Oecologia

, Volume 185, Issue 3, pp 513–524 | Cite as

Nutrient limitation of soil microbial activity during the earliest stages of ecosystem development

  • Sarah C. Castle
  • Benjamin W. Sullivan
  • Joseph Knelman
  • Eran Hood
  • Diana R. Nemergut
  • Steven K. Schmidt
  • Cory C. Cleveland
Ecosystem ecology – original research

Abstract

A dominant paradigm in ecology is that plants are limited by nitrogen (N) during primary succession. Whether generalizable patterns of nutrient limitation are also applicable to metabolically and phylogenetically diverse soil microbial communities, however, is not well understood. We investigated if measures of N and phosphorus (P) pools inform our understanding of the nutrient(s) most limiting to soil microbial community activities during primary succession. We evaluated soil biogeochemical properties and microbial processes using two complementary methodological approaches—a nutrient addition microcosm experiment and extracellular enzyme assays—to assess microbial nutrient limitation across three actively retreating glacial chronosequences. Microbial respiratory responses in the microcosm experiment provided evidence for N, P and N/P co-limitation at Easton Glacier, Washington, USA, Puca Glacier, Peru, and Mendenhall Glacier, Alaska, USA, respectively, and patterns of nutrient limitation generally reflected site-level differences in soil nutrient availability. The activities of three key extracellular enzymes known to vary with soil N and P availability developed in broadly similar ways among sites, increasing with succession and consistently correlating with changes in soil total N pools. Together, our findings demonstrate that during the earliest stages of soil development, microbial nutrient limitation and activity generally reflect soil nutrient supply, a result that is broadly consistent with biogeochemical theory.

Keywords

Extracellular enzymes Nutrient fertilization Primary succession Soil respiration 

Notes

Acknowledgements

We would like to thank R. Callaway, S. Dobrowski, A. Larson, Y. Lekberg, A. Marklein, M. Nasto, and three anonymous reviewers for comments on early drafts of this manuscript. Authors declare no conflict of interest. This work was supported by a National Science Foundation Grant (NSF DEB-0922306) made to CC, EH, DN, and SS.

Author contribution statement

SCC and CCC conceived and designed the experiments. SCC performed the experiments and analyzed the data. SCC, BWS, JK, and CCC wrote the manuscript; other authors provided editorial advice and all authors approved of the final version of the manuscript.

Supplementary material

442_2017_3965_MOESM1_ESM.docx (320 kb)
Supplementary material 1 (DOCX 319 kb)

References

  1. Alexander EB, Burt R (1996) Soil development on moraines of Mendenhall Glacier, southeast Alaska. 1. The moraines and soil morphology. Geoderma 72:1–17CrossRefGoogle Scholar
  2. Allison SD (2006) Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochemistry 81:361–373CrossRefGoogle Scholar
  3. Allison VJ, Condron LM, Peltzer DA, Richardson SJ, Turner BL (2007) Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand. Soil Biol Biochem 39:1770–1781CrossRefGoogle Scholar
  4. Anesio AM, Hodson AJ, Fritz A, Psenner R, Sattler B (2008) High microbial activity on glaciers: importance to the global carbon cycle. Glob Change Biol 15:955–960CrossRefGoogle Scholar
  5. Bardgett RD, Richter A, Bol R, Garnett MH, Bäumler R, Xu X, Lopez-Capel E, Manning DA, Hobbs PJ, Hartley IR, Wanek W (2007) Heterotrophic microbial communities use ancient carbon following glacial retreat. Biol Lett 3:487–490CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bååth E (2001) Estimation of fungal growth rates in soil using 14C-acetate incorporation into ergosterol. Soil Biol Biochem 33:2011–2018CrossRefGoogle Scholar
  7. Bradford MA, Fierer N, Reynolds JF (2008) Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils. Funct Ecol 22:964–974CrossRefGoogle Scholar
  8. Brankatschk R, Toewe S, Kleineidam K, Schloter M, Zeyer J (2011) Abundances and potential activities of nitrogen cycling microbial communities along a chronosequence of a glacier forefield. ISME J 5:1025–1037CrossRefPubMedGoogle Scholar
  9. Castle SC, Neff JC (2009) Plant response to nutrient availability across bedrock geologies. Ecosystems 12:101–113CrossRefGoogle Scholar
  10. Castle SC, Lekberg Y, Affleck D, Cleveland CC (2016a) Soil abiotic and biotic controls on plant performance during primary succession in a glacial landscape. J Ecol 104:1555–1565CrossRefGoogle Scholar
  11. Castle SC, Nemergut DR, Grandy AS, Leff JW, Graham EB, Hood E, Schmidt SK, Wickings K, Cleveland CC (2016b) Biogeochemical drivers of microbial community convergence across actively retreating glaciers. Soil Biol Biochem 101:74–84CrossRefGoogle Scholar
  12. Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175CrossRefGoogle Scholar
  13. Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Nat Acad Sci 103:10316–10321CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cleveland C, Liptzin D (2007) C:N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252CrossRefGoogle Scholar
  15. Cleveland CC, Reed SC, Townsend AR (2006) Nutrient regulation of organic matter decomposition in a tropical rain forest. Ecology 87:492–503CrossRefPubMedGoogle Scholar
  16. Cline LC, Zak DR (2015) Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology 96:3374–3385CrossRefPubMedGoogle Scholar
  17. Craine JM, Morrow C, Fierer M (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113CrossRefPubMedGoogle Scholar
  18. Crews TE, Kitayama K, Fownes JH, Riley RH, Herbert DA, Mueller-Dombois D, Vitousek PM (1995) Changes in soil-phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. J Ecol 76:1407–1424CrossRefGoogle Scholar
  19. Darcy JL, Schmidt SK (2016) Nutrient limitation of microbial phototrophs on a debris-covered glacier. Soil Biol Biochem 95:156–163CrossRefGoogle Scholar
  20. Dick WA, Tabatabai MA (1987) Kinetics and activities of phosphatase-clay complexes. Soil Sci 143:5–15CrossRefGoogle Scholar
  21. Doane T, Horwath W (2003) Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36:2713–2722CrossRefGoogle Scholar
  22. Duc L, Noll M, Meier BE, Burgmann H, Zeyer J (2009) High diversity of diazotrophs in the forefield of a receding alpine glacier. Microb Ecol 57:179–190CrossRefPubMedGoogle Scholar
  23. Elser JJ, Bracken ME, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142CrossRefPubMedGoogle Scholar
  24. Eviner VT, Chapin FS III, Vaughn CE (2000) Nutrient manipulations in terrestrial ecosystems. In: Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods in ecosystem science. Springer, New York, pp 291–307CrossRefGoogle Scholar
  25. Fernández-Martínez MA, Pérez-Ortega S, Pointing SB, Green TA, Pintado A, Rozzi R, Sancho LG, de los Ríos A (2017) Microbial succession dynamics along glacier forefield chronosequences in Tierra del Fuego (Chile). Polar Biol 40:1939–1957CrossRefGoogle Scholar
  26. Fierer N, Nemergut DR, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161:635–642CrossRefPubMedGoogle Scholar
  27. Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual 29:15–23CrossRefGoogle Scholar
  28. Gallo ME, Amonette R, Lauber C, Sinsabaugh RL, Zak DR (2004) Microbial community structure and oxidative enzyme activity in Nitrogen-amended north temperate forest soils. Microb Ecol 48:218–229CrossRefPubMedGoogle Scholar
  29. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397CrossRefGoogle Scholar
  30. Göransson H, Venterink HO, Bååth E (2011) Soil bacterial growth and nutrient limitation along a chronosequence from a glacier forefield. Soil Biol Biochem 43:1333–1340CrossRefGoogle Scholar
  31. Halvorson JJ, Franz EH, Smith JL, Black RA (1992) Nitrogenase activity, nitrogen fixation, and nitrogen inputs by lupines at Mount St Helens. Ecology 73:87–98CrossRefGoogle Scholar
  32. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken ME, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862CrossRefPubMedGoogle Scholar
  33. Hobbie SE, Vitousek PM (2000) Nutrient limitation of decomposition in Hawaiian forests. Ecology 81:1867–1877CrossRefGoogle Scholar
  34. Horwath W, Paul E (1994) Microbial biomass. In: Weaver RW, Angle JS, Bottomley PS (eds) Methods of soil analysis, part 2: microbiological and biochemical properties. Soil Science Society of America, Fitchburg, pp 754–760Google Scholar
  35. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefPubMedGoogle Scholar
  36. Jeannotte R, Sommerville DW, Hamel C, Whalen JK (2004) A microplate assay to measure soil microbial biomass phosphorus. Biol Fertil Soils 40:201–205CrossRefGoogle Scholar
  37. King AJ, Meyer AF, Schmidt SK (2008) High levels of microbial biomass and activity in unvegetated tropical and temperate alpine soils. Soil Biol Biochem 40:2605–2610CrossRefGoogle Scholar
  38. Knelman JE, Legg TM, O’Neill SP, Washenberger CL, González A, Cleveland CC, Nemergut DR (2012) Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield. Soil Biol Biogeochem 46:172–180CrossRefGoogle Scholar
  39. Knelman JE, Schmidt SK, Lynch RC, Darcy JL, Castle SC, Cleveland CC, Nemergut DR (2014) Nutrient addition dramatically accelerates microbial community succession. PloS One 9: e102609. doi:10.1371/journal.pone.0102609 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Laliberté E, Turner BL, Costes T, Pearse SJ, Wyrwoll K-H, Zemunik G, Lambers H (2012) Experimental assessment of nutrient limitation along a 2-million year dune chronosequence in the south-western Australia biodiversity hotspot. J Ecol 100:631–642CrossRefGoogle Scholar
  41. Lebauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379CrossRefPubMedGoogle Scholar
  42. Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JM, McCulley RL (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci 112(35):10967–10972CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ley R, Williams M, Schmidt S (2004) Microbial population dynamics in an extreme environment: controlling factors in talus soils at 3750 m in the Colorado Rocky Mountains. Biogeochemistry 68:313–335CrossRefGoogle Scholar
  44. Matthews JA (1992) The ecology of recently-deglaciated terrain: a geoecological approach to glacier forelands and primary succession. Cambridge University Press, CambridgeGoogle Scholar
  45. McGill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–286CrossRefGoogle Scholar
  46. Menge DNL, Hedin LO (2009) Nitrogen fixation in different biogeochemical niches along a 120,000-year chronosequence in New Zealand. Ecology 90:2190–2201CrossRefPubMedGoogle Scholar
  47. Mulvaney RL (1994) Nitrogen—inorganic forms. In: Sparks DL (ed) Methods of soil analysis, part 3: chemical methods. Soil Science Society of America, Fitchburg, pp 1129–1131Google Scholar
  48. Nemergut, DR (2004) Evolution and ecology of high altitude soil microbial communities. Ph.D. dissertation, University of Colorado, Boulder, COGoogle Scholar
  49. Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated recently deglaciated soil. Microb Ecol 53:110–122CrossRefPubMedGoogle Scholar
  50. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models, 4th edn. Irwin McGraw-Hill, ChicagoGoogle Scholar
  51. Ohtonen R, Fritze H, Pennanen T, Jumpponen A, Trappe J (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119:239–246CrossRefPubMedGoogle Scholar
  52. Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–191CrossRefGoogle Scholar
  53. Parfitt RL, Ross DJ, Coomes DA, Richardson SJ, Smale MC, Dahlgren RA (2005) N and P in New Zealand soil chronosequences and relationships with foliar N and P. Biogeochemistry 75:305–328CrossRefGoogle Scholar
  54. Peltzer D, Wardle D, Allison V, Baisden W (2010) Understanding ecosystem retrogression. Ecol Monogr 80:509–529CrossRefGoogle Scholar
  55. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  56. Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Change Biol 18:1918–1927CrossRefGoogle Scholar
  57. Reed SC, Vitousek PM, Cleveland CC (2011) Are patterns in nutrient limitation belowground consistent with those aboveground: results from a 4 million year chronosequence. Biogeochemistry 106:323–336CrossRefGoogle Scholar
  58. Reynolds H, Packer A, Bever J, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291CrossRefGoogle Scholar
  59. Richardson SJ, Peltzer DA, Allen RB, McGlone MS, Parfitt RL (2004) Rapid development of phosphorus limitation in termperate rainforest along the Franz Josef chronosequence. Oecologia 139:267–276CrossRefPubMedGoogle Scholar
  60. Saiya-Cork K, Sinsabaugh R, Zak D (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  61. Sattin S, Cleveland C, Hood E, Reed S (2009) Functional shifts in unvegetated, perhumid, recently-deglaciated soils do not correlate with shifts in soil bacterial community composition. J Microbiol 47:673–681CrossRefPubMedGoogle Scholar
  62. Schimel JP, Schaffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3:1–11CrossRefGoogle Scholar
  63. Schmidt SK, Reed SC, Nemergut DR, Grandy AS, Cleveland CC, Weintraub MN, Hill AW, Costello EK, Meyer AF, Neff JC, Martin AM (2008) The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc R Soc B Biol Sci 275:2793–2802CrossRefGoogle Scholar
  64. Schmidt SK, Nemergut DR, Sowell P, Reed SC, Cleveland CC (2011) Estimating phosphorus availability for microbial growth in an emerging landscape. Geoderma 163:135–140CrossRefGoogle Scholar
  65. Schmidt SK, Nemergut DR, Todd BT, Lynch RC, Darcy JL, Cleveland CC, King AJ (2012) A simple method for determining limiting nutrients for photosynthetic crusts. Plant Ecol Divers. doi:10.1080/175508742012738714 Google Scholar
  66. Selmants P, Hart S (2010) Phosphorus and soil development: does the Walker and Syers model apply to semiarid ecosystems? Ecology 91:474–484CrossRefPubMedGoogle Scholar
  67. Sigler WV, Zeyer J (2004) Colony-forming analysis of bacterial community succession in deglaciated soils indicates pioneer stress-tolerant opportunists. Microb Ecol 48:316–323CrossRefPubMedGoogle Scholar
  68. Sinsabaugh RL (1994) Enzymic analysis of microbial patterns and process. Biol Fertil Soils 17:69–74CrossRefGoogle Scholar
  69. Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343CrossRefGoogle Scholar
  70. Sinsabaugh RL, Antibus RK, Linkins AE, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74:1586–1593CrossRefGoogle Scholar
  71. Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24CrossRefGoogle Scholar
  72. Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264PubMedGoogle Scholar
  73. Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798CrossRefPubMedGoogle Scholar
  74. Stursova M, Crenshaw CL, Sinsabaugh RL (2006) Microbial responses to long-term N deposition in a semiarid grassland. Microb Ecol 51:90–98CrossRefPubMedGoogle Scholar
  75. Sullivan BW, Alvarez-Clare S, Castle SC, Porder S, Reed SC, Schreeg L, Townsend AR, Cleveland CC (2014) Assessing nutrient limitation in complex forested ecosystems: alternatives to large-scale fertilization experiments. Ecology 95:668–681CrossRefPubMedGoogle Scholar
  76. Tabor RW, Haugerud RA, Hildreth W, Brown EH (2003) Geologic map of the Mount Baker 30 × 60 minute quadrangle. Washington US Geological Survey Map I-2660, scale 1:100,000Google Scholar
  77. Tscherko D, Rustemeier J, Richter A, Wanek W, Kanedler E (2003) Functional diversity of the soil microflora in primary succession across two glacier forelands in the Central Alps. Eur J Soil Sci 54:685–696CrossRefGoogle Scholar
  78. Turner BL, Laliberté E (2014) Soil development and nutrient availability along a 2 million-year coastal dune chronosequence under species-rich mediterranean shrubland in southwestern Australia. Ecosystems 100:631–642Google Scholar
  79. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  80. Vitousek PM (2004) Nutrient cycling and limitation: Hawai’i as a model system. Princeton University Press, PrincetonGoogle Scholar
  81. Vitousek P, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75CrossRefGoogle Scholar
  82. Vitousek PM, Walker LR, Whiteaker LD, Matson PA (1993) Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23:197–215CrossRefGoogle Scholar
  83. Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846CrossRefGoogle Scholar
  84. Walker L, del Moral R (2003) Primary succession and ecosystem rehabilitation. Cambridge University Press, New YorkCrossRefGoogle Scholar
  85. Walker T, Syers J (1976) Fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  86. Wardle D, Bardgett R, Klironomos J, Setälä H, van der Putten W, Wall D (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633CrossRefPubMedGoogle Scholar
  87. Weatherburn MW (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39:971–974CrossRefGoogle Scholar
  88. Weintraub M, Scott-Denton L, Schmidt S, Monson R (2007) The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a subalpine forest ecosystem. Oecologia 154:327–338CrossRefPubMedGoogle Scholar
  89. Yoshitake S, Uchida M, Koizumi H, Nakatsubo T (2007) Carbon and nitrogen limitation of soil microbial respiration in a High Arctic successional glacier foreland near Ny-Ålesund, Svalbard. Polar Res 26:22–30CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Sarah C. Castle
    • 1
    • 7
  • Benjamin W. Sullivan
    • 2
  • Joseph Knelman
    • 3
  • Eran Hood
    • 4
  • Diana R. Nemergut
    • 5
  • Steven K. Schmidt
    • 6
  • Cory C. Cleveland
    • 1
  1. 1.Department of Ecosystem and Conservation SciencesUniversity of MontanaMissoulaUSA
  2. 2.Department of Natural Resources and Environmental ScienceUniversity of NevadaRenoUSA
  3. 3.Institute of Arctic and Alpine Research and Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  4. 4.Environmental Science ProgramUniversity of Alaska SoutheastJuneauUSA
  5. 5.Department of BiologyDuke UniversityDurhamUSA
  6. 6.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  7. 7.Department of Plant PathologyUniversity of MinnesotaSaint PaulUSA

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