Abstract
Background and aims
Specific associations exist between plant species and the soil microbial community and these associations vary between habitat types and different plant groups. However, there is evidence that the associations are highly specific. Hence, we aimed to determine the specificity of plant-microbe relationships amongst co-occurring grass species in a temperate grassland.
Methods and results
We examined the broad microbial groups of bacteria and fungi as well as a specific fungal group, the arbuscular mycorrhizal community amongst two dominant C3 and C4 species and one sub-dominant C3 species using terminal restriction fragment length polymorphism (T-RFLP) analysis. We found that the two dominant species were more similar to each other in their bacterial and arbuscular mycorrhizal community composition than either was to the sub-dominant species, but not in their fungal community composition. We also found no clear evidence that those differences were directly linked to soil chemical properties.
Conclusions
Our results demonstrate that co-occurring grass species have a distinct soil microbial community and T-RFLP analysis is able to detect plant species effect on the microbial community composition on an extremely local scale, providing an insight into the differences in the response of bacterial, fungal and arbuscular mycorrhizal communities to different, but similar and co-occurring, plant species.
Similar content being viewed by others
References
Anderson MJ (2004) PERMDISP: a FORTRAN computer program for permutatinoal analysis of multivariate dispersions (for any two-factor ANOVA design) using permutation tests. University of Auckland, New Zealand
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525
Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ (1999) Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol 13:650–660
Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8:217–230
Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P and Kauserud H (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol. 10
Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473
Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, Mortimer SR, Van der Putten WH (2006) 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
Bremer C, Braker G, Matthies D, Reuter A, Engels C, Conrad R (2007) Impact of plant functional group, plant species, and sampling time on the composition of nirK-Type denitrifier communities in soil. Appl Environ Microbiol 73:6876–6884
Carson JK, Gleeson DB, Clipson N, Murphy DV (2010) Afforestation alters community structure of soil fungi. Fungal Biol 114:580–584
Chapman SK, Langley JA, Hart SC, Koch GW (2006) Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol 169:27–34
Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205–219
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, Plymouth
Cookson WR, Osman M, Marschner P, Abaye DA, Clark I, Murphy DV, Stockdale EA, Watson CA (2007) Controls on soil nitrogen cycling and microbial community composition across land use and incubation temperature. Soil Biol Biochem 39:744–756
Costa R, Gotz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56:236–249
Day RW, Quinn GP (1989) Comparisons of treatments after an analysis of variance in ecology. Ecol Monogr 59:433–463
del Alguacil MM, Lozano Z, Campoy M, Roldán A (2010) Phosphorus fertilisation management modifies the biodiversity of AM fungi in a tropical savanna forage system. Soil Biol Biochem 42:1114–1122
Dukes JS, Field CB (2000) Diverse mechanisms for CO2 effects on grassland litter decomposition. Glob Chang Biol 6:145–154
Edel-Hermann V, Gautheron N, Alabouvette C, Steinberg C (2008) Fingerprinting methods to approach multitrophic interactions among microflora and microfauna communities in soil. Biol Fertil Soils 44:975–984
Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631
Gotzenberger L, de Bello F, Brathen KA, Davison J, Dubuis A, Guisan A, Leps J, Lindborg R, Moora M, Partel M, Pellissier L, Pottier J, Vittoz P, Zobel K, Zobel M (2012) Ecological assembly rules in plant communities-approaches, patterns and prospects. Biol Rev 87:111–127
Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378
Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD (2001) Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33:533–551
Haichar FE, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230
Harte J, Shaw R (1995) Shifting dominance within a montane vegetation community: results of a climate-warming experiment. Science 267:876–880
Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257
Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80:1187–1195
Hauben L, Vauterin L, Swings J, Moore ERB (1997) Comparison of 16S ribosomal DNA sequences of all Xanthomonas species. Int J Syst Bacteriol 47:328–335
Hausmann NT, Hawkes CV (2009) Plant neighborhood control of arbuscular mycorrhizal community composition. New Phytol 183:1188–1200
Hedlund K (2002) Soil microbial community structure in relation to vegetation management on former agricultural land. Soil Biol Biochem 34:1299–1307
Hossain MZ, Sugiyama S (2011) Influences of plant litter diversity on decomposition, nutrient mineralization and soil microbial community structure. Grassl Sci 57:72–80
Hovenden MJ, Miglietta F, Zaldei A, Vander Schoor JK, Wills KE, Newton PCD (2006) The TasFACE climate-change impacts experiment: design and performance of combined elevated CO2 and temperature enhancement in a native Tasmanian grassland. Aust J Bot 54:1–10
Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33
Kardol P, Cregger MA, Campany CE, Classen AT (2010) Soil ecosystem functioning under climate change: plant species and community effects. Ecology 91:767–781
Khidir HH, Eudy DM, Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL (2010) A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. J Arid Environ 74:35–42
Kourtev PS, Ehrenfeld JG, Haggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166
Kuske CR, Ticknor LO, Miller ME, Dunbar JM, Davis JA, Barns SM, Belnap J (2002) Comparison of soil bacterial communities in rhizospheres of three plant species and the interspaces in an arid grassland. Appl Environ Microbiol 68:1854–1863
Larkin RP (2003) Characterization of soil microbial communities under different potato cropping systems by microbial population dynamics, substrate utilization, and fatty acid profiles. Soil Biol Biochem 35:1451–1466
Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349
Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799
Marsh TL (2005) Culture-independent microbial community analysis with terminal restriction fragment length polymorphism. In Environ. Microbiol. pp 308–329. Elsevier Academic Press Inc, San Diego
Martinez-Garcia LB, Pugnaire FI (2011) Arbuscular mycorrhizal fungi host preference and site effects in two plant species in a semiarid environment. Appl Soil Ecol 48:313–317
Meidute S, Demoling F, Baath E (2008) Antagonistic and synergistic effects of fungal and bacterial growth in soil after adding different carbon and nitrogen sources. Soil Biol Biochem 40:2334–2343
Mitchell RJ, Hester AJ, Campbell CD, Chapman SJ, Cameron CM, Hewison RL, Potts JM (2012) Explaining the variation in the soil microbial community: do vegetation composition and soil chemistry explain the same or different parts of the microbial variation? Plant Soil 351:355–362
Moora M, Zobel M (1996) Effect of arbuscular mycorrhiza on inter- and intraspecific competition of two grassland species. Oecologia 108:79–84
Nunan N, Daniell TJ, Singh BK, Papert A, McNicol JW, Prosser JI (2005) Links between plant and rhizoplane bacterial communities in grassland soils, characterized using molecular techniques. Appl Environ Microbiol 71:6784–6792
Okubo A, Sugiyama S (2009) Comparison of molecular fingerprinting methods for analysis of soil microbial community structure. Ecol Res 24:1399–1405
Opik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790
Osanai Y, Flittner A, Janes JK, Theobald P, Pendall E, Newton PCD, Hovenden MJ (2012) Decomposition and nitrogen transformation rates in a temperate grassland vary among co-occurring plant species. Plant Soil 350:365–378
Osborne CA, Zwart AB, Broadhurst LM, Young AG, Richardson AE (2011) The influence of sampling strategies and spatial variation on the detected soil bacterial communities under three different land-use types. FEMS Microbiol Ecol 78:70–79
Paterson E (2003) Importance of rhizodeposition in the coupling of plant and microbial productivity. Eur J Soil Sci 54:741–750
Patra AK, Abbadie L, Clays-Josserand A, Degrange V, Grayston SJ, Guillaumaud N, Loiseau P, Louault F, Mahmood S, Nazaret S, Philippot L, Poly F, Prosser JI, Le Roux X (2006) Effects of management regime and plant species on the enzyme activity and genetic structure of N-fixing, denitrifying and nitrifying bacterial communities in grassland soils. Environ Microbiol 8:1005–1016
Rees GN, Baldwin DS, Watson GO, Perryman S, Nielsen DL (2004) Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Antonie Van Leeuwenhoek 86:339–347
Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291
Robinson CH, Szaro TM, Izzo AD, Anderson IC, Parkin PI, Bruns TD (2009) Spatial distribution of fungal communities in a coastal grassland soil. Soil Biol Biochem 41:414–416
Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562
Sagova-Mareckova M, Omelka M, Cermak L, Kamenik Z, Olsovska J, Hackl E, Kopecky J, Hadacek F (2011) Microbial communities show parallels at sites with distinct litter and soil characteristics. Appl Environ Microbiol 77:7560–7567
Sanon A, Andrianjaka ZN, Prin Y, Bally R, Thioulouse J, Comte G, Duponnois R (2009) Rhizosphere microbiota interfers with plant-plant interactions. Plant Soil 321:259–278
SAS Institute Inc (2003) SAS/STAT user’s guide, version 9.1. SAS Publishing, Cary
Shaver GR, Canadell J, Chapin FS, Gurevitch J, Harte J, Henry G, Ineson P, Jonasson S, Melillo J, Pitelka L, Rustad L (2000) Global warming and terrestrial ecosystems: a conceptual framework for analysis. Bioscience 50:871–882
Shaw MR, Harte J (2001) Control of litter decomposition in a subalpine meadow-sagebrush steppe ecotone under climate change. Ecol Appl 11:1206–1223
Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751
Söderberg KH, Probanza A, Jumpponen A, Bååth E (2004) The microbial community in the rhizosphere determined by community-level physiological profiles (CLPP) and direct soil- and cfu-PLFA techniques. Appl Soil Ecol 25:135–145
van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck JM, Fitter AH, Young JPW (2002) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11:1555–1564
Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095
Veresoglou SD, Mamolos AP, Thornton B, Voulgari OK, Sen R, Veresoglou DS (2011) Medium-term fertilization of grassland plant communities masks plant species-linked effects on soil microbial community structure. Plant Soil 344:187–196
Wagg C, Jansa J, Stadler M, Schmid B, van der Heijden MGA (2011) Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92:1303–1313
White TJ, Bruns T, Lee S, Taylor J (1990) Amplication and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: A Guide to Methods and Applications. Academic, San Diego, pp 315–322
Williamson WM, Wardle DA, Yeates GW (2005) Changes in soil microbial and nematode communities during ecosystem decline across a long-term chronosequence. Soil Biol Biochem 37:1289–1301
Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487
Zechmeister-Boltenstern S, Michel K, Pfeffer M (2011) Soil microbial community structure in European forests in relation to forest type and atmospheric nitrogen deposition. Plant Soil 343:37–50
Acknowledgment
Dr Mandeep Kaur provided useful feedback on a draft of this manuscript. We thank the Australian Federal Department of Defence for access to the Pontville Small Arms Range Complex. This research was supported by the Australian Research Council Discovery Projects scheme.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Stefano Manzoni.
Rights and permissions
About this article
Cite this article
Osanai, Y., Bougoure, D.S., Hayden, H.L. et al. Co-occurring grass species differ in their associated microbial community composition in a temperate native grassland. Plant Soil 368, 419–431 (2013). https://doi.org/10.1007/s11104-012-1529-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-012-1529-4