Soil bacteria and fungi respond on different spatial scales to invasion by the legume Lespedeza cuneata

Frontiers in Microbiology

Volumn 2, Issue JUNE, 2011, Pages

  Yannarell, Anthony C ^a   Busby, Ryan R ^b   Denight, Michael L ^b   Gebhart, Dick L ^b   Taylor, Steven J ^c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b U S ARMY ENGINEER RESEARCH AND DEVELOPMENT CENTER   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Bacteria; Fungi; Invasive species; Lespedeza cuneata; Multivariate data analysis; Soil microbial community; Spatial scaling

Indexed keywords

EID: 84859432621     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00127     Document Type: Article

References (70)

1. Agrawal, A. A., Kotanen, P. M., Mitchell, C. E., Power, A. G., Godsoe, W., and Klironomos, J. (2005). Enemy release? An experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology 86, 2979-2989.
2. Allen, E. B., Allen, M. F., Helm, D. J., Trappe, J. M., Molina, R., and Rin-con, E. (1995). Patterns and regulation of mycorrhizal plant and fungal diversity. Plant Soil 170, 47-62.
3. Berg, G., and Smalla, K. (2009). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhi-zosphere. FEMS Microbiol. Ecol. 68, 1-13.
4. Bever, J. D. (1994). Feedback between plants and their soil communities in an old field community. Ecology 75, 1965-1977.
5. Bever, J. D. (2003). Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phy-tol. 157,465-473.
6. Bezemer, T. M., Harvey, J. A., Kowalchuk, G. A., Korpershoek, H., and van der Putten, W. H. (2006a). Interplay between Senecio jacobaea and plant, soil, and aboveground insect community composition. Ecology 87, 2002-2013.
7. Bezemer, T. M., Lawson, C. S., Hedlund, K., Edwards, A. R., Brook, A. J., Igual, J. M., Mortimer, S. R., and Van der Putten, W. H. (2006b). Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands. J. Ecol. 94, 893-904.
8. Borneman, J., and Triplett, E. W. (1997). Molecular microbial diversity in soils from Eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl. Environ. Microbiol. 63, 2647-2653.
9. Brandon, A. L., Gibson, D. J., and Mid-dleton, B. A. (2004). Mechanisms for dominance in an early successional old field by the invasive non-native Lespedeza cuneata (Dum. Cours.) G. Don. Biol. Invasions 6, 483-493.
10. Broz, A. K., Manter, D. K., and Vivanco, J. M. (2007). Soil fungal abundance and diversity: another victim of the invasive plant Centaurea maculosa. ISMEJ. 1,763-765.
11. Callaway, R. M., Cipollini, D., Barto, K., Thelen, G. C., Hallett, S. G., Prati, D., Stinson, K., and Klironomos, J. (2008). Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89, 1043-1055.
12. Callaway, R. M., Thelen, G. C., Barth, S., Ramsey, P. W., and Gannon, J. E. (2004). Soil fungi alter interactions between the invader Centaurea mac-ulosa and North American natives. Ecology 85, 1062-1071.
13. Cappuccino, N., and Arnason, J.T. (2006). Novel chemistry of invasive exotic plants. Biol. Lett. 2, 189-193.
14. Chapuis-Lardy, L., Vanderhoeven, S., Dassonville, N., Koutika, L. S., and Meerts, P. (2006). Effect of the exotic invasive plant Solidago gigantea on soil phosphorus status. Biol. Fertil. Soils 42, 481-489.
15. Culman, S. W., Gauch, H. G., Black-wood, C. B., and Thies, J. E. (2008). Analysis of T-RFLP data using analysis of variance and ordination methods: a comparative study. J. Microbiol. Methods 75, 55-63.
16. Ehrenfeld, J. G. (2003). Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6, 503-523.
17. Engelkes, T., Morrien, E., Verhoeven, K. J. F., Bezemer, T. M., Biere, A., Harvey, J. A., McIntyre, L. M., Tamis, W. L. M., and van der Putten, W. H. (2008). Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456, 946-948.
18. Fisher, M. M., and Triplett, E. W. (1999). Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl. Environ. Microbiol. 65, 4630-4636.
19. Fumanal, B., Plenchette, C., Chau-vel, B., and Bretagnolle, F. (2006). Which role can arbuscular myc-orrhizal fungi play in the facilitation of Ambrosia artemisiifolia L. invasion in France? Mycorrhiza 17, 25-35.
20. Griffiths, B. S., Ritz, K., Ebblewhite, N., and Dobson, G. (1999). Soil microbial community structure: effects of substrate loading rates. Soil Biol. Biochem. 31, 145-153.
21. Gu, C. T., Wang, E. T., Sui, X. H., Chen, WE,and Chen, W.X. (2007).Diversity and geographical distribution of rhizobia associated with Lespedeza spp. in temperate and subtropical regions of China. Arch. Microbiol. 188,355-365.
22. Guernsey, W J. (1970). Sericea Lespedeza: its Use and Management Washington, DC: U.S. Department of Agriculture.
23. Heneghan, L., Fatemi, F., Umek, L., Grady, K., Fagen, K., and Workman, M. (2006). The invasive shrub European buckthorn (Rhamnus cathar-tica, L.) alters soil properties in Midwestern US woodlands. Appl. Soil Ecol. 32, 142-148.
24. Kalburtji, K. L., and Mosjidis, J. A. (1992). Effects of Sericea lespedeza residues on warm-season grasses. J. Range Manag. 45, 441-444.
25. Kalburtji, K. L., and Mosjidis, J. A. (1993a). Effects of Sericea lespedeza residues on cool-season grasses. J. Range Manag. 46, 315-319.
26. Kalburtji, K. L., and Mosjidis, J. A. (1993b). Effects of Sericea lespedeza root exudates on some perennial grasses. J. Range Manag. 46, 312-315.
27. Kalburtji, K. L., Mosjidis, J. A., and Mamolos, A. P. (1999). Litter dynamics of low and high tannin Sericea lespedeza plants under field conditions. Plant Soil 208, 271-281.
28. Kalburtji, K. L., Mosjidis, J. A., and Mamolos, A. P. (2001). Allelo-pathic plants. 2. Lespedeza cuneata. Allelopathy I 8,41-49.
29. Kardol, P., Cornips, N. J., van Kem-pen, M. M. L., Bakx-Schotman, J. M. T., and van der Putten, W. H. (2007). Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol. Monogr. 77, 147-162.
30. Kardol, P., Cregger, M. A., Cam-pany, C. E., and Classen, A. T. (2010). Soil ecosystem functioning under climate change: plant species and community effects. Ecology 91, 767-781.
31. Kent, A. D., and Triplett, E. W. (2002). Microbial communities and their interactions in soil and rhizosphere ecosystems. Annu. Rev. Microbiol. 56, 211-236.
32. Klironomos, J. (2002). Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417, 67-70.
33. Klironomos, J. N. (2003). Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84, 2292-2301.
34. Kourtev, P. S., Ehrenfeld, J. G., and Haggblom, M. (2002). Exotic plant species alter the microbial community structure and function in the soil. Ecology 83, 3152-3166.
35. Kourtev, P. S., Ehrenfeld, J. G., and Haggblom,M. (2003). Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol. Biochem. 35, 895-905.
36. Kulmatiski, A., Heavilin, J., and Beard, K. H. (2011). Testing predictions of a three-species plant-soil feedback model. J. Ecol. 99, 542-550.
37. Langdale, G. W., and Giddens, J. E. (1967). Phytotoxic phenolic compounds in Sericea lespedeza residues. Agron. J.59,581-584.
38. Lankau, R. (2010). Soil microbial communities alter allelopathic competition between Alliaria petiolata and a native species. Biol. Invasions 12, 2059-2068.
39. Lankau, R. (2011). Resistance and recovery of soil microbial communities in the face of Alliaria petiolata invasions. New Phytol. 189, 536-548.
40. Legendre, P., and Gallagher, E. D. (2001). Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271-280.
41. Legendre, P., and Legendre, L. (1998). Numerical Ecology, 2nd English Edn. Amsterdam: Elsevier Science, BV.
42. Lorenzo, P., Rodriguez-Echeverria, S., Gonzalez, L., and Freitas, H. (2010). Effect of invasive Acacia dealbata Link on soil microorganisms as determined by PCR-DGGE. Appl. Soil Ecol. 44,245-251.
43. Lynd, J. Q., and Ansman, T. R. (1993). Symbiotic tripartite nitrogen fixation effectual in eroded soil restoration with 20 year-age Sericea lespedeza. J. Plant Nutr. 16, 149-164.
44. Mangan, S. A., Herre, E. A., and Bever, J. D. (2010a). Specificity between Neotropical tree seedlings and their fungal mutualists leads to plant-soil feedback. Ecology 91, 2594-2603.
45. Mangan, S. A., Schnitzer, S. A., Herre, E. A., Mack, K. M. L., Valencia, M. C., Sanchez, E. I., and Bever, J. D. (2010b). Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466, U752-U710.
46. McArdle, B. H., and Anderson, M. J. (2001). Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290-297.
47. Miki, T., Ushio, M., Fukui, S., and Kondoh, M. (2010). Functional diversity of microbial decomposers facilitates plant coexistence in a plant-microbe-soil feedback model. Proc. Natl. Acad. Sci. U.S.A. 107, 14251-14256.
48. Miller, J. H. (2003). Nonnative Invasive Plants in Southern Forests: a Field Guide for Identification and Control. Asheville, NC: US Forest Service, Southern Research Station.
49. Min, B. R., Pinchak, W. E., Merkel, R., Walker, S.,Tomita,G., and Anderson, R. C. (2008). Comparative antimicrobial activity of tannin extracts from perennial plants on mastitis pathogens. Sci.. Res. Essays 3, 66-73.
50. Oksannen, J., Kindt, R., Legendre, P., O'Hara, B., Simpson, G. L., Solymos, P., Stevens, H. H., and Wagner, H. (2009). Vegan: Community Ecology Package, Version 1.15-4. Available at: http://CRAN.R-project.org/package=vegan
51. Pringle, A., Bever, J. D., Gardes, M., Parrent, J. L., Rillig, M. C., and Klironomos, J. N. (2009). Mycorrhizal symbioses and plant invasions. Annu. Rev. Ecol. Evol. Syst. 40, 699-715.
52. R Development Core Team. (2005). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available at: http://www.R-project.org
53. Ranjard, L., Poly, F., Lata, J. C., Mougel, C., Thioulouse, J., and Nazaret, S. (2001). Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: biological and methodological variability. Appl. Environ. Microbiol. 67, 4479-4487.
54. Reinhart, K. O., and Callaway, R. M. (2004). Soil biota facilitate exotic Acer invasions in Europe and North America. Ecol. Appl. 14, 1737-1745.
55. Reinhart, K. O., and Callaway, R. M. (2006). Soil biota and invasive plants. New Phytol. 170, 445-457.
56. Reinhart, K. O., Packer, A., Van der Putten, W H., and Clay, K. (2003). Plant-soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol. Lett. 6, 1046-1050.
57. Richardson, D. M., Allsopp, N., D'Antonio, C. M., Milton, S. J., and Rejmanek, M. (2000). Plant invasions - the role of mutualisms. Biol. Rev. 75, 65-93.
58. Schutzenhofer, M. R., Valone, T. J., and Knight, T. M. (2009). Herbivory and population dynamics of invasive and native Lespedeza. Oecologia 161, 57-66.
59. Smith, S. E., and Read, D. J. (2002). Mycorrhizal Symbiosis, 2nd Edn. London: Academic Press.
60. Soil Survey Staff. (2009). Web Soil Survey. Natural Resources Conservation Service, U.S. Department of Agriculture. Available at: http://websoilsurvey.nrcs.usda.gov/
61. Stinson, K. A., Campbell, S. A., Powell, J. R., Wolfe, B. E., Callaway, R. M., Thelen, G. C., Hallett, S. G., Prati, D., and Klironomos, J. N. (2006). Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol. 4, 727-731. doi: 10.1371/jour-nal.pbio.0040140
62. van der Putten, W. H., Klironomos, J. N., and Wardle, D. A. (2007a). Microbial ecology of biological invasions. ISMEJ. 1,28-37.
63. van der Putten, W. H., Kowalchuk, G. A., Brinkman,E. P., Doodeman, G. T. A., van der Kaaij, R. M., Kamp, A. F. D., Menting, F. B. J., and Veenendaal, E. M. (2007b). Soil feedback of exotic savanna grass relates to pathogen absence and mycorrhizal selectivity. Ecology 88, 978-988.
64. Venables, W. N., and Ripley, B. D. (2002). Modern Applied Statistics with S. New York: Springer.
65. Vogelsang, K. M., and Bever, J. D. (2009). Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90, 399-407.
66. Wardle, D. A., Bardgett, R. D., Klironomos, J. N., Setala, H., van der Putten, W H., and Wall, D. H. (2004). Ecological linkages between aboveground and belowground biota. Science 304, 1629-1633.
67. Wolfe, B. E., and Klironomos, J. N. (2005). Breaking new ground: soil communities and exotic plant invasion. Bioscience 55, 477-487.
68. Wolfe, B. E., Rodgers, V. L., Stinson, K. A., and Pringle, A. (2008). The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. J. Ecol. 96, 777-783.
69. Woods, T. M., Hartnett, D. C., and Ferguson, C. J. (2009). High propag-ule production and reproductive fitness homeostasis contribute to the invasiveness of Lespedeza cuneata (Fabaceae). Biol Invasions 11, 1913-1927.
70. Zou, J. W., Rogers, W E., DeWalt, S. J., and Siemann, E. (2006). The effect of Chinese tallow tree (Sapium seb-iferum) ecotype on soil-plant system carbon and nitrogen processes. Oecologia 150,272-281.