • Zalamea P-C, Turner BL, Winter K, Jones FA, Sarmiento C, Dalling JW (2016) Seedling growth responses to phosphorus reflect adult distribution patterns of tropical trees. New Phytol 212:400–408. https://doi.org/10.1111/nph.14045

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Jorge Aranda, Jose Salas, Aurelio Virgo, Ben Turner, David Roubik, Jack Burdette, Cleo Chou, Andrew Budnick, and Eskender McCoy for assistance with plant growth and the harvests. Funding was provided by the National Science Foundation (GRFP), Walbridge Fellowship, Princeton Energy and Climate Scholars, and the Smithsonian Tropical Research Institute. A.M.T. was recipient of a Smithsonian Short-Term Fellowship.

Data accessibility

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.07nd0hc

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Authors and Affiliations

Authors

Contributions

A.M.T., K.W. and L.O.H. designed the research. A.M.T. and K.W. performed the experiment. A.M.T. analyzed the data. A.M.T. and L.O.H. drafted the paper with all authors contributed to the writing of the manuscript.

Corresponding author

Correspondence to Annette M. Trierweiler.

Additional information

Responsible Editor: Euan K. James.

Electronic supplementary material

Supplemental Fig. 1

Nutrient response ratios of two nitrogen fixing species, Ormosia macrocalyx and Inga marginata. Biomass ratio of nutrient treatments to baseline versus fixation ratios of nutrient treatments compared to the baseline. The baseline is the nutrient treatment without addition P or Mo where each point is the ratio of the means for each given CO2 level with the error bars representing 1 s.e.m. Ormosia is represented by circles as the Inga is represented by triangles. The direction of the colored arrows represents increasing CO2 for Inga.. The reference lines at x=1 (vertical) and y=1 represents (horizontal) the baseline performance of the control forest soil treatment for both species. Points, which fall along this line, mean that plants with the added nutrient performed as well as those without that nutrient. For points to fall left of the x=1 reference line (biomass growth) or above the y=1 line (for nitrogen fixation), the nutrient treatment enhanced growth or fixation by that ratio more than the control growth or fixation. (PDF 120 kb)

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Trierweiler, A.M., Winter, K. & Hedin, L.O. Rising CO2 accelerates phosphorus and molybdenum limitation of N2-fixation in young tropical trees. Plant Soil 429, 363–373 (2018). https://doi.org/10.1007/s11104-018-3685-7

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