Nitrogen deposition decreases the benefits of symbiosis in a native legume
- 480 Downloads
Anthropogenic nitrogen deposition can provide legumes with a cheap source of nitrogen relative to symbiotic nitrogen fixation, leading to the potential breakdown of this critical symbiosis. Here, the effects of nitrogen deposition were tested on a native symbiosis between legumes and rhizobia.
Deposition rates, soil nitrogen concentration, and plant nitrogen isotopic composition were quantified along a predicted deposition gradient in California. Acmispon strigosus seedlings were exposed to fertilization spanning nitrogen concentrations observed in the plant’s California range. Both wild and experimental plants from pristine and nitrogen polluted sites were tested using rhizobial strains that varied in nitrogen fixation.
Deposition intensity was tightly correlated with nitrogen concentration in soils. The growth benefits of rhizobial nodulation were dramatically reduced by even modest levels of mineral nitrogen, and all Acmispon lines failed to form root nodules at high nitrogen concentrations.
Our dataset suggests that anthropogenic deposition has greatly increased soil nitrogen concentrations in Southern California leading to significantly reduced benefits of rhizobial symbiosis. If nitrogen deposition increases continue, plant host mortality and a total collapse of the symbiosis could result.
KeywordsAnthropogenic nitrogen deposition Biological nitrogen fixation Legume rhizobium symbiosis Mutualism breakdown
We acknowledge the U.C. Natural Reserve System and Bodega Marine Reserve in particular. This research was supported by NSF DEB-1150278 to JLS and Mildred E. Mathias Graduate Student Research Award to JUR.
- Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20(1):30–59CrossRefPubMedGoogle Scholar
- Bremner J (1965) Organic Nitrogen in Soils. In: Bartholomew WV, Clark FE (eds) Soil Nitrogen. American Society of Agronomy Inc., Madison, pp. 93–132Google Scholar
- Carroll JA, Caporn SJM, Johnson D, Morecroft MD, Lee JA (2003) The interactions between plant growth, vegetation structure and soil processes in semi-natural acidic and calcareous grasslands receiving long-term inputs of simulated pollutant nitrogen deposition. Environ Pollut 121(3):363–376CrossRefPubMedGoogle Scholar
- Dentener F, Drevet J, Lamarque JF, Bey I, Eickhout B, Fiore AM, Hauglustaine D, Horowitz LW, Krol M, Kulshrestha UC, Lawrence M, Galy-Lacaux C, Rast S, Shindell D, Stevenson D, Van Noije T, Atherton C, Bell N, Bergman D, Butler T, Cofala J, Collins B, Doherty R, Ellingsen K, Galloway J, Gauss M, Montanaro V, Mueller JF, Pitari G, Rodriguez J, Sanderson M, Solmon F, Strahan S, Schultz M, Sudo K, Szopa S, Wild O (2006) Nitrogen and sulfur deposition on regional and global scales: a multimodel evaluation. Glob Biogeochem Cycles 20(4):GB4003CrossRefGoogle Scholar
- EPA (2012) CASTNET 2010 annual report, clean air status and trends network. EPA Contract No. EP-W-09-028Google Scholar
- Galloway JN, Leach AM, Bleeker A, Erisman JW (2013) A chronology of human understanding of the nitrogen cycle. Philos Trans R Soc B Biol Sci 368(1621)Google Scholar
- Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13(3):394–407CrossRefPubMedGoogle Scholar
- Holtgrieve GW, Schindler DE, Hobbs WO, Leavitt PR, Ward EJ, Bunting L, Chen G, Finney BP, Gregory-Eaves I, Holmgren S, Lisac MJ, Lisi PJ, Nydick K, Rogers LA, Saros JE, Selbie DT, Shapley MD, Walsh PB, Wolfe AP (2011) A coherent signature of anthropogenic nitrogen deposition to remote watersheds of the northern hemisphere. Science 334(6062):1545–1548CrossRefPubMedGoogle Scholar
- Regus JU, Gano KA, Hollowell AC, Sachs JL (2014) Efficiency of partner choice and sanctions in Lotus is not altered by nitrogen fertilization. Proc R Soc B Biol Sci 281(1781):20132587Google Scholar
- Regus JU, Gano KA, Hollowell AC, Sofish V, Sachs JL (2015) Lotus hosts delimit the mutualism-parasitism continuum of Bradyrhizobium. J Evol Biol 28(2):447–456Google Scholar
- Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman D (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7(3):737–750Google Scholar