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Nutrient feedbacks to soil heterotrophic nitrogen fixation in forests

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Abstract

Multiple nutrient cycles regulate biological nitrogen (N) fixation in forests, yet long-term feedbacks between N-fixation and coupled element cycles remain largely unexplored. We examined soil nutrients and heterotrophic N-fixation across a gradient of 24 temperate conifer forests shaped by legacies of symbiotic N-fixing trees. We observed positive relationships among mineral soil pools of N, carbon (C), organic molybdenum (Mo), and organic phosphorus (P) across sites, evidence that legacies of symbiotic N-fixing trees can increase the abundance of multiple elements important to heterotrophic N-fixation. Soil N accumulation lowered rates of heterotrophic N-fixation in organic horizons due to both N inhibition of nitrogenase enzymes and declines in soil organic matter quality. Experimental fertilization of organic horizon soil revealed widespread Mo limitation of heterotrophic N-fixation, especially at sites where soil Mo was scarce relative to C. Fertilization also revealed widespread absence of P limitation, consistent with high soil P:Mo ratios. Responses of heterotrophic N-fixation to added Mo (positive) and N (negative) were correlated across sites, evidence that multiple nutrient controls of heterotrophic N-fixation were more common than single-nutrient effects. We propose a conceptual model where symbiotic N-fixation promotes coupled N, C, P, and Mo accumulation in soil, leading to positive feedback that relaxes nutrient limitation of overall N-fixation, though heterotrophic N-fixation is primarily suppressed by strong negative feedback from long-term soil N accumulation.

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References

  • Barron AR, Wurzburger N, Bellenger JP, Wright SJ, Kraepiel AML, Hedin LO (2009) Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat Geosci 2:42–45

    Article  Google Scholar 

  • Becking JH (1961a) Molybdenum and symbiotic nitrogen fixation by alder (Alnus glutinosa Gaertn.). Nature 192:1204–1205

    Article  Google Scholar 

  • Becking JH (1961b) A requirement of molybdenum for the symbiotic nitrogen fixation in alder (Alnus glutinosa Gaertn.). Plant Soil 15:217–227

    Article  Google Scholar 

  • Bélanger PA, Bellenger JP, Roy S (2013) Strong modulation of nutrient distribution in Alnus glutinosa as a function of the actinorhizal symbiosis. Botany 91:218–224

    Article  Google Scholar 

  • Bellenger JP, Wichard T, Kustka AB, Kraepiel AML (2008) Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores. Nat Geosci 1:243–246

    Article  Google Scholar 

  • Bellenger JP, Wichard T, Xu Y, Kraepiel AML (2011) Essential metals for nitrogen fixation in a free-living N2-fixing bacterium: chelation, homeostasis and high use efficiency. Environ Microbiol 13:1395–1411

    Article  Google Scholar 

  • Bellenger JP, Xu Y, Zhang X, Morel FM, Kraepiel AML (2014) Possible contribution of alternative nitrogenases to nitrogen fixation by asymbiotic N2 fixing bacteria in soils. Soil Biol Biochem 69:413–420

    Article  Google Scholar 

  • Binkley D (2005) How nitrogen-fixing trees change soil carbon. In: Binkley D, Menyailo O (eds) Tree species effects on soils: implications for global change. NATO Science Series, Springer, Dordrecht

    Chapter  Google Scholar 

  • Binkley D, Sollins P, Bell R, Sachs D, Myrold D (1992) Biogeochemistry of adjacent conifer and alder-conifer stands. Ecology 73:2022–2033

    Article  Google Scholar 

  • Binkley D, Cromack K Jr, Baker DD (1994) Nitrogen fixation by red alder: biology, rates, and controls. In: Hibbs DE, DeBell DS, Tarrant RF (eds) The biology and management of Red Alder. Oregon State University Press, Corvallis, pp 57–72

    Google Scholar 

  • Brodrick SJ, Giller KE (1991) Root nodules of Phaseolus: efficient scavengers of molybdenum for N2-fixation. J Exp Bot 42:679–686

    Article  Google Scholar 

  • Brown KR (2002) Effects of phosphorus additions on growth, mineral nutrition, and gas exchange of red alder seedlings grown in outdoor sandbeds. West J Appl For 17:209–215

    Google Scholar 

  • Bürgmann H, Meier S, Bunge M, Widmer F, Zeyer J (2005) Effects of model root exudates on structure and activity of a soil diazotroph community. Environ Microbiol 7:1711–1724

    Article  Google Scholar 

  • Compton JE, Cole DW (2001) Fate and effects of phosphorus additions in soils under N2-fixing red alder. Biogeochemistry 53:225–247

    Article  Google Scholar 

  • Crews TE, Farrington H, Vitousek PM (2000) Changes in asymbiotic, heterotrophic nitrogen fixation on leaf litter of Metrosideros polymorpha with long-term ecosystem development in Hawaii. Ecosystems 3:386–395

    Article  Google Scholar 

  • Darnajoux R, Zhang X, McRose DL, Miadlikowska J, Lutzoni F, Kraepiel AM, Bellenger JP (2017) Biological nitrogen fixation by alternative nitrogenases in boreal cyanolichens: importance of molybdenum availability and implications for current biological nitrogen fixation estimates. New Phytol 213:680–689

    Article  Google Scholar 

  • Duval BD, Natali SA, Hungate BA (2014) What constitutes plant available molybdenum in acidic soils? Commun Soil Sci Plant Anal 46:318–326

    Article  Google Scholar 

  • Eady RR (1996) Structure-function relationships of alternative nitrogenases. Chem Rev 96:3013–3030

    Article  Google Scholar 

  • Einsle O, Tezcan FA, Andrade S, Schmid B, Yoshida M, Howard J, Rees D (2002) Nitrogenase MoFe-protein at 1.16 angstrom resolution: a central ligand in the FeMo-cofactor. Science 297:1696–1700

    Article  Google Scholar 

  • Eisele KA, Schimel D, Kapustka LA, Parton W (1989) Effects of available P and N:P ratios on non-symbiotic dinitrogen fixation in tallgrass prairie soils. Oecologia 79:471–474

    Article  Google Scholar 

  • Fogel R, Cromack K Jr (1977) Effect of habitat and substrate quality on Douglas-fir litter decomposition in western Oregon. Can J Bot 55:1632–1640

    Article  Google Scholar 

  • Glass JB, Axler RP, Chandra S, Goldman CR (2012) Molybdenum limitation of microbial nitrogen assimilation in aquatic ecosystems and pure cultures. Front Microbiol 3:33

    Google Scholar 

  • Gupta UC (1997) Molybdenum in agriculture. Cambridge University Press, Cambridge

    Book  Google Scholar 

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

    Article  Google Scholar 

  • Hart SK, Hibbs DE, Perakis SS (2013) Riparian litter inputs to streams in the central Oregon Coast Range. Freshw Sci 32:343–358

    Article  Google Scholar 

  • Heath B, Sollins P, Perry DA, Cromack K Jr (1988) Asymbiotic nitrogen fixation in litter from Pacific Northwest forests. Can J For Res 18:68–74

    Article  Google Scholar 

  • Hernandez JA, George SJ, Rubio LM (2009) Molybdenum trafficking for nitrogen fixation. Biochemistry 48:9711–9721

    Article  Google Scholar 

  • Horstmann JL, Denison WC, Silvester WB (1982) 15N2 fixation and molybdenum enhancement of acetylene reduction by Lobaria spp. New Phytol 92:235–241

    Article  Google Scholar 

  • Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–331

    Article  Google Scholar 

  • Hynicka JD, Pett-Ridge JC, Perakis SS (2016) Nitrogen enrichment regulates calcium sources in forests. Glob Chang Biol 22:4067–4079

    Article  Google Scholar 

  • Jean ME, Phayvong K, Forest-Drolet J, Bellenger JP (2013) Molybdenum and phosphorus limitation of asymbiotic nitrogen fixation in forests of Eastern Canada: influence of vegetative cover and seasonal variability. Soil Biol Biochem 67:140–146

    Article  Google Scholar 

  • King EK, Thompson A, Chadwick OA, Pett-Ridge JC (2016) Molybdenum sources and isotopic composition during early stages of pedogenesis along a basaltic climate transect. Chem Geol 445:54–67

    Article  Google Scholar 

  • Levy-Booth DJ, Winder RS (2010) Quantification of nitrogen reductase and nitrite reductase genes in soil of thinned and clear-cut Douglas-fir stands by using real-time PCR. Appl Environ Microbiol 76:7116–7125

    Article  Google Scholar 

  • Mainwaring DB, Maguire DA, Perakis SS (2014) Three-year growth response of young Douglas-fir to nitrogen, calcium, phosphorus, and blended fertilizers in Oregon and Washington. For Ecol Manag 327:178–188

    Article  Google Scholar 

  • Marks JA, Perakis SS, King EA, Pett-Ridge JC (2015a) Soil organic matter regulates molybdenum storage and mobility in forests. Biogeochemistry 125:167–183

    Article  Google Scholar 

  • Marks JA, Pett-Ridge JC, Perakis SS, Allen JJ, McCune B (2015b) Response of the nitrogen-fixing lichen Lobaria pulmonaria to phosphorus, molybdenum, and vanadium. Ecosphere 6(9):1–17

    Article  Google Scholar 

  • Menge DN, Levin SA, Hedin LO (2009) Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am Nat 174:465–477

    Article  Google Scholar 

  • Menge DNL, Wolf AA, Funk JL (2015) Diversity of nitrogen fixation strategies in Mediterranean legumes. Nat Plants. doi:10.1038/nplants.2015.64

    Google Scholar 

  • Perakis SS, Sinkhorn ER (2011) Biogeochemistry of a temperate forest nitrogen gradient. Ecology 92:1481–1491

    Article  Google Scholar 

  • Perakis SS, Maguire DA, Bullen TD, Cromack K, Waring RH, Boyle JR (2006) Coupled nitrogen and calcium cycles in forests of the Oregon Coast Range. Ecosystems 9:63–74

    Article  Google Scholar 

  • Perakis SS, Sinkhorn ER, Compton JE (2011) δ15N constraints on long-term nitrogen balances in temperate forests. Oecologia 167:793–807

    Article  Google Scholar 

  • Perakis SS, Matkins JJ, Hibbs DE (2012) Interactions of tissue and fertilizer nitrogen on decomposition dynamics of lignin-rich conifer litter. Ecosphere 3(6):54

    Article  Google Scholar 

  • Perakis SS, Sinkhorn ER, Catricala CE, Bullen TD, Fitzpatrick J, Hynicka JD, Cromack K (2013) Forest calcium depletion and biotic retention along a soil nitrogen gradient. Ecol Appl 23:1947–1961

    Article  Google Scholar 

  • Pérez SE, Pérez CA, Carmona MR, Farina JM, Armesto JJ (2008) Efectos del fo´sforo y carbono labiles en la fijacionno simbiotica del N2 de bosques siempreverdes manejados y no manejados de la Isla de Chiloe´, Chile. Rev Chil Hist Nat 81:267–278

    Article  Google Scholar 

  • Pérez CA, Thomas FM, Silva WA, Aguilera R, Armesto JJ (2017) Biological nitrogen fixation in a post-volcanic chronosequence from south-central Chile. Biogeochemistry. doi:10.1007/s10533-016-0285-6

    Google Scholar 

  • Pourhassan N, Bruno S, Jewell MD, Shipley B, Roy S, Bellenger JP (2016) Phosphorus and micronutrient dynamics during gymnosperm and angiosperm litters decomposition in temperate cold forest from Eastern Canada. Geoderma 273:25–31

    Article  Google Scholar 

  • Reddy KJ, Munn LC, Wang L (1997) Chemistry and mineralogy of molybdenum in soils. In: Gupta UC (ed) Molybdenum in agriculture. Cambridge University Press, Cambridge

    Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512

    Article  Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2013) Relationships of phosphorus, molybdenum and free-living nitrogen fixation in tropical rain forests. Biogeochemistry 114:135–147

    Article  Google Scholar 

  • Romero IC, Klein NJ, Sanudo-Wilhelmy SA, Capone DG (2013) Potential trace metal co-limitation controls on N2 fixation and NO3 − uptake in lakes with varying trophic status. Front Microbiol 4:54

    Article  Google Scholar 

  • Rousk K, Degboe J, Michelsen A, Bradley R, Bellenger JP (2017) Molybdenum and phosphorus limitation of moss-associated nitrogen fixation in boreal ecosystems. New Phytol 214:97–107

    Article  Google Scholar 

  • Silvester WB (1989) Molybdenum limitation of asymbiotic nitrogen-fixation in forests of Pacific Northwest America. Soil Biol Biochem 21:283–289

    Article  Google Scholar 

  • Sitters J, Edwards PJ, Venterink HO (2013) Increases of soil C, N, and P pools along an Acacia tree density gradient and their effects on trees and grasses. Ecosystems 16:347–357

    Article  Google Scholar 

  • Swanston CW, Homann PS, Caldwell BA, Myrold DD, Ganio L, Sollins P (2004) Long-term effects of elevated nitrogen on soil organic matter stability. Biogeochemistry 70:227–250

    Article  Google Scholar 

  • Valachovic YS, Caldwell BA, Cromack K Jr, Griffiths RP (2004) Leaf litter chemistry controls on decomposition of Pacific Northwest trees and woody shrubs. Can J For Res 34:2131–2147

    Article  Google Scholar 

  • van Groenigen KJ, Six J, Hungate BA, de Graaff MA, Van Breemen N, Van Kessel C (2006) Element interactions limit soil carbon storage. PNAS 103:6571–6574

    Article  Google Scholar 

  • van Huysen TL, Perakis SS, Harmon ME (2016) Decomposition drives convergence of forest litter nutrient stoichiometry following phosphorus addition. Plant Soil 1:1–14

    Article  Google Scholar 

  • Van Soest PJ, Wine RH (1967) Use of detergents in the analysis of fibrous feeds. IV. Determination of plant cell-wall constituents. J Assoc Off Anal Chem 50:50–55

    Google Scholar 

  • Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45

    Article  Google Scholar 

  • Wang YP, Houlton BZ (2009) Nitrogen constraints on terrestrial carbon uptake: implications for the global carbon-climate feedback. Geophys Res Lett 36:L24403

    Article  Google Scholar 

  • Wichard T, Mishra B, Myneni SCB, Bellenger JP, Kraepiel AML (2009) Storage and bioavailability of molybdenum in soils increased by organic matter complexation. Nat Geosci 2:625–629

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Xu N, Christodoulatos C, Braida W (2006) Adsorption of molybdate and tetrathiomolybdate onto pyrite and goethite: effect of pH and competitive anions. Chemosphere 62:1726–1735

    Article  Google Scholar 

  • Yelenik SG, Perakis SS, Hibbs DE (2013) Regional constraints to N-fixation in post-fire forest communities. Ecology 94:739–750

    Article  Google Scholar 

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Acknowledgements

We thank Clarinda Wilson, Jade Marks, Justin Hynicka, April Strid, Kecia Jones, and Lauren Armony for field and laboratory assistance, SNCC cooperators for access to field sites, and Liz King, Annette Trierweiler, and two anonymous reviewers for manuscript comments. We acknowledge National Science Foundation support through grants DEB-1457650 to S. Perakis and EAR-1053470 to J. Pett-Ridge. Any use of trade names does not imply endorsement by the US Government.

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  1. US Geological Survey, Forest and Rangeland Ecosystem Science Center, Corvallis, OR, 97331, USA

    Steven S. Perakis & Christina E. Catricala

  2. Department of Crop and Soil Science, Oregon State University, Corvallis, OR, 97331, USA

    Julie C. Pett-Ridge

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  1. Steven S. Perakis
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Correspondence to Steven S. Perakis.

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Perakis, S.S., Pett-Ridge, J.C. & Catricala, C.E. Nutrient feedbacks to soil heterotrophic nitrogen fixation in forests. Biogeochemistry 134, 41–55 (2017). https://doi.org/10.1007/s10533-017-0341-x

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