Urbanization erodes ectomycorrhizal fungal diversity and may cause microbial communities to converge


Urbanization alters the physicochemical environment, introduces non-native species and causes ecosystem characteristics to converge. It has been speculated that these alterations contribute to loss of regional and global biodiversity, but so far most urban studies have assessed macro-organisms and reported mixed evidence for biodiversity loss. We studied five cities on three continents to assess the global convergence of urban soil microbial communities. We determined the extent to which communities of bacteria, archaea and fungi are geographically distributed, and to what extent urbanization acts as a filter on species diversity. We discovered that microbial communities in general converge, but the response differed among microbial domains; soil archaeal communities showed the strongest convergence, followed by fungi, while soil bacterial communities did not converge. Our data suggest that urban soil archaeal and bacterial communities are not vulnerable to biodiversity loss, whereas urbanization may be contributing to the global diversity loss of ectomycorrhizal fungi. Ectomycorrhizae decreased in both abundance and species richness under turf and ruderal land-uses. These data add to an emerging pattern of widespread suppression of ectomycorrhizal fungi by human land-uses that involve physical disruption of the soil, management of the plant community, or nutrient enrichment.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Geographic distribution of cities sampled, edaphic co-factors and community composition.
Figure 2: Effect of land-use on beta diversity, abundance and alpha diversity of microbial domains.
Figure 3: Within-group multivariate dispersal by grouping variable in each domain.
Figure 4: Relationship bewtween land-use, and ECM diversity and abundance.


  1. 1

    Ellis, E. C. & Ramankutty, N. Putting people in the map: anthropogenic biomes of the world. Front. Ecol. Environ. 6, 439–447 (2007).

    Article  Google Scholar 

  2. 2

    Foster, D. et al. The importance of land-use legacies to ecology and conservation. Bioscience 53, 77–88 (2003).

    Article  Google Scholar 

  3. 3

    Rothwell, A., Ridoutt, B., Page, G. & Bellotti, W. Feeding and housing the urban population: environmental impacts at the peri-urban interface under different land-use scenarios. Land Use Policy 48, 377–388 (2015).

    Article  Google Scholar 

  4. 4

    Scheffer, M., Carpenter, S., Foley, J. A., Folke, C. & Walker, B. Catastrophic shifts in ecosystems. Nature 413, 591–596 (2001).

    CAS  Article  Google Scholar 

  5. 5

    Pouyat, R. V. et al. A global comparison of surface soil characteristics across five cities: a test of the urban ecosystem convergence hypothesis. Soil Sci. 180, 136–145 (2015).

    CAS  Article  Google Scholar 

  6. 6

    Groffman, P. M. et al. Ecological homogenization of urban USA. Front. Ecol. Environ. 12, 74–81 (2014).

    Article  Google Scholar 

  7. 7

    McKinney, M. L. & Lockwood, J. L. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol. Evol. 14, 450–453 (1999).

    CAS  Article  Google Scholar 

  8. 8

    Baiser, B., Olden, J. D., Record, S., Lockwood, J. L. & McKinney, M. L. Pattern and process of biotic homogenization in the New Pangaea. Proc. R. Soc. B 279, 4772–4777 (2012).

  9. 9

    Tabarelli, M., Peres, C. A. & Melo, F. P. L. The ‘few winners and many losers’ paradigm revisited: emerging prospects for tropical forest biodiversity. Biol. Conserv. 155, 136–140 (2012).

    Article  Google Scholar 

  10. 10

    McKinney, M. L. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260 (2006).

    Article  Google Scholar 

  11. 11

    Olden, J. D. & Rooney, T. P. On defining and quantifying biotic homogenization. Glob. Ecol. Biogeogr. 15, 113–120 (2006).

    Article  Google Scholar 

  12. 12

    Fukami, T., Martijn Bezemer, T., Mortimer, S. R. & van der Putten, W. H. Species divergence and trait convergence in experimental plant community assembly. Ecol. Lett. 8, 1283–1290 (2005).

    Article  Google Scholar 

  13. 13

    Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).

    CAS  Article  Google Scholar 

  14. 14

    Boyero, L. et al. Global patterns of stream detritivore distribution: implications for biodiversity loss in changing climates. Glob. Ecol. Biogeogr. 21, 134–141 (2012).

    Article  Google Scholar 

  15. 15

    Oksanen, J. et al. Vegan: Community Ecology Package. R package version 2.0-4 (R Foundation for Statistical Computing, 2016).

  16. 16

    Reese, A. T. et al. Urban stress is associated with variation in microbial species composition—but not richness—in Manhattan. ISME J. 10, 751–760 (2016).

    Article  Google Scholar 

  17. 17

    Fierer, N., Strickland, M. S., Liptzin, D., Bradford, M. A. & Cleveland, C. C. Global patterns in belowground communities. Ecol. Lett. 12, 1238–1249 (2009).

    Article  Google Scholar 

  18. 18

    Rousk, J. et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4, 1340–1351 (2010).

    Article  Google Scholar 

  19. 19

    Bru, D. et al. Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J. 5, 532–542 (2011).

    CAS  Article  Google Scholar 

  20. 20

    R Core Team A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2015).

  21. 21

    Anderson, M. J. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253 (2006).

    Article  Google Scholar 

  22. 22

    Karpati, A. S., Handel, S. N., Dighton, J. & Horton, T. R. Quercus rubra-associated ectomycorrhizal fungal communities of disturbed urban sites and mature forests. Mycorrhiza 21, 537–547 (2011).

    Article  Google Scholar 

  23. 23

    Jumpponen, A. & Egerton-Warburton, L. M. in The Fungal Community: Its Organization and Role in the Ecosystem 3rd edn (eds Dighton, J., White, J. F. & Oudemans, P.) Ch. 7, 130–164 (Mycology Series Vol. 23, 2005).

    Google Scholar 

  24. 24

    Tedersoo, L. et al. Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol. Ecol. 21, 4160–4170 (2012).

    Article  Google Scholar 

  25. 25

    Barberán, A. et al. Continental-scale distributions of dust-associated bacteria and fungi. Proc. Natl Acad. Sci. USA 112, 5756–5761 (2015).

    Article  Google Scholar 

  26. 26

    Taddei, F. et al. Role of mutator alleles in adaptive evolution. Nature 387, 700–702 (1997).

    CAS  Article  Google Scholar 

  27. 27

    Tenaillon, O., Toupance, B., Nagard, H. L., Taddei, F. & Godelle, B. Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics 152, 485–493 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28

    Ochman, H., Lawrence, J. G. & Groisman, E. A. Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304 (2000).

    CAS  Article  Google Scholar 

  29. 29

    Verhamme, D. T., Prosser, J. I. & Nicol, G. W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 5, 1067–1071 (2011).

    CAS  Article  Google Scholar 

  30. 30

    Nicol, G. W., Leininger, S., Schleper, C. & Prosser, J. I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10, 2966–2978 (2008).

    CAS  Article  Google Scholar 

  31. 31

    Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C. & Martiny, J. B. H. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506 (2012).

    CAS  Article  Google Scholar 

  32. 32

    Nemergut, D. R. et al. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77, 342–356 (2013).

    Article  Google Scholar 

  33. 33

    Ramirez, K. S. et al. Biogeographic patterns in below-ground diversity in New York City’s Central Park are similar to those observed globally. Proc. R. Soc. B 281, 20141988 (2014).

    Article  Google Scholar 

  34. 34

    Högberg, M. N., Yarwood, S. A. & Myrold, D. D. Fungal but not bacterial soil communities recover after termination of decadal nitrogen additions to boreal forest. Soil Biol. Biochem. 72, 35–43 (2014).

    Article  Google Scholar 

  35. 35

    Newbold, T. et al. Global effects of land-use on local terrestrial biodiversity. Nature 520, 45–50 (2015).

    CAS  Article  Google Scholar 

  36. 36

    Averill, C. & Hawkes, C. V. Ectomycorrhizal fungi slow soil carbon cycling. Ecol. Lett. 19, 937–947 (2016).

    Article  Google Scholar 

  37. 37

    Abarenkov, K. et al. The UNITE database for molecular identification of fungi – recent updates and future perspectives. New Phytol. 186, 281–285 (2010).

    Article  Google Scholar 

  38. 38

    Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624 (2012).

    CAS  Article  Google Scholar 

  39. 39

    Fierer, N., Jackson, J. A., Vilgalys, R. & Jackson, R. B. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl. Environ. Microbiol. 71, 4117–4120 (2005).

    CAS  Article  Google Scholar 

  40. 40

    Hargreaves, S. K., Roberto, A. A. & Hofmockel, K. S. Reaction- and sample-specific inhibition affect standardization of Q-PCR assays of soil bacterial communities. Soil Biol. Biochem. 59, 89–97 (2013).

    CAS  Article  Google Scholar 

  41. 41

    Edgar, R. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).

    CAS  Article  Google Scholar 

  42. 42

    Wang, Q., Garrity, G., Tiedje, J. & Cole, J. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).

    CAS  Article  Google Scholar 

  43. 43

    DeSantis, T. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072 (2006).

    CAS  Article  Google Scholar 

  44. 44

    Aronesty, E. ea-utils (2011); https://expressionanalysis.github.io/ea-utils/

  45. 45

    McCune, B. & Mefford, M. PC-ORD: Multivariate Analysis of Ecological Data (MjM Software, 2011).

    Google Scholar 

  46. 46

    Dufrêne, M. & Legendre, P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366 (1997).

    Google Scholar 

  47. 47

    Gastrwirth, J. et al. lawstat v. 3.0 (2015); https://cran.r-project.org/web/packages/lawstat/index.html

  48. 48

    Nguyen, N. H. et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20, 241–248 (2016).

    Article  Google Scholar 

  49. 49

    Dlott, G., Maul, J. E., Buyer, J. & Yarwood, S. Microbial rRNA:rDNA gene ratios may be unexpectedly low due to extracellular DNA preservation in soils. J. Microbiol. Methods 115, 112–120 (2015).

    CAS  Article  Google Scholar 

Download references


This research was funded through NSF ACI 1244820; soil chemical analysis was funded through SZIE-ÁOTK: KK-UK-12007. We acknowledge G. Dlott for technical support in QIIME, and R. E. Draskovits, S. Molnar, E. Powell, M. Bernard, Z. Toth and S. Mishra assisted with field sampling.

Author information




D.J.E.S. constructed the DNA and sequencing libraries, and conducted Q-PCR, bioinformatics processing and statistical analyses. K.S. is the PI of the grant, designed the study and selected the sites in Baltimore. R.V.P., H.S., D.J.K., E.H., S.C. and I.Y. designed the study, selected the sites and participated in soil sampling. M.D. participated in soil sampling and provided nutrient data on soils; S.A.Y. designed the study, and oversaw all of the lab work, bioinformatics and data analysis. All authors discussed results and commented on the manuscript.

Corresponding author

Correspondence to Stephanie A. Yarwood.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–5, Supplementary Tables 1–8, Supplementary References (PDF 1821 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Epp Schmidt, D., Pouyat, R., Szlavecz, K. et al. Urbanization erodes ectomycorrhizal fungal diversity and may cause microbial communities to converge. Nat Ecol Evol 1, 0123 (2017). https://doi.org/10.1038/s41559-017-0123

Download citation

Further reading