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Microbe-mediated plant–soil feedback and its roles in a changing world

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Ecological Research

Abstract

Plants affect soil conditions, which in turn alter plant growth and interspecific competition, forming plant–soil feedback (PSF) systems. PSF is a good example of bidirectional interactions between biomes and the non-living environments, acting as a major driving force of community structure and ecosystem function. Among the major types of PSF mediated by various soil components, there are many holes in our knowledge of the interactions between PSF mediated by plant species-specific litter and PSF mediated by soil microbes. Here I discuss the role of the functional diversity of microbial decomposers in litter-mediated PSF and also propose new hypotheses on the role of microbial diversity in PSF mediated by pathogenic and mutualistic soil microbes. I also review how PSF interacts with human-induced environmental change, i.e., direct drivers of change in the ecosystem (e.g. climate change and the invasion of alien species). Many authors have suggested that the impact of alien plant species on ecosystems is mediated by PSF, which also interacts with other direct drivers, such as climate change. Using a simple model of litter-mediated PSF with microbial decomposers, I confirm that the interactions between PSF and other direct drivers affect the invasion process of alien species. The model also demonstrates that the functional diversity of microbial decomposers accelerates or decelerates the speed of the invasion depending on the environmental change scenarios. Further theoretical and empirical studies are needed to derive general predictions on how exogenous environmental change induced by human activities alters communities and ecosystems through disturbance or modification of endogenous community–ecosystem interactions, such as the functioning of PSF.

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References

  • Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–449

    Article  Google Scholar 

  • Aerts R, de Caluwe H (1997) Nutritional and plant-mediated controls on leaf litter decomposition of Carex species. Ecology 78:244–260

    Google Scholar 

  • Aerts R, de Caluwe H, Beltman B (2003) Plant community mediated vs. nutritional control on litter decomposition rates in grasslands. Ecology 84:3198–3208

    Article  Google Scholar 

  • Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawaii. Oecologia 141:612–619

    Article  PubMed  Google Scholar 

  • Ashton IW, Miller AE, Bowman WD, Suding KN (2008) Nitrogen preferences and plant–soil feedbacks as influenced by neighbors in the alpine tundra. Oecologia 156:625–636

    Article  PubMed  CAS  Google Scholar 

  • Ayres E, Steltzer H, Simmons BL, Simpson RT, Steinweg JM, Wallenstein MD, Mellor N, Parton WJ, Moore JC, Wall DH (2009) Home-field advantage accelerates leaf litter decomposition in forest. Soil Biol Biochem 41:606–610

    Article  CAS  Google Scholar 

  • Bardgett RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass, and ecosystem functions in temperate grasslands. Soil Biol Biochem 31:317–321

    Article  CAS  Google Scholar 

  • Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2:805–814

    Article  PubMed  CAS  Google Scholar 

  • Bartelt-Ryser J, Joshi J, Schmid B, Brandl H, Balser T (2005) Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspect Plant Ecol Evol Syst 7:27–49

    Article  Google Scholar 

  • Beckstead J, Parker IM (2003) Invasiveness of Ammophila arenaria: release from soil-borne pathogens? Ecology 84:2824–2831

    Article  Google Scholar 

  • Berendse F (1994) Litter decomposability—a neglected component of plant fitness. J Ecol 82:187–190

    Article  Google Scholar 

  • Berendse F, Scheffer M (2009) The angiosperm radiation revisited, an ecological explanation for Darwin’s ‘abominable mystery’. Ecol Lett 12:865–872

    Article  PubMed  Google Scholar 

  • Bever JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977

    Article  Google Scholar 

  • Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc Lond B 269:2595–2601

    Article  Google Scholar 

  • Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473

    Article  Google Scholar 

  • Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the unity of the feedback approach. J Ecol 85:561–573

    Article  Google 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

    Article  CAS  Google Scholar 

  • Binkley D, Giardina C (1998) Why do tree species affect soils? The warp and woof of tree-soil interactions. Biogeochemistry 42:89–106

    Article  Google Scholar 

  • Bragazza L, Freeman C, Jones T, Rydin H, Limpens J, Fenner N, Ellis T, Gerdol R, Hájek M, Hájek T, Iacumin P, Kutnar L, Tahvanainen T, Toberman H (2006) Atmospheric nitrogen deposition promotes carbon loss from peat bogs. Proc Natl Acad Sci USA 103:19386–19389

    Article  PubMed  CAS  Google Scholar 

  • Buckeridge KM, Zufelt E, Chu H, Grogan P (2010) Soil nitrogen cycling rates in low arctic shrub tundra are enhanced by litter feedbacks. Plant Soil 330:407–421

    Article  CAS  Google Scholar 

  • Carvalho LM, Antunes PM, Martins-Loução MA, Klironomos JN (2010) Disturbance influences the outcome of plant–soil biota interactions in the invasive Acacia longifolia and in native species. Oikos 119:1172–1180

    Article  Google Scholar 

  • Chapin FS III (2003) Effects of plant traits on ecosystem and regional processes: a conceptual framework for predicting the consequences of global change. Ann Bot 91:455–463

    Article  PubMed  Google Scholar 

  • Chapman SK, Feller IC (2011) Away-field advantage: mangrove seedlings grow best in litter from other mangrove species. Oikos. 120:1880–1888

    Article  Google Scholar 

  • Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366

    Article  Google Scholar 

  • Clark BR, Hartley SE, Suding KN, de Mazancourt C (2005) The effect of recycling on plant competitive hierarchies. Am Nat 165:609–622

    Article  PubMed  Google Scholar 

  • Comita LS, Muller-Landau HC, Aguilar S, Hubbell SP (2010) Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329:330–332

    Article  PubMed  CAS  Google Scholar 

  • Daufresne T, Hedin LO (2005) Plant coexistence depends on ecosystem nutrient cycles: extension of the resource-ratio theory. Proc Natl Acad Sci USA 102:9212–9217

    Article  PubMed  CAS  Google Scholar 

  • De Deyn GB, Cornelissen HC, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett 11:516–531

    Article  PubMed  Google Scholar 

  • Diez JM, Dickie I, Edwards G, Hulme PE, Sullivan JJ, Duncan RP (2010) Negative soil feedbacks accumulate over time for non-native plant species. Ecol Lett 13:803–809

    Article  PubMed  Google Scholar 

  • Dornbush ME (2007) Grasses, litter, and their interaction affect microbial biomass and soil enzyme activity. Soil Biol Biochem 39:2241–2249

    Article  CAS  Google Scholar 

  • Ehrenfeld JG, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300

    Article  Google Scholar 

  • Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedbacks in the plant–soil system. Annu Rev Environ Resour 30:75–115

    Article  Google Scholar 

  • Eppinga MB, Rietkerk M, Dekker SC, De Ruiter PC, van der Putten WH (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114:168–176

    Article  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631

    Article  PubMed  CAS  Google Scholar 

  • Funk JL (2005) Hedychium gardnerianum invasion into Hawaiian montane rainforest: interactions among litter quality, decomposition rate, and soil nitrogen availability. Biogeochemistry 76:441–451

    Article  Google Scholar 

  • Gao Q, Peng S, Zhao P, Zeng X, Cai X, Yu M, Shen W, Yinghui Liu (2003) Explanation of vegetation succession in subtropical southern China based on ecophysiological characteristics of plant species. Tree Physiol 23:641–648

    Article  PubMed  Google Scholar 

  • Geritz SAH, Kisdi E, Meszéna G, Metz JAJ (1998) Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol Ecol 12:35–57

    Article  Google Scholar 

  • Gholz HL, Wedin DA, Smitherman SM, Harmon ME, Parton WJ (2000) Long-term dynamics of pine and hardwood litter in contrasting environments: toward a global model of decomposition. Glob Change Biol 6:751–765

    Article  Google Scholar 

  • Haeckel E (1866) Generelle morphologie der organismen. Allgemeine grundzüge der organischen formen-wissenschaft, mechanisch begründet durch die von Charles Darwin reformirte descendenz-theorie. G. Reimer, Berlin

  • Harrison KA, Bardgett RD (2010) Influence of plant species and soil conditions on plant–soil feedback in mixed grassland communities. J Ecol 98:384–395

    Article  Google Scholar 

  • Hooper DU, Solan M, Symstad A, Díaz S, Gessner MO, Buchmann N, Degrange V, Grime P, Hulot F, Mermillod-Bondin H, Roy J, Spehn E, van Peer L (2002) Species diversity, functional diversity, and ecosystem functioning. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning. Oxford University Press, Oxford

    Google Scholar 

  • Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  • Inderjit, van der Putten WH (2010) Impact of soil microbial communities on exotic plant invasion. Trends Ecol Evol 25:512–519

  • Jiang L, Han X, Zhang G, Kardol P (2010) The role of plant–soil feedbacks and land-use legacies in restoration of a temperate steppe in northern China. Ecol Res 25:1101–1111

    Article  Google Scholar 

  • Kardol P, Bezemer TM, van der Putten WH (2006) Temporal variation in plant–soil feedback controls succession. Ecol Lett 9:1080–1088

    Article  PubMed  Google Scholar 

  • Kardol P, Cornips NJ, van Kempen MML, Bakx-Schotman JMT, van der Putten WH (2007) Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Eco Monogr 77:147–162

    Article  Google Scholar 

  • Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70

    Article  PubMed  CAS  Google Scholar 

  • Knops JMH, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466

    Article  Google Scholar 

  • Kulmatiski A, Kardol P (2008) Getting plant–soil feedbacks out of the greenhouse: experimental and conceptual approaches. Prog Bot 69:449–472

    Article  Google Scholar 

  • Kulmatiski A, Beard KH, Stark JM (2006) Soil history as a primary control on plant invasion in abandoned agricultural fields. J Appl Ecol 43:868–876

    Article  Google Scholar 

  • Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant–soil feedbacks: a meta-analytical review. Ecol Lett 2008:980–992

    Article  Google Scholar 

  • Kulmatiski A, Heavilin J, Beard KH (2011) Testing predictions of a three-species plant–soil feedback model. J Ecol 99:542–550

    Google Scholar 

  • Lang SI, Cornelissen JHC, Klahn T, van Logtestijn RSP, Broekman R, Schweikert W, Aerts R (2009) An experimental comparison of chemical traits and litter decomposition rates in a diverse range of subarctic bryophyte, lichen and vascular plant species. J Ecol 97:886–900

    Article  CAS  Google Scholar 

  • Lovelock JE (1972) Gaia as seen through the atmosphere. Atmos Environ 6:579–580

    Article  Google Scholar 

  • Lovelock JE, Margulis L (1974) Atmospheric homeostasis by and for the biosphere: the Gaia hypothesis. Tellus 26:2–10

    Article  CAS  Google Scholar 

  • Mallik AU (2003) Conifer regeneration problems in boreal and temperate forests with ericaceous understory: role of disturbance, seedbed limitation, and keystone species change. Crit Rev Plant Sci 22:341–366

    Article  Google Scholar 

  • Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–756

    Article  PubMed  CAS  Google Scholar 

  • Manning P, Morrison SA, Bonkowski M, Bardgett RD (2008) Nitrogen enrichment modifies plant community structure via changes to plant–soil feedback. Oecologia 157:661–673

    Article  PubMed  CAS  Google Scholar 

  • Miki T, Kondoh M (2002) Feedbacks between nutrient cycling and vegetation predict plant species coexistence and invasion. Ecol Lett 5:624–633

    Article  Google Scholar 

  • Miki T, Ushio M, Fukui S, Kondoh M (2010) Functional diversity of microbial decomposers facilitates plant coexistence in a plant–microbe–soil feedback model. Prod Nat Acad Sci USA 107:14251–14256

    Article  CAS  Google Scholar 

  • Milcu A, Manning P (2011) All size classes of soil fauna and litter quality control the acceleration of litter decay in its home environment. Oikos 120:1366–1370

    Article  Google Scholar 

  • Millennium Ecosystem Assessment (MA) (2005) Ecosystem and human well-bing: synthesis. Island Press, Washington, DC

    Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    Article  PubMed  CAS  Google Scholar 

  • Morimoto Y (2011) What is Satoyama? Points for discussion on its future direction. Landsc Ecol Eng 7:163–171

    Article  Google Scholar 

  • Nelson GC (2005) Drivers of ecosystem change (summary chapter). In: Millennium Ecosystem Assessment: ecosystems and human well-being: current state and trends. Island Press, Washington, DC

  • Orwin KH, Buckland SM, Johnson D, Turner BL, Smart S, Oakley S, Bardgett RD (2010) Linkage of plant traits to soil properties and the functioning of temperate grassland. J Ecol 98:1074–1083

    Article  Google Scholar 

  • Reinhart KO, Packer A, van der Putten WH, Clay K (2003) Plant–soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol Lett 6:1046–1050

    Article  Google Scholar 

  • Shah MA, Reshi Z, Rashid I (2008) Mycorrhizal source and neighbour identity differently influence Anthemis cotula L. invasion in the Kashmir Himalaya, India. Appl Soil Ecol 40:330–337

    Article  Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451

    Article  PubMed  Google Scholar 

  • Strum M, McFadden JP, Lison GE, Chapin FS III, Racine CH, Holmgren J (2001) Snow–shrub interactions in Arctic tundra: a hypothesis with climatic implications. J Clim 14:336–344

    Article  Google Scholar 

  • Strum M, Chimel J, Michaelson G, Welker JM, Oberbauer SF, Liston GE, Fahnestock J, Romanovsky VE (2005) Winter biological processes could help convert Arctic tundra to shrubland. Bioscience 55:17–26

    Article  Google Scholar 

  • Suding KN, Ashton IW, Bechtold H, Bowman WD, Mobley ML, Winkleman R (2008) Plant and microbe contribution to community resilience in a directionally changing environment. Ecol Monogr 78:313–329

    Article  Google Scholar 

  • Tansley AG (1935) The use and abuse of vegetational concepts and terms. Ecology 16:284–307

    Article  Google Scholar 

  • te Beest M, Stevens N, Olff H, van der Putten WH (2009) Plant–soil feedback induces shits in biomass allocation in the invasive plant Chromolaena odorata. J Ecol 97:1281–1290

    Article  Google Scholar 

  • Teuben M (1991) Nutrient availability and interactions between soil arthropods and microorganisms during decomposition of coniferous litter: a mesocosm study. Biol Fertil Soils 10:256–266

    Article  CAS  Google Scholar 

  • Tilman D (1980) A graphical-mechanistic approach to competition and predation. Am Nat 116:362–393

    Article  Google Scholar 

  • United Nations (1992) Convention on biological diversity. Article 2. Use of terms. Available at: http://www.cbd.int/doc/legal/cbd-en.pdf

  • Ushio M, Wagai R, Balser TC, Kitayama K (2008) Variations in the soil microbial community composition of a tropical montane forest ecosystem: does tree species matter? Soil Biol Biochem 40:2699–2702

    Article  CAS  Google Scholar 

  • van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • van der Putten WH, Peters BA (1997) How soil-borne pathogens may affect plant competition. Ecology 78:1785–1795

    Article  Google Scholar 

  • van der Putten WH, van Dijk C, Peters BAM (1993) Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–56

    Article  Google Scholar 

  • van Grunsven RHA, van der Putten WH, Bezemer TM, Tamis WLM, Berendse F, Veenendaal EM (2007) Reduced plant–soil feedback of plant species expanding their range as compared to natives. J Ecol 95:1050–1057

    Article  Google Scholar 

  • van Grunsven RHA, van der Putten WH, Bezemer TM, Berendse F, Veenendaal EM (2010) Plant–soil interactions in the expansion and native range of a poleward shifting plant species. Glob Change Biol 16:380–385

    Article  Google Scholar 

  • Vinton MA, Goergen EM (2006) Plant–soil feedbacks contribute to the persistence of Bromus inermis in tallgrass prairie. Ecosystems 9:967–976

    Article  CAS  Google Scholar 

  • Vitousek P (2006) Ecosystem science and human-environment interactions in the Hawaiian archipelago. J Ecol 94:510–521

    Article  Google Scholar 

  • Wardle DA (2002) Community and ecosystems: linking the aboveground and belowground components. Princeton University Press, Princeton

    Google Scholar 

  • Wardle DA, Bonner KI, Barker GM, Yeates GW, Nicholson KS, Bardgett RD, Watson RN, Ghani A (1999) Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecol Monogr 69:535–568

    Article  Google Scholar 

  • Watson AJ, Lovelock JE (1983) Biological homeostasis of the global environment: the parable of Daisyworld. Tellus 35B:284–289

    Article  Google Scholar 

  • Yelenik SG, Levine JM (2010) Native shrub reestablishment in exotic annual grasslands: do ecosystem processes recover? Ecol Appl 20:716–727

    Article  PubMed  CAS  Google Scholar 

  • Yelenik SG, Stock WD, Richardson DM (2004) Ecosystem level impacts of invasive Acacia saligna in the South African Fynbos. Restor Ecol 12:44–51

    Article  Google Scholar 

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Acknowledgments

The anonymous reviewers are thanked for their valuable suggestions on the earlier versions of the manuscript. This work was supported by National Taiwan University (97R0034-29) and National Science Council (NSC 97-2611-M-002-011-MY3), Taiwan.

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  1. Institute of Oceanography, National Taiwan University, No. 1, Sec. 4, Roosevelt Road, Taipei, 10617, Taiwan

    Takeshi Miki

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Correspondence to Takeshi Miki.

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Takeshi Miki is the recipient of the 15th Denzaburo Miyadi Award.

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Miki, T. Microbe-mediated plant–soil feedback and its roles in a changing world. Ecol Res 27, 509–520 (2012). https://doi.org/10.1007/s11284-012-0937-5

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