Article | Published:

Phylogenetic-scale disparities in the soil microbial diversity–ecosystem functioning relationship

The ISME Journal (2018) | Download Citation


The historical conditions under which bacterial lineages evolve determine their functional traits, and consequently their contribution to ecosystem functions (EFs). Under significant trait conservatism, which is common in prokaryotes, phylogeny may track the evolutionary history of species and predict their functionality. Productive communities can arise from: (i) the coexistence of functional, and therefore phylogenetically distant lineages, producing high EF rates at large phylogenetic diversity (PD); (ii) the dominance of productive lineages that outcompete other clades, generating high EF at low PD. Community composition will modulate the PD–EF relationship: The effects of anciently divergent lineages, whose deeply conserved functions determine the occupancy of major niches, may differ from that of recently divergent lineages showing adaptations to current conditions. We hypothesized that, in our model Mediterranean ecosystem, EF can be explained both by competitive superiority of ancient lineages and functional complementarity of recent lineages. To test this hypothesis, we sequenced a phylogenetic marker targeting bacteria across 28 soil plots and quantified EF related to microbial productivity, decomposition and nutrient cycling. Plots accumulating recently divergent lineages consistently showed higher EF levels that were slightly modified by the accumulation of ancient lineages. We discuss the assembly processes behind these phylogenetic-scale disparities and the final outcome in terms of ecosystem functioning.

  • Subscribe to The ISME Journal for full access:



Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.


  1. 1.

    Bardgett RD, Van der Putten WH. Belowground diversity and ecosystem functioning. Nature. 2014;515:505–511.

  2. 2.

    Gravel D, Bell T, Barbera C, Bouvier T, Pommeir T, Venail P, et al. Experimental niche evolution alters the strength of the diversity-productivity relationship. Nature. 2011;469:89–92.

  3. 3.

    Midgley GF. Biodiversity and ecosystem function. Science. 2012;335:174–175.

  4. 4.

    Van der Heijden MGA, Bardgett RD, van Straalen NM. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett. 2008;11:296–310.

  5. 5.

    Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH. Ecological linkages between aboveground and belowground biota. Science. 2004;304:1629–1633.

  6. 6.

    Hooper DU, Chapin ES III, Ewel JJ, Hector A, Inchausti P, Lavorel S, et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr. 2005;75:3–35.

  7. 7.

    Díaz S, Purvis A, Cornelissen JHC, Mace GM, Donoghue MJ, Ewers RM, et al. Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecol Evol. 2013;3(9):2958–2975.

  8. 8.

    Wilson EO. Biodiversity. Washington D.C., USA: National Academy Press; 1988.

  9. 9.

    Goberna M, Verdú M. Predicting microbial traits with phylogenies. ISME J. 2016;10:959–967.

  10. 10.

    Blomberg SP, Garland T Jr, Ives AR. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution. 2003;57:717–745.

  11. 11.

    Flynn DF, Mirotchnick N, Jain M, Palmer MI, Naeem S. Functional and phylogenetic diversity as predictors of biodiversity–ecosystem-function relationships. Ecology. 2011;92:1573–1581.

  12. 12.

    Cadotte MW. Experimental evidence that evolutionarily diverse assemblages result in higher productivity. Proc Natl Acad Sci USA. 2013;110:8996–9000.

  13. 13.

    Navarro-Cano JA, Goberna M, Valiente-Banuet A, Montesinos-Navarro A, García C, Verdú M. Plant phylodiversity enhances soil microbial productivity in facilitation-driven communities. Oecologia. 2014;174:909–920.

  14. 14.

    Pérez-Valera E, Goberna M, Verdú M. Phylogenetic structure of soil bacterial communities predicts ecosystem functioning. FEMS Microbiol Ecol. 2015;91:fiv031.

  15. 15.

    Srivastava DS, Cadotte MW, MacDonald AAM, Marushia RG, Mirotchnick N. Phylogenetic diversity and the functioning of ecosystems. Ecol Lett. 2012;15:637–648.

  16. 16.

    Gravel D, Bell T, Barbera C, Combe M, Pommier T, Mouquet N. Phylogenetic constraints on ecosystem functioning. Nat Comm. 2012;3:1117.

  17. 17.

    Cadotte MW, Davies JT, Peres-Neto PR. Why phylogenies do not always predict ecological differences. Ecol Monogr. 2017;87:535–551.

  18. 18.

    Venail P, Gross K, Oakley TH, Narwani A, Allan E, Flombaum P, et al. Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct Ecol. 2015;29:615–626.

  19. 19.

    de Bello F, Šmilauer P, Diniz-Filho JAF, Carmona CP, Lososová Z, Herben T, et al. Decoupling phylogenetic and functional diversity to reveal hidden signals in community assembly. Methods Ecol Evol. 2017;8:1200–1211.

  20. 20.

    Martiny AC, Treseder K, Pusch G. Phylogenetic conservatism of functional traits in microorganisms. ISME J. 2013;7:830–838.

  21. 21.

    Cavender-Bares J, Ackerly DD, Hobbie SE, Townsend PA. Evolutionary legacy effects on ecosystems: biogeographic origins, plant traits, and implications for management in the Era of global change. Annu Rev Ecol Evol Syst. 2016;47:433–462.

  22. 22.

    Davies TJ, Urban M, Rayfield B, Cadotte MW, Peres-Neto PR. Deconstructing the relationships between phylogenetic diversity and ecology: a case study on ecosystem functioning. Ecology. 2016;97:2212–2222.

  23. 23.

    Groussin M, Mazel F, Sanders J, Smillie C, Lavergne S, Thuiller W, et al. Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nat Comm. 2017;8:14319.

  24. 24.

    Mazel F, Davies TJ, Gallien L, Renaud J, Groussin M, Münkemüller T, Thuiller W. Influence of tree shape and evolutionary time-scale on phylogenetic diversity metrics. Ecography. 2015;39:913–920.

  25. 25.

    Yguel B, Jactel H, Pearse IS, Moen D, Winter M, Hortal J, et al. The evolutionary legacy of diversification predicts ecosystem function. Am Nat. 2016;188:398–410.

  26. 26.

    Herrera CM. Historical effects and sorting processes as explanations for contemporary ecological patterns: character syndromes in Mediterranean woody plants. Am Nat. 1992;140:421–446.

  27. 27.

    Valiente-Banuet A, Vital A, Verdú M, Callaway R. Modern Quaternary plant lineages promote diversity through facilitation of ancient Tertiary lineages. Proc Natl Acad Sci USA. 2006;103:16812–16817.

  28. 28.

    Martiny JBH, Jones SE, Lennon JT, Martiny AC. Microbiomes in light of traits: a phylogenetic perspective. Science. 2015;350:aac9323-1–8.

  29. 29.

    Carroll IT, Cardinale BJ, Nisbet RM. Niche and fitness differences relate the maintenance of diversity to ecosystem function. Ecology. 2011;92:1157–1165.

  30. 30.

    Pianka ER. Evolutionary ecology. 7th edn – ebook. 2011.

  31. 31.

    Goberna M, Navarro-Cano JA, Verdú M. Opposing phylogenetic diversity gradients of plant and soil bacterial communities. Proc R Soc London B. 2016;283.

  32. 32.

    Mayfield MM, Levine JM. Opposing effects of competitive exclusion on the phylogenetic structure of the communities. Ecol Lett. 2010;13:1085–1093.

  33. 33.

    Morrissey EM, Mau RL, Schwartz E, Caporaso JG, Dijkstra P, van Gestel N, et al. Phylogenetic organization of bacterial activity. ISME J. 2016;10:2336–2340.

  34. 34.

    Fierer N, Bradford MA, Jackson RB. Toward an ecological classification of soil bacteria. Ecology. 2007;88:1354–1364.

  35. 35.

    Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, et al. Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Micro. 2011;2:1–10.

  36. 36.

    Goberna M, García C, Verdú M. A role for biotic filtering in driving phylogenetic clustering in soil bacterial communities. Glob Ecol Biogeog. 2014;23:1346–1355.

  37. 37.

    Hodapp D, Hillebrand H, Blasius B, Ryabov AB. Environmental and trait variability constrain community structure and the biodiversity-productivity relationship. Ecology. 2016;97(6):1463–1474.

  38. 38.

    Isbell F, Cowles J, Dee LE, Loreau M, Reich PB, Gonzalez A, et al. Quantifying effects of biodiversity on ecosystem functioning across times and places. Ecol Lett. 2018;21(6):763–778.

  39. 39.

    Cadotte MW. Functional traits explain ecosystem function through opposing mechanisms. Ecol Lett. 2017;20:989–996.

  40. 40.

    Goberna M, Navarro-Cano JA, Valiente-Banuet A, García C, Verdú M. Abiotic stress tolerance and competition related traits underlie phylogenetic clustering in soil bacterial communities. Ecol Lett. 2014;17:1191–1201.

  41. 41.

    Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB, Cornell HV, et al. Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett. 2010;13:1310–1324.

  42. 42.

    Goberna M, Pascual JA, García C, Sánchez J. Do plant clumps constitute microbial hotspots in semi-arid Mediterranean patchy landscapes? Soil Biol Biochem. 2007;39:1047–1054.

  43. 43.

    Turner S, Pryer KM, Miao VPW, Palmer JD. Investigating deep phylogenetic relationships among Cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol. 1999;46:327–338.

  44. 44.

    Muyzer G, De Waal EC, Uitterlinden AG. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol. 1993;59:695–700.

  45. 45.

    Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, et al. The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009;37:D141–145.

  46. 46.

    Nawrocki EP, Eddy SR. Query-dependent banding (QDB) for faster RNA similarity searches. PLoS Comput Biol. 2007;3:e56.

  47. 47.

    Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–5267.

  48. 48.

    Kembel SW, Wu M, Eisen JA, Green JL. Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comp Biol. 2012;8:e1002743.

  49. 49.

    Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–2690.

  50. 50.

    Lane DJ. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. New York, NY: Wiley; 1991. p. 115–175.

  51. 51.

    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl Acids Res. 2013;41:D590–D596. (D1)

  52. 52.

    Sheridan PP, Freeman KH, Brenchley JE. Estimated minimal divergence times of the major bacterial and archaeal phyla. Geomicrobiol J. 2003;20:1–14.

  53. 53.

    Marin J, Battistuzzi FU, Brown AC, Hedges SB. The timetree of prokaryotes: new insights into their evolution and speciation. Mol Biol Evol. 2017;34:437–446.

  54. 54.

    Smith SA, O’Meara BC. treePL: divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics. 2012;28(20):2689–2690.

  55. 55.

    Vance ED, Brookes PC, Jenkinson DS. An extraction method for measuring soil microbial biomass C. Soil Biol Biochem. 1987;19:703–707.

  56. 56.

    Webster JJ, Hampton GJ, Leach FR. ATP in soil: a new extractant and extraction procedure. Soil Biol Biochem. 1984;16:335–342.

  57. 57.

    Alef K, Nannipieri P. Methods in applied soil microbiology and biochemistry. London: Academic Press; 1995.

  58. 58.

    Nannipieri P, Grego S, Ceccanti B. Ecological significance of the biological activity in soil. In: Bollag JM, Stotzky G, editors. Soil biochemistry. New York, NY: Marcel Dekker; 1990. p. 293–355.

  59. 59.

    Yeoman CJ, Han Y, Dodd D, Schroeder CM, Mackie RI, Cann IKO. Thermostable enzymes as biocatalysts in the biofuel industry. Adv Appl Microbiol. 2010;70:1–55. e-pub

  60. 60.

    Tabatabai MA. Soil enzymes. In: Bottomley PS, Angle JS, Weaver RW, editors. Methods of soil analysis, Part 2. Microbiological and biochemical properties. Madison: SSSA Book Series, no 5. Soil Science Society of America; 1994. p. 775–833.

  61. 61.

    Eivazi F, Tabatabai MA. Glucosidases and galactosidases in soils. Soil Biol Biochem. 1988;20:601–606.

  62. 62.

    Tabatabai MA, Bremner JM. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem. 1969;1:301–307.

  63. 63.

    Kandeler E, Gerber H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fert Soils. 1988;6:68–72.

  64. 64.

    Kraft NJB, Cornwell WK, Webb CO, Ackerly DD. Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat. 2007;170:271–283.

  65. 65.

    Tucker CM, Cadotte MW, Carvalho SB, Davies TJ, Ferrier S, Fritz SA, et al. A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol Rev. 2017;92:698–715.

  66. 66.

    Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics. 2010;26:1463–1464.

  67. 67.

    Webb CO, Ackerly DD, McPeek MA, Donoghue MJ. Phylogenies and community ecology. Annu Rev Ecol Syst. 2002;33:475–505.

  68. 68.

    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2017.

  69. 69.

    Schloss PD, Handelsman J. Towards a census of bacteria in soil. PLoS Comput Biol. 2006;2(7):e92

  70. 70.

    Hutchinson GE. The paradox of the plankton. Am Nat. 1961;95:137–145.

  71. 71.

    Chesson P. Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst. 2000;31:343–366.

  72. 72.

    HilleRisLambers J, Adler PB, Harpole WS, Levine MS, Mayfield MM. Rethinking community assembly through the lens of coexistence theory. Annu Rev Ecol Evol Syst. 2012;43:227–248.

  73. 73.

    Qian H, Chen S, Zhang JL. Disentangling environmental and spatial effects on phylogenetic structure of angiosperm tree communities in China. Sci Rep. 2017; 7.

  74. 74.

    Turnbull LA, Isbell F, Purves DW, Loreau M, Hector A. Understanding the value of plant diversity for ecosystem functioning through niche theory. Proc R Soc B. 2016;283:20160536.

  75. 75.

    Tazisong IA, Senwo ZN, He Z. Phosphatase hydrolysis of organic phosphorus compounds. Adv Enz Res. 2015;3:39–51.

  76. 76.

    Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad USA. 2015;112:10967–10972.

  77. 77.

    Zhou J, Jiang X, Wei D, Zhao B, Ma M, Chen S, et al. Consistent effects of nitrogen fertilization on soil bacterial communities in black soils for two crop seasons in China. Sci Rep. 2017;7:3267.

  78. 78.

    Gallien L. Intransitive competition and its effects on community functional diversity. Oikos. 2017;126:615–623.

  79. 79.

    Godoy O, Kraft NJB, Levine JM. Phylogenetic relatedness and the determinants of competitive outcomes. Ecol Lett. 2014;17:836–844.

Download references


Thanks to B Yguel, J Hortal and E Pérez-Valera for helping with the ELDERness models. Financial support was provided by the Spanish Ministry of Economy and Competitiveness (CGL2014-58333-P; CGL2016-81706-REDT; CGL2017-89751-R) and the Generalitat Valenciana (SEJI/2017/030). MG acknowledges support by the Ramón y Cajal Programme of the Spanish Ministry of Economy and Competitiveness.

Author information


  1. Centro de Investigaciones Sobre Desertificación (CIDE; CSIC-UV-GV), Carretera Moncada-Náquera km. 4.5, Valencia, E-46113, Spain

    • Marta Goberna
    •  & Miguel Verdú


  1. Search for Marta Goberna in:

  2. Search for Miguel Verdú in:

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Miguel Verdú.

Electronic supplementary material

About this article

Publication history






Rights and permissions

To obtain permission to re-use content from this article visit RightsLink.