Soil microbial community structure of range-expanding plant species differs from co-occurring natives

Journal of Ecology

Volumn 101, Issue 5, 2013, Pages 1093-1102

  Morriën, Elly ^a   van der Putten, Wim H ^a,b  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Denaturating gradient gel electrophoresis; Ergosterol; Invasion ecology; Invasive plants; Legacy effects; Phylogenetically controlled comparison; Plant soil feedback; Range shift; Real time PCR; Rhizosphere microbial community; Soil pathogens

Indexed keywords

ABUNDANCE; ACCUMULATION; BIOMASS; COMMUNITY STRUCTURE; CONDITIONING; ELECTROKINESIS; ERGOSTEROL; GLOBAL WARMING; HARVESTING; MICROBIAL COMMUNITY; PLANT; POLYMERASE CHAIN REACTION; RANGE EXPANSION; RHIZOSPHERE; SOIL; SOIL BIOTA;

ARBUSCULAR; BACTERIA (MICROORGANISMS); FUNGI; FUSARIUM;

EID: 84883299175     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12117     Document Type: Article

References (67)

1. Agrawal, A.A., Kotanen, P.M., Mitchell, C.E., Power, A.G., Godsoe, W. & Klironomos, J. (2005) Enemy release? An experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology, 86, 2979-2989.
2. Ayres, E., Steltzer, H., Simmons, B.L., Simpson, R.T., Steinweg, J.M., Wallenstein, M.D., Mellor, N., Parton, W.J., Moore, J.C. & Wall, D.H. (2009) Home-field advantage accelerates leaf litter decomposition in forests. Soil Biology & Biochemistry, 41, 606-610.
3. 14C-acetate incorporation into ergosterol. Soil Biology & Biochemistry, 33, 2011-2018.
4. Bennett, A.E., Alers-Garcia, J. & Bever, J.D. (2006) Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. American Naturalist, 167, 141-152.
5. Berg, G. & Smalla, K. (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. Fems Microbiology Ecology, 68, 1-13.
6. Berg, M.P., Kiers, E.T., Driessen, G., Van der Heijden, M., Kooi, B.W., Kuenen, F., Liefting, M., Verhoef, H.A. & Ellers, J. (2010) Adapt or disperse: understanding species persistence in a changing world. Global Change Biology, 16, 587-598.
7. Bever, J.D. (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytologist, 157, 465-473.
8. Bever, J.D., Westover, K.M. & Antonovics, J. (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. Journal of Ecology, 85, 561-573.
9. Booth, C. (1971) The Genus Fusarium. Farnham Royal, Commonwealth Agricultural Bureaux [for the] Commonwealth Mycological Institute.
10. Callaway, R.M., Thelen, G.C., Rodriguez, A. & Holben, W.E. (2004) Soil biota and exotic plant invasion. Nature, 427, 731-733.
11. Carney, K.M. & Matson, P.A. (2005) Plant communities, soil microorganisms, and soil carbon cycling: Does altering the world belowground matter to ecosystem functioning? Ecosystems, 8, 928-940.
12. Chapman, S.K. & Koch, G.W. (2007) What type of diversity yields synergy during mixed litter decomposition in a natural forest ecosystem? Plant and Soil, 299, 153-162.
13. Clarke, K.R. (1993) Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology, 18, 117-143.
14. De Boer, W., Kowalchuk, G.A. & Van Veen, J.A. (2006) 'Root-food' and the rhizosphere microbial community composition. New Phytologist, 170, 3-6.
15. Diez, J.M., Dickie, I., Edwards, G., Hulme, P.E., Sullivan, J.J. & Duncan, R.P. (2010) Negative soil feedbacks accumulate over time for non-native plant species. Ecology Letters, 13, 803-809.
16. Eisenhauer, N., Milcu, A., Sabais, A.C.W., Bessler, H., Brenner, J., Engels, C. et al. (2011) Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term. PLoS ONE, 6, e16055.
17. Engelkes, T., Morriën, E., Verhoeven, K.J.F., Bezemer, T.M., Biere, A., Harvey, J.A., McIntyre, L.M., Tamis, W.L.M. & van der Putten, W.H. (2008) Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature, 456, 946-948.
18. Eom, A.H., Hartnett, D.C. & Wilson, G.W.T. (2000) Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia, 122, 435-444.
19. Funk, J.L. & Vitousek, P.M. (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature, 446, 1079-1081.
20. Gholz, H.L., Wedin, D.A., Smitherman, S.M., Harmon, M.E. & Parton, W.J. (2000) Long-term dynamics of pine and hardwood litter in contrasting environments: toward a global model of decomposition. Global Change Biology, 6, 751-765.
21. Gollote, A., van Tuinen, D. & Atkinson, D. (2004) Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza, 14, 111-117.
22. Gomes, N.C.M., Fagbola, O., Costa, R., Rumjanek, N.G., Buchner, A., Mendonca-Hagler, L. & Smalla, K. (2003) Dynamics of fungal communities in bulk and maize rhizosphere soil in the tropics. Applied and Environmental Microbiology, 69, 3758-3766.
23. van Grunsven, R.H.A., van der Putten, W.H., Bezemer, T.M., Tamis, W.L.M., Berendse, F. & Veenendaal, E.M. (2007) Reduced plant-soil feedback of plant species expanding their range as compared to natives. Journal of Ecology, 95, 1050-1057.
24. van Grunsven, R.H.A., van der Putten, W.H., Bezemer, T.M., Berendse, F. & Veenendaal, E.M. (2010) Plant-soil interactions in the expansion and native range of a poleward shifting plant species. Global Change Biology, 16, 380-385.
25. Hartmann, A., Schmid, M., Tuinen, D. & Berg, G. (2009) Plant-driven selection of microbes. Plant and Soil, 321, 235-257.
26. Heuer, H., Krsek, M., Baker, P., Smalla, K. & Wellington, E. (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel electrophoretic separation in denaturating gradients. Applied and Environmental Microbiology, 63, 3233-3241.
27. Hickling, R., Roy, D.B., Hill, J.K., Fox, R. & Thomas, C.D. (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Global Change Biology, 12, 450-455.
28. Inderjit & van der Putten, W.H. (2010) Impacts of soil microbial communities on exotic plant invasions. Trends in Ecology & Evolution, 25, 512-519.
29. Klironomos, J.N. (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature, 417, 67-70.
30. Klironomos, J.N. (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology, 84, 2292-2301.
31. Kowalchuk, G.A., Buma, D.S., de Boer, W., Klinkhamer, P.G.L. & van Veen, J.A. (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 81, 509-520.
32. Legendre, P. & Anderson, M.J. (1999) Distance-based redundancy analysis: Testing multispecies responses in multifactorial ecological experiments. Ecological Monographs, 69, 1-29.
33. Legendre, P. & Legendre, L. (1998) Numerical Ecology. Elsevier, Amsterdam.
34. Marschner, P., Yang, C.H., Lieberei, R. & Crowley, D.E. (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biology & Biochemistry, 33, 1437-1445.
35. Menendez, R., Gonzalez-Megias, A., Lewis, O.T., Shaw, M.R. & Thomas, C.D. (2008) Escape from natural enemies during climate-driven range expansion: a case study. Ecological Entomology, 33, 413-421.
36. Mille-Lindblom, C., von Wachenfeldt, E. & Tranvik, L.J. (2004) Ergosterol as a measure of living fungal biomass: persistence in environmental samples after fungal death. Journal of Microbiological Methods, 59, 253-262.
37. Mitchell, C.E. & Power, A.G. (2003) Release of invasive plants from fungal and viral pathogens. Nature, 421, 625-627.
38. Mitchell, C.E., Blumenthal, D., Jarosik, V., Puckett, E.E. & Pysek, P. (2010) Controls on pathogen species richness in plants' introduced and native ranges: roles of residence time, range size and host traits. Ecology Letters, 13, 1525-1535.
39. Moora, M., Berger, S., Davison, J., Öpik, M., Bommarco, R., Bruelheide, H. et al. (2011) Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study massively parallel 454 sequencing. Journal of Biogeography, 38, 1305-1317.
40. Muyzer, G., Dewaal, E.C. & Uitterlinden, A.G. (1993) Profiling of complex microbial populations by Denaturing Gradient Gel Electrophoresis analysis of Polymerase Chain Reaction amplified genes coding for 16S ribosomal-RNA. Applied and Environmental Microbiology, 59, 695-700.
41. Nelson, E.B. (1990) Exudates molecules initiating fungal responses to seeds and roots. Plant and Soil, 129, 61-73.
42. Newsham, K.K., Fitter, A.H. & Watkinson, A.R. (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. Journal of Ecology, 83, 991-1000.
43. Olsson, P.A., Larsson, L., Bago, B., Wallander, H. & van Aarle, I.M. (2003) Ergosterol and fatty acids for biomass estimation of mycorrhizal fungi. New Phytologist, 159, 7-10.
44. Packer, A. & Clay, K. (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature, 404, 278-281.
45. Parmesan, C. & Yohe, G. (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42.
46. Pearson, R.G. & Dawson, T.P. (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecology and Biogeography, 12, 361-371.
47. Petermann, J.S., Fergus, A.J.F., Turnbull, L.A. & Schmid, B. (2008) Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecology, 89, 2399-2406.
48. Pregitzer, C.C., Bailey, J.K., Hart, S.C. & Schweitzer, J.A. (2010) Soils as agents of selection: feedbacks between plants and soils alter seedling survival and performance. Evolutionary Ecology, 24, 1045-1059.
49. Pringle, A., Bever, J.D., Gardes, M., Parrent, J.L., Rillig, M.C. & Klironomos, J.N. (2009) Mycorrhizal symbioses and plant invasions. Annual Review of Ecology Evolution and Systematics, 40, 699-715.
50. van der Putten, W.H., Klironomos, J.N. & Wardle, D.A. (2007) Microbial ecology of biological invasions. ISME Journal, 1, 28-37.
51. van der Putten, W.H., de Ruiter, P.C., Bezemer, T.M., Harvey, J.A., Wassen, M. & Wolters, V. (2004) Trophic interactions in a changing world. Basic and Applied Ecology, 5, 487-494.
52. Reinhart, K.O. & Callaway, R.M. (2006) Soil biota and invasive plants. New Phytologist, 170, 445-457.
53. Reinhart, K.O., Packer, A., van der Putten, W.H. & Clay, K. (2003) Plant-soil biota interactions and spatial distributions of black cherry in its native and invasive ranges. Ecology Letters, 6, 1046-1050.
54. Richardson, D.M., Allsopp, N., D'Antonio, C.M., Milton, S.J. & Rejmanek, M. (2000) Plant invasions - the role of mutualisms. Biological Reviews, 75, 65-93.
55. de Ridder-Duine, A.S., Smant, W., van der Wal, A., van Veen, J.A. & de Boer, W. (2006) Evaluation of a simple, non-alkaline extraction protocol to quantify soil ergosterol. Pedobiologia, 50, 293-300.
56. Sanon, A., Andrianjaka, Z., Prin, Y., Bally, R., Thioulouse, J., Comte, G. & Duponnois, R. (2009) Rhizosphere microbiota interfers with plant-plant interactions. Plant and Soil, 321, 259-278.
57. Suding, K.N., Harpole, W.S., Fukami, T., Kulmatiski, A., MacDougall, A.S., Stein, C. & van der Putten, W.H. (2013) Consequences of plant-soil feedbacks in invasion. Journal of Ecology, 101, 298-308.
58. Tamis, W.L.M. (2005) Changes in the flora of the Netherlands in the 20th century. Gorteria Supplement, 6, 153-229.
59. Ter Braak, C.J.F. & Šmilauer, P. (2002) CANOCO Reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, NY, USA.
60. Thuiller, W., Richardson, D.M. & Midgley, G.F. (2007) Will Climate Change Promote Alien Plant Invasions? Biological Invasions (ed. W. Nentwig), pp. 197-211. Springer-Verlag, Heidelberg.
61. Vainio, E.J. & Hantula, J. (2000) Direct analysis of wood-inhabiting fungi using denaturating gradient gel electrophoresis of amplified ribosomal DNA. Mycological Research, 104, 927-936.
62. Walker, T.S., Bais, H.P., Grotewold, E. & Vivanco, J.M. (2003) Root exudation and rhizosphere biology. Plant Physiology, 132, 44-51.
63. Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.M., Hoegh-Guldberg, O. & Bairlein, F. (2002) Ecological responses to recent climate change. Nature, 416, 389-395.
64. Welch, B.L. (1947) The generalization of 'Students'problem when several different population variances are involved. Biometrika, 34, 28-35.
65. Yang, C.H. & Crowley, D.E. (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Applied and Environmental Microbiology, 66, 345-351.
66. Yergeau, E., Filion, M., Vujanovic, V. & St-Arnaud, M. (2005) A PCR-denaturating gradient gel electrophoresis approach to assess Fusarium diversity in asparagus. Journal of Microbiological Methods, 60, 143-154.
67. Zhao, X.R., Lin, Q. & Brookes, P.C. (2005) Does soil ergosterol concentration provide a reliable estimate of soil fungal biomass? Soil Biology & Biochemistry, 37, 311-317.