Plant and Soil

, Volume 338, Issue 1–2, pp 483–495

Effects of plant species richness and evenness on soil microbial community diversity and function

  • Eric G. Lamb
  • Nabla Kennedy
  • Steven D. Siciliano
Regular Article

Abstract

Understanding the links between plant diversity and soil communities is critical to disentangling the mechanisms by which plant communities modulate ecosystem function. Experimental plant communities varying in species richness, evenness, and density were established using a response surface design and soil community properties including bacterial and archaeal abundance, richness, and evenness were measured. The potential to perform a representative soil ecosystem function, oxidation of ammonium to nitrite, was measured via archaeal and bacterial amoA genes. Structural equation modeling was used to explore the direct and indirect effects of the plant community on soil diversity and potential function. Plant communities influenced archaea and bacteria via different pathways. Species richness and evenness had significant direct effects on soil microbial community structure, but the mechanisms driving these effects did not include either root biomass or the pools of carbon and nitrogen available to the soil microbial community. Species richness had direct positive effects on archaeal amoA prevalence, but only indirect impacts on bacterial communities through modulation of plant evenness. Increased plant evenness increased bacterial abundance which in turn increased bacterial amoA abundance. These results suggest that plant community evenness may have a strong impact on some aspects of soil ecosystem function. We show that a more even plant community increased bacterial abundance, which then increased the potential for bacterial nitrification. A more even plant community also increased total dissolved nitrogen in the soil, which decreased the potential for archaeal nitrification. The role of plant evenness in structuring the soil community suggests mechanisms including complementarity in root exudate profiles or root foraging patterns.

Keywords

Plant–soil interaction Structural equation modeling Community structure Ecosystem function 

Supplementary material

11104_2010_560_MOESM1_ESM.doc (182 kb)
ESM 1Supplementary methods and figures detailing the relationships between mesocosm plant community composition and plant species richness, evenness, density, functional group composition, and harvest plant evenness. Supplementary tables include variable ranges and transformations, detailed structural equation model results, and variance–covariance matrices of the data reported in this paper. (DOC 182 kb)
11104_2010_560_MOESM2_ESM.xls (88 kb)
ESM 2A spreadsheet containing the raw data and accompanying metadata used in this study is also provided. (XLS 87 kb)

References

  1. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67CrossRefGoogle Scholar
  2. Arp DJ, Stein LY (2003) Metabolism of inorganic N compounds by Ammonia-oxidizing bacteria. Crit Rev Biochem Mol Biol 38:471–495CrossRefPubMedGoogle Scholar
  3. Bardgett R (2005) The biology of soil: a community and ecosystem approach. Oxford University Press, OxfordGoogle Scholar
  4. Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ (1999) Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol 13:650–660CrossRefGoogle Scholar
  5. Bartelt-Ryser J, Joshi J, Schmid B, Brandl H, Balser T (2005) Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspect Plant Ecol Evol Syst 7:27–49CrossRefGoogle Scholar
  6. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13CrossRefPubMedGoogle Scholar
  7. Bever JD (2003) Soil Community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473CrossRefGoogle Scholar
  8. Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, Mortimer SR, Van Der Putten WH (2006) Plant species and functional group effects on abiotic and microbial soil properties and plant–soil feedback responses in two grasslands. J Ecol 94:893–904CrossRefGoogle Scholar
  9. Blackwood CB, Hudleston D, Zak DR, Buyer JS (2007) Interpreting ecological diversity indices applied to terminal restriction fragment length polymorphism data: insights from simulated microbial communities. Appl Environ Microbiol 73:5276–5283CrossRefPubMedGoogle Scholar
  10. Cahill JF Jr, McNickle GG, Haag JJ, Lamb EG, Nyanumba SM, St. Clair CC (2010) Plants integrate information about nutrients and neighbors. Science 328:1657CrossRefPubMedGoogle Scholar
  11. Cenciarini-Borde C, Courtois S, La Scola B (2009) Nucleic acids as viability markers for bacteria detection using molecular tools. Future Microbiol 4:45–64CrossRefPubMedGoogle Scholar
  12. Chung H, Zak DR, Reich PB, Ellsworth DS (2007) Plant species richness, elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Glob Chang Biol 13:980–989CrossRefGoogle Scholar
  13. Coolen MJL, Hopmans EC, Rijpstra WIC, Muyzer G, Schouten S, Volkman JK, Sinninghe Damsté JS (2004) Evolution of the methane cycle in Ace Lake (Antarctica) during the Holocene: response of methanogens and methanotrophs to environmental change. Org Geochem 35:1151–1167CrossRefGoogle Scholar
  14. Coupland RT, Brayshaw TC (1953) The fescue grassland in Saskatchewan. Ecology 34:386–405CrossRefGoogle Scholar
  15. de Deyn GB, Quirk H, Bardgett RD (2010) Plant species richness, identity and productivity differentially influence key groups of microbes in grassland soils of contrasting fertility. Biol Lett. doi:10.1098/rsbl.2010.0575
  16. Delgado-Viscogliosi P, Solignac L, Delattre J-M (2009) Viability PCR, a culture-independent method for rapid and selective quantification of viable Legionella pneumophila cells in environmental water samples. Appl Environ Microbiol 75:3502–3512CrossRefPubMedGoogle Scholar
  17. Dell CJ, Rice CW (2005) Short-term competition for ammonium and nitrate in tallgrass prairie. Soil Sci Soc Am J 69:371–377CrossRefGoogle Scholar
  18. Eisenhauer N, Beßler H, Engels C, Gleixner G, Habekost M, Milcu A, Partsch S, Sabais ACW, Scherber C, Steinbeiss S, Weigelt A, Weisser WW, Scheu S (2010) Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91:485–496CrossRefPubMedGoogle Scholar
  19. Fogel GB, Collins CR, Li J, Brunk CF (1999) Prokaryotic genome size and SSU rDNA copy number: estimation of microbial relative abundance from a mixed population. Microb Ecol 38:93–113CrossRefPubMedGoogle Scholar
  20. Fornara DA, Tilman D, Hobbie SE (2009) Linkages between plant functional composition, fine root processes and potential soil N mineralization rates. J Ecol 97:48–56CrossRefGoogle Scholar
  21. Gillman LN, Wright SD (2006) The influence of productivity on the species richness of plants: a critical assessment. Ecology 87:1234–1243CrossRefPubMedGoogle Scholar
  22. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, UKCrossRefGoogle Scholar
  23. Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491CrossRefPubMedGoogle Scholar
  24. Grüter D, Schmid B, Brandl H (2006) Influence of plant diversity and elevated atmospheric carbon dioxide levels on belowground bacterial diversity. BMC Microbiol 6:68CrossRefPubMedGoogle Scholar
  25. He JS, Wolfe-Bellin KS, Schmid B, Bazzaz FA (2005) Density may alter diversity–productivity relationships in experimental plant communities. Basic Appl Ecol 6:505–517CrossRefGoogle Scholar
  26. Hedlund K, Santa Regina I, Van der Putten WH, Lepš J, Diaz T, Korthals GW, Lavorel S, Brown VK, Gormsen D, Mortimer SR, Rodriguez Barrueco C, Roy J, Smilauer P, Smilauerová M, Van Dijk C (2003) Plant species diversity, plant biomass and responses of the soil community on abandoned land across Europe: idiosyncracy or above-belowground time lags. Oikos 103:45–58CrossRefGoogle Scholar
  27. Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520CrossRefPubMedGoogle Scholar
  28. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
  29. Horner-Devine MC, Carney KM, Bohannan BJM (2004) An ecological perspective on bacterial biodiversity. Proc R Soc Lond B Biol Sci 271:113–122CrossRefGoogle Scholar
  30. Inglis GD, McAllister TA, Larney FJ, Topp E (2010) Prolonged survival of Campylobacter species in bovine manure compost. Appl Environ Microbiol 76:1110–1119CrossRefPubMedGoogle Scholar
  31. Isbell FI, Polley HW, Wilsey BJ (2009) Species interaction mechanisms maintain grassland plant species diversity. Ecology 90:1821–1830CrossRefPubMedGoogle Scholar
  32. Jon N (2004) Biodiversity and ecosystem functioning: a complex adaptive systems approach. Limnol Oceanogr 49:1269–1277CrossRefGoogle Scholar
  33. Jones DL, Shannon D, Murphy D, Farrar J (2004) Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biol Biochem 36:749–756CrossRefGoogle Scholar
  34. Kalbitz K, Solinger S, Park JH, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: a review. Soil Sci 165:277–304CrossRefGoogle Scholar
  35. Kielak A, Pijl AS, van Veen JA, Kowalchuk GA (2008) Differences in vegetation composition and plant species identity lead to only minor changes in soil-borne microbial communities in a former arable field. FEMS Microbiol Ecol 63:372–382CrossRefPubMedGoogle Scholar
  36. Kirwan L, Scher A, Sebasti TM, Finn JA, Collins RP, Porqueddu C, Helgadottir A, Baadshaug OH, Brophy C, Coran C, Dalmannsd TS, Delgado I, Elgersma A, Fothergill M, Frankow-Lindberg BE, Golinski P, Grieu P, Gustavsson AM, Glind M, Huguenin-Elie O, Iliadis C, Rgensen M, Kadziuliene Z, Karyotis T, Lunnan T, Malengier M, Maltoni S, Meyer V, Nyfeler D, Nykanen-Kurki P, Parente J, Smit HJ, Thumm U, Connolly J (2007) Evenness drives consistent diversity effects in intensive grassland systems across 28 European sites. J Ecol 95:530–539CrossRefGoogle Scholar
  37. Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Leeuwenhoek 81:509–520CrossRefPubMedGoogle Scholar
  38. Lamb EG (2008) Direct and indirect control of species richness and evenness by litter, resources, and neighbor biomass in a native grassland. Ecology 89:216–225CrossRefPubMedGoogle Scholar
  39. Levang-Brilz N, Biondini ME (2003) Growth rate, root development and nutrient uptake of 55 plant species from the Great Plains Grasslands, USA. Plant Ecol 165:117–144CrossRefGoogle Scholar
  40. Loranger-Merciris G, Barthes L, Gastine A, Leadley P (2006) Rapid effects of plant species diversity and identity on soil microbial communities in experimental grassland ecosystems. Soil Biol Biochem 38:2336–2343CrossRefGoogle Scholar
  41. Maestre FT, Reynolds JF (2006) Spatial heterogeneity in soil nutrient supply modulates nutrient and biomass responses to multiple global change drivers in model grassland communities. Glob Chang Biol 12:2431–2441CrossRefGoogle Scholar
  42. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979CrossRefPubMedGoogle Scholar
  43. Mattingly WB, Hewlate R, Reynolds HL (2007) Species evenness and invasion resistance of experimental grassland communities. Oikos 116:1164–1170CrossRefGoogle Scholar
  44. Milcu A, Partsch S, Langel R, Scheu S (2006) The response of decomposers (earthworms, springtails and microorganisms) to variations in species and functional group diversity of plants. Oikos 112:513–524CrossRefGoogle Scholar
  45. Mills DK, Fitzgerald K, Litchfield CD, Gillevet PM (2003) A comparison of DNA profiling techniques for monitoring nutrient impact on microbial community composition during bioremediation of petroleum-contaminated soils. J Microbiol Methods 54:57–74CrossRefPubMedGoogle Scholar
  46. Mintie AT, Heichen RS, Cromack K Jr, Myrold DD, Bottomley PJ (2003) Ammonia-oxidizing bacteria along meadow-to-forest transects in the Oregon Cascade Mountains. Appl Environ Microbiol 69:3129–3136CrossRefPubMedGoogle Scholar
  47. Mommer L, van Ruijven J, de Caluwe H, Smit-Tiekstra AE, Wagemaker CA, Ouborg NJ, Bögemann GM, van der Weerden GM, Berendse F, de Kroon H (2010) Unveiling below-ground species abundance in a biodiversity experiment: a test of vertical niche differentiation among grassland species. J Ecol 98:1117–1127CrossRefGoogle Scholar
  48. Mulder CPH, Bazeley-White E, Dimitrakopoulos PG, Hector A, Scherer-Lorenzen M, Schmid B (2004) Species evenness and productivity in experimental plant communities. Oikos 107:50–63CrossRefGoogle Scholar
  49. Nijs I, Roy J (2000) How important are species richness, species evenness and interspecific differences to productivity? A mathematical model. Oikos 88:57–66CrossRefGoogle Scholar
  50. Nunan N, Daniell TJ, Singh BK, Papert A, McNicol JW, Prosser JI (2005) Links between plant and rhizoplane bacterial communities in grassland soils, characterized using molecular techniques. Appl Environ Microbiol 71:6784–6792CrossRefPubMedGoogle Scholar
  51. Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5:787–797CrossRefPubMedGoogle Scholar
  52. Orwin KH, Wardle DA (2005) Plant species composition effects on belowground properties and the resistance and resilience of the soil microflora to a drying disturbance. Plant Soil 278:205–221CrossRefGoogle Scholar
  53. Orwin KH, Wardle DA, Greenfield LG (2006) Ecological consequences of carbon substrate identity and diversity in a laboratory study. Ecology 87:580–593CrossRefPubMedGoogle Scholar
  54. Osborne CA, Rees GN, Bernstein Y, Janssen PH (2006) New threshold and confidence estimates for terminal restriction fragment length polymorphism analysis of complex bacterial communities. Appl Environ Microbiol 72:1270–1278CrossRefPubMedGoogle Scholar
  55. Ovreas L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373PubMedGoogle Scholar
  56. Park H-D, Wells GF, Bae H, Criddle CS, Francis CA (2006) Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl Environ Microbiol 72:5643–5647CrossRefPubMedGoogle Scholar
  57. Pisz JM, Lawrence JR, Schafer AN, Siciliano SD (2007) Differentiation of genes extracted from non-viable versus viable micro-organisms in environmental samples using ethidium monoazide bromide. J Microbiol Methods 71:312–318CrossRefPubMedGoogle Scholar
  58. Pucheta E, Bonamici I, Cabido M, Diaz S (2004) Below-ground biomass and productivity of a grazed site and a neighbouring ungrazed exclosure in a grassland in central Argentina. Austral Ecol 29:201–208CrossRefGoogle Scholar
  59. Smith B, Wilson JB (1996) A consumer’s guide to evenness indices. Oikos 76:70–82CrossRefGoogle Scholar
  60. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845CrossRefPubMedGoogle Scholar
  61. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  62. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefPubMedGoogle Scholar
  63. Wilsey BJ, Potvin C (2000) Biodiversity and ecosystem functioning: importance of species evenness in an old field. Ecology 81:887–892CrossRefGoogle Scholar
  64. Wilsey BJ, Chalcraft DR, Bowles CM, Willig MR (2005) Relationships among indices suggest that richness is an incomplete surrogate for grassland biodiversity. Ecology 86:1178–1184CrossRefGoogle Scholar
  65. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579CrossRefPubMedGoogle Scholar
  66. Yu Z, Kraus TEC, Dahlgren RA, Horwath WR, Zasoski RJ (2003) Mineral and dissolved organic nitrogen dynamics along a soil acidity–fertility gradient. Soil Sci Soc Am J 67:878–888CrossRefGoogle Scholar
  67. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2052CrossRefGoogle Scholar
  68. Zul D, Denzel S, Kotz A, Overmann J (2007) Effects of plant biomass, plant diversity, and water content on bacterial communities in soil lysimeters: implications for the determinants of bacterial diversity. Appl Environ Microbiol 73:6916–6929CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Eric G. Lamb
    • 1
  • Nabla Kennedy
    • 2
  • Steven D. Siciliano
    • 3
  1. 1.Department of Plant SciencesUniversity of SaskatchewanSaskatoonCanada
  2. 2.Ecosystem Science and Management ProgramUniversity of Northern British ColumbiaPrince GeorgeCanada
  3. 3.Department of Soil ScienceUniversity of SaskatchewanSaskatoonCanada

Personalised recommendations