Interactions between soil properties, soil microbes and plants in remnant-grassland and old-field areas: a reciprocal transplant approach
Background and aims
The importance of plant-soil feedback is becoming widely acknowledged; however, how different soil conditions influence these interactions is still relatively unknown. Using soil from a degraded old-field and a remnant grassland, we aimed to explore home-field advantages in plant-soil feedbacks and plant responses to the abiotic and biotic soil conditions. We quantified the soil bacterial and fungal community from these sites and their responses to soil conditions and plant species.
Sterilized old-field and remnant-grassland soil was inoculated with home or away soil in a reciprocal transplant experiment using a native grass, Rytidosperma auriculatum, and an invasive grass, Avena barbata, as test species. The soil fungal and bacterial communities were characterised using high throughput sequencing.
Plants had a greater growth response to microbes when an inoculant was added to its home soil. However, this relationship is complex, with microbial communities changing in response to the plant species and soil type.
The apparent home-field advantage of the soil microbes shown in this study may restrict the utility of inoculants as a management tool. However, since we inoculated sterile soil, future work should focus on understanding how the inoculated microbial community interacts and competes with resident communities.
KeywordsBacterial community eDNA Fungal community Invasive annual grass Native perennial grass Old-fields Remnant grasslands Home-field advantage
We thank Olivia Cousins for providing an internal review, and two anonymous reviewers for advice and helpful comments on a previous version of the manuscript and Dr. Matthew Christmas and Rebecca Stoner for advice and help setting up the experiment. This project was funded by Nature Foundation of South Australia Incorporated, Australian Flora Foundation Incorporated and the Holsworth Wildlife Research Endowment.
- Bálint M, Bahram M, Eren AM, Faust K, Fuhrman JA, Lindahl B, O'Hara RB, Öpik M, Sogin ML, Unterseher M, Tedersoo L (2016) Millions of reads, thousands of taxa: microbial community structure and associations analyzed via marker genes. FEMS Microbiol Rev 40:686–700. https://doi.org/10.1093/femsre/fuw017 CrossRefPubMedGoogle Scholar
- Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1Google Scholar
- Bever JD, Platt TG, Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265–283. https://doi.org/10.1146/annurev-micro-092611-150107 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1111/j.1365-2745.2006.01158.x CrossRefGoogle Scholar
- Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403. https://doi.org/10.1016/j.chom.2015.01.011 CrossRefPubMedPubMedCentralGoogle Scholar
- Bureau of Meteorology (2017) Climate data: Roseworthy, viewed on 25th November 2017, <http://www.bom.gov.au/climate/data/>
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
- Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x CrossRefGoogle Scholar
- Graham JH, Leonard RT, Menge JA (1982) Interaction of light-intensity and soil-temperature with phosphorus inhibition of vesicular arbuscular. New Phytol 91:683–690. https://doi.org/10.1111/j.1469-8137.1982.tb03347.x CrossRefGoogle Scholar
- Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x CrossRefGoogle Scholar
- Koide RT, Li MG (1990) On host regulation of the vesicular arbuscular mycorrhizal symbiosis. New Phytol 114:59–64. https://doi.org/10.1111/j.1469-8137.1990.tb00373.x CrossRefGoogle Scholar
- Kõljalg U, Larsson K-H, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Vrålstad T (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068. https://doi.org/10.1111/j.1469-8137.2005.01376.x CrossRefPubMedGoogle Scholar
- Kulmatiski A, Kardol P (2008) Getting plant—soil feedbacks out of the greenhouse: experimental and conceptual approaches. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in botany. Springer, Berlin HeidelbergGoogle Scholar
- Lambert DH, Cole H, Baker DE (1980) Adaptation of vesicular-arbuscular mycorrhizae to edaphic factors. New Phytol 85:513–520. https://doi.org/10.1111/j.1469-8137.1980.tb00766.x CrossRefGoogle Scholar
- Leff JW, Jones SE, Prober SM, Barberan A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JMH, McCulley RL, La Pierre K, Risch AC, Seabloom EW, Schutz M, Steenbock C, Stevens CJ, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci U S A 112:10967–10972. https://doi.org/10.1073/pnas.1508382112 CrossRefPubMedPubMedCentralGoogle Scholar
- Neuenkamp L, Prober SM, Price JN, Zobel M, Standish RJ (2018) Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type, restoration context and time. Fungal Ecol. https://doi.org/10.1016/j.funeco.2018.05.004
- Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4–3, https://cran.r-project.org/package=vegan
- R Core Team (2017) R: a language and environment for statistical computing. In: R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
- Rosser L (2013) Ecological restoration plan for Para woodlands reserve. Department of Environment, Water and Natural Resources, South Australian Government, Adelaide, AustraliaGoogle Scholar
- Rua MA, Antoninka A, Antunes PM, Chaudhary VB, Gehring C, Lamit LJ, Piculell BJ, Bever JD, Zabinski C, Meadow JF, Lajeunesse MJ, Milligan BG, Karst J, Hoeksema JD (2016) Home-field advantage? Evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:15. https://doi.org/10.1186/s12862-016-0698-9 CrossRefGoogle Scholar
- Smith ME (2018) Interactions between native and exotic plants in the context of grassland restoration and the importance of below-ground processes. University of Adelaide. Faculty of Science. Biological SciencesGoogle Scholar
- Smith FA, Smith SE (1981) Mycorrhizal infection and growth of Trifolium subterraneum: use of sterilized soil as a control treatment. New Phytol 88:299–309. https://doi.org/10.1111/j.1469-8137.1981.tb01726.x CrossRefGoogle Scholar
- Son CL, Smith SE (1988) Mycorrhizal growth-responses - interactions between photon irradiance and phosphorus-nutrition. New Phytol 108:305–314. https://doi.org/10.1111/j.1469-8137.1988.tb04167.x CrossRefGoogle Scholar
- Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727–731. https://doi.org/10.1371/journal.pbio.0040140 CrossRefGoogle Scholar
- Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University PressGoogle Scholar
- van der Heijden MGA, Bakker R, Verwaal J, Scheublin TR, Rutten M, van Logtestijn R, Staehelin C (2006) Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiol Ecol 56:178–187. https://doi.org/10.1111/j.1574-6941.2006.0086.x CrossRefPubMedGoogle Scholar
- Warcup J (1957) Chemical and biological aspects of soil sterilization. Soils Fert 20:1–5Google Scholar
- Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University PressGoogle Scholar
- Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vázquez-Baeza Y, Birmingham A, Hyde ER, Knight R (2017) Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5:27. https://doi.org/10.1186/s40168-017-0237-y CrossRefPubMedPubMedCentralGoogle Scholar
- Wong MR (2013) Above-and below-ground linkages of semi-arid perennial tussock grasslands. Monash University. Faculty of Science. Biological SciencesGoogle Scholar