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

Nature Ecology and Evolution

Volumn 1, Issue 5, 2017, Pages

  Epp Schmidt, Dietrich J ^a   Pouyat, Richard ^b   Szlavecz, Katalin ^c   Setälä, Heikki ^d   Kotze, D Johan ^d   Yesilonis, Ian ^b   Cilliers, Sarel ^e   Hornung, Erzsébet ^f   Dombos, Miklós ^g   Yarwood, Stephanie A ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b USDA FOREST SERVICE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d UNIVERSITY OF HELSINKI   (Finland)

^e NORTH WEST UNIVERSITY   (South Africa)

^f UNIVERSITY OF VETERINARY MEDICINE   (Hungary)

^g INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85029852729     PISSN: None     EISSN: 2397334X     Source Type: Journal    
DOI: 10.1038/s41559-017-0123     Document Type: Article

References (49)

1. Ellis, E. C. & Ramankutty, N. Putting people in the map: anthropogenic biomes of the world. Front. Ecol. Environ. 6, 439-447 (2007).
2. Foster, D. et al. The importance of land-use legacies to ecology and conservation. Bioscience 53, 77-88 (2003).
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).
4. Scheffer, M., Carpenter, S., Foley, J. A., Folke, C. & Walker, B. Catastrophic shifts in ecosystems. Nature 413, 591-596 (2001).
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).
6. Groffman, P. M. et al. Ecological homogenization of urban USA. Front. Ecol. Environ. 12, 74-81 (2014).
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).
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. 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).
10. McKinney, M. L. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247-260 (2006).
11. Olden, J. D. & Rooney, T. P. On defining and quantifying biotic homogenization. Glob. Ecol. Biogeogr. 15, 113-120 (2006).
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).
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).
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).
15. Oksanen, J. et al. Vegan: Community Ecology Package. R package version 2.0-4 (R Foundation for Statistical Computing, 2016).
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).
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).
18. Rousk, J. et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4, 1340-1351 (2010).
19. Bru, D. et al. Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J. 5, 532-542 (2011).
20. R Core Team A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2015).
21. Anderson, M. J. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245-253 (2006).
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).
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).
24. Tedersoo, L. et al. Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol. Ecol. 21, 4160-4170 (2012).
25. Barberán, A. et al. Continental-scale distributions of dust-associated bacteria and fungi. Proc. Natl Acad. Sci. USA 112, 5756-5761 (2015).
26. Taddei, F. et al. Role of mutator alleles in adaptive evolution. Nature 387, 700-702 (1997).
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).
28. Ochman, H., Lawrence, J. G. & Groisman, E. A. Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299-304 (2000).
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).
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).
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).
32. Nemergut, D. R. et al. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77, 342-356 (2013).
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).
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).
35. Newbold, T. et al. Global effects of land-use on local terrestrial biodiversity. Nature 520, 45-50 (2015).
36. Averill, C. & Hawkes, C. V. Ectomycorrhizal fungi slow soil carbon cycling. Ecol. Lett. 19, 937-947 (2016).
37. Abarenkov, K. et al. The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytol. 186, 281-285 (2010).
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).
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).
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).
41. Edgar, R. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
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).
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).
44. Aronesty, E. ea-utils (2011); https://expressionanalysis.github.io/ea-utils/
45. McCune, B. & Mefford, M. PC-ORD: Multivariate Analysis of Ecological Data (MjM Software, 2011).
46. Dufrêne, M. & Legendre, P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345-366 (1997).
47. Gastrwirth, J. et al. lawstat v. 3.0 (2015); https://cran.r-project.org/web/ packages/lawstat/index.html
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).
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).