1932

Abstract

Microorganisms drive several processes needed for robust plant growth and health. Harnessing microbial functions is thus key to productive and sustainable food production. Molecular methods have led to a greater understanding of the soil microbiome composition. However, translating species or gene composition into microbiome functionality remains a challenge. Community ecology concepts such as the biodiversity–ecosystem functioning framework may help predict the assembly and function of plant-associated soil microbiomes. Higher diversity can increase the number and resilience of plant-beneficial functions that can be coexpressed and unlock the expression of plant-beneficial traits that are hard to obtain from any species in isolation. We combine well-established community ecology concepts with molecular microbiology into a workable framework that may enable us to predict and enhance soil microbiome functionality to promote robust plant growth in a global change context.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-110617-062605
2019-11-02
2024-10-11
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/50/1/annurev-ecolsys-110617-062605.html?itemId=/content/journals/10.1146/annurev-ecolsys-110617-062605&mimeType=html&fmt=ahah

Literature Cited

  1. Achouak W, Conrod S, Cohen V, Heulin T 2004. Phenotypic variation of Pseudomonas brassicacearum as a plant root-colonization strategy. Mol. Plant-Microbe Interact. 17:872–79
    [Google Scholar]
  2. Agaras BC, Scandiani M, Luque A, Fernández L, Farina F et al. 2015. Quantification of the potential biocontrol and direct plant growth promotion abilities based on multiple biological traits distinguish different groups of Pseudomonas spp. isolates. Biol. Control 90:173–86
    [Google Scholar]
  3. Awasthi A, Singh M, Soni SK, Singh R, Kalra A 2014. Biodiversity acts as insurance of productivity of bacterial communities under abiotic perturbations. ISME J 8:2445–52
    [Google Scholar]
  4. Badri DV, Zolla G, Bakker MG, Manter DK, Vivanco JM 2013. Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. New Phytol 198:264–73
    [Google Scholar]
  5. Barea J-M, Pozo MJ, Azcón R, Azcón-Aguilar C 2005. Microbial co-operation in the rhizosphere. J. Exp. Bot. 56:1761–78
    [Google Scholar]
  6. Becker J, Eisenhauer N, Scheu S, Jousset A 2012. Increasing antagonistic interactions cause bacterial communities to collapse at high diversity. Ecol. Lett. 15:468–74
    [Google Scholar]
  7. Bell T, Lilley AK, Hector A, Schmid B, King L, Newman JA 2009. A linear model method for biodiversity–ecosystem functioning experiments. Am. Nat. 174:836–49
    [Google Scholar]
  8. Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK 2005. The contribution of species richness and composition to bacterial services. Nature 436:1157–60
    [Google Scholar]
  9. Bender SF, Wagg C, van der Heijden MGA 2016. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 31:440–52
    [Google Scholar]
  10. Berendsen RL, Pieterse CMJ, Bakker PAHM 2012. The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–86
    [Google Scholar]
  11. Berendsen RL, Vismans G, Yu K, Song Y, de Jonge R et al. 2018. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J 12:1496–507
    [Google Scholar]
  12. Boles BR, Thoendel M, Singh PK 2004. Self-generated diversity produces “insurance effects” in biofilm communities. PNAS 101:16630–35
    [Google Scholar]
  13. Bronick CJ, Lal R. 2005. Soil structure and management: a review. Geoderma 124:3–22
    [Google Scholar]
  14. Brophy C, Dooley Á, Kirwan L, Finn JA, McDonnell J et al. 2017. Biodiversity and ecosystem function: making sense of numerous species interactions in multi-species communities. Ecology 98:1771–78
    [Google Scholar]
  15. Calderón K, Spor A, Breuil M-C, Bru D, Bizouard F et al. 2017. Effectiveness of ecological rescue for altered soil microbial communities and functions. ISME J 11:272–83
    [Google Scholar]
  16. Carlson RP, Taffs RL. 2010. Molecular-level tradeoffs and metabolic adaptation to simultaneous stressors. Curr. Opin. Biotechnol. 21:670–76
    [Google Scholar]
  17. Chaparro JM, Badri DV, Vivanco JM 2014. Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803
    [Google Scholar]
  18. Connolly J, Bell T, Bolger T, Brophy C, Carnus T et al. 2013. An improved model to predict the effects of changing biodiversity levels on ecosystem function. J. Ecol. 101:344–55
    [Google Scholar]
  19. Coyte KZ, Schluter J, Foster KR 2015. The ecology of the microbiome: networks, competition, and stability. Science 350:663–66
    [Google Scholar]
  20. Dary M, Chamber-Pérez MA, Palomares AJ, Pajuelo E 2010. Insitu” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J. Hazard. Mater. 177:323–30
    [Google Scholar]
  21. Degens BP, Sparling GP. 1995. Repeated wet-dry cycles do not accelerate the mineralization of organic C involved in the macro-aggregation of a sandy loam soil. Plant Soil 175:197–203
    [Google Scholar]
  22. Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ et al. 2016. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7:10541
    [Google Scholar]
  23. Dragoš A, Kiesewalter H, Martin M, Hsu C-Y, Hartmann R et al. 2018. Division of labor during biofilm matrix production. Curr. Biol. 28:1903–13
    [Google Scholar]
  24. Driscoll WW, Pepper JW, Pierson LS, Pierson EA 2011. Spontaneous Gac mutants of Pseudomonas biological control strains: cheaters or mutualists?. Appl. Environ. Microbiol. 77:7227–35
    [Google Scholar]
  25. Dubuis C, Haas D. 2007. Cross-species GacA-controlled induction of antibiosis in pseudomonads. Appl. Environ. Microbiol. 73:650–54
    [Google Scholar]
  26. Dubuis C, Keel C, Haas D 2007. Dialogues of root-colonizing biocontrol pseudomonads. Eur. J. Plant Pathol. 119:311–28
    [Google Scholar]
  27. Eisenhauer N, Schulz W, Scheu S, Jousset A 2013. Niche dimensionality links biodiversity and invasibility of microbial communities. Funct. Ecol. 27:282–88
    [Google Scholar]
  28. Faust K, Raes J. 2012. Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10:538
    [Google Scholar]
  29. Fiegna F, Moreno-Letelier A, Bell T, Barraclough TG 2015. Evolution of species interactions determines microbial community productivity in new environments. ISME J 9:1235–45
    [Google Scholar]
  30. Fierer N. 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15:579
    [Google Scholar]
  31. Freilich S, Kreimer A, Meilijson I, Gophna U, Sharan R, Ruppin E 2010. The large-scale organization of the bacterial network of ecological co-occurrence interactions. Nucleic Acids Res 38:3857–68
    [Google Scholar]
  32. Freilich S, Zarecki R, Eilam O, Segal ES, Henry CS et al. 2011. Competitive and cooperative metabolic interactions in bacterial communities. Nat. Commun. 2:589
    [Google Scholar]
  33. Fu L, Penton CR, Ruan Y, Shen Z, Xue C et al. 2017. Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol. Biochem. 104:39–48
    [Google Scholar]
  34. Fussmann KE, Schwarzmüller F, Brose U, Jousset A, Rall BC 2014. Ecological stability in response to warming. Nat. Clim. Change 4:206–10
    [Google Scholar]
  35. Gamfeldt L, Snäll T, Bagchi R, Jonsson M, Gustafsson L et al. 2013. Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun. 4:1340
    [Google Scholar]
  36. Gravel D, Bell T, Barbera C, Bouvier T, Pommier T et al. 2011. Experimental niche evolution alters the strength of the diversity–productivity relationship. Nature 469:89–92
    [Google Scholar]
  37. Griffiths BS, Ritz K, Wheatley R, Kuan HL, Boag B et al. 2001. An examination of the biodiversity–ecosystem function relationship in arable soil microbial communities. Soil Biol. Biochem. 33:1713–22
    [Google Scholar]
  38. Hartmann M, Frey B, Mayer J, Mäder P, Widmer F 2015. Distinct soil microbial diversity under long-term organic and conventional farming. ISME J 9:1177–94
    [Google Scholar]
  39. Hautier Y, Isbell F, Borer ET, Seabloom EW, Harpole WS et al. 2018. Local loss and spatial homogenization of plant diversity reduce ecosystem multifunctionality. Nat. Ecol. Evol. 2:50–56
    [Google Scholar]
  40. Hector A, Bagchi R. 2007. Biodiversity and ecosystem multifunctionality. Nature 448:188–90
    [Google Scholar]
  41. Hibbing ME, Fuqua C, Parsek MR, Peterson SB 2010. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8:15–25
    [Google Scholar]
  42. Hillebrand H, Matthiessen B. 2009. Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol. Lett. 12:1405–19
    [Google Scholar]
  43. Hol WHG, de Boer W, de Hollander M, Kuramae EE, Meisner A, van der Putten WH 2015a. Context dependency and saturating effects of loss of rare soil microbes on plant productivity. Front. Plant Sci. 6:485
    [Google Scholar]
  44. Hol WHG, de Boer W, Termorshuizen AJ, Meyer KM, Schneider JHM et al. 2010. Reduction of rare soil microbes modifies plant–herbivore interactions. Ecol. Lett. 13:292–301
    [Google Scholar]
  45. Hol WHG, Garbeva P, Hordijk C, Hundscheid MPJ, Gunnewiek PJAK et al. 2015b. Non-random species loss in bacterial communities reduces antifungal volatile production. Ecology 96:2042–48
    [Google Scholar]
  46. Hu J, Wei Z, Friman V-P, Gu S, Wang X et al. 2016. Probiotic diversity enhances rhizosphere microbiome function and plant disease suppression. mBio 7:e01790–16
    [Google Scholar]
  47. Hu J, Wei Z, Weidner S, Friman V-P, Xu Y-C et al. 2017. Probiotic Pseudomonas communities enhance plant growth and nutrient assimilation via diversity-mediated ecosystem functioning. Soil Biol. Biochem. 113:122–29
    [Google Scholar]
  48. Hunt HW, Wall DH. 2002. Modelling the effects of loss of soil biodiversity on ecosystem function. Glob. Change Biol. 8:33–50
    [Google Scholar]
  49. Hussain S, Siddique T, Saleem M, Arshad M, Khalid A 2009. Impact of pesticides on soil microbial diversity, enzymes, and biochemical reactions. Adv. Agron. 102:159–200
    [Google Scholar]
  50. Irikiin Y, Nishiyama M, Otsuka S, Senoo K 2006. Rhizobacterial community-level, sole carbon source utilization pattern affects the delay in the bacterial wilt of tomato grown in rhizobacterial community model system. Appl. Soil Ecol. 34:27–32
    [Google Scholar]
  51. Ji P, Wilson M. 2002. Assessment of the importance of similarity in carbon source utilization profiles between the biological control agent and the pathogen in biological control of bacterial speck of tomato. Appl. Environ. Microbiol. 68:4383–89
    [Google Scholar]
  52. Jiang L, Pu Z, Nemergut DR 2008. On the importance of the negative selection effect for the relationship between biodiversity and ecosystem functioning. Oikos 117:488–93
    [Google Scholar]
  53. Jiang X, Zerfaß C, Feng S, Eichmann R, Asally M et al. 2018. Impact of spatial organization on a novel auxotrophic interaction among soil microbes. ISME J 12:1443–56
    [Google Scholar]
  54. Jousset A, Becker J, Chatterjee S, Karlovsky P, Scheu S, Eisenhauer N 2014. Biodiversity and species identity shape the antifungal activity of bacterial communities. Ecology 95:1184–90
    [Google Scholar]
  55. Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A et al. 2017. Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J 11:853–62
    [Google Scholar]
  56. Jousset A, Eisenhauer N, Materne E, Scheu S 2013. Evolutionary history predicts the stability of cooperation in microbial communities. Nat. Commun. 4:2573
    [Google Scholar]
  57. Jousset A, Eisenhauer N, Merker M, Mouquet N, Scheu S 2016. High functional diversity stimulates diversification in experimental microbial communities. Sci. Adv. 2:e1600124
    [Google Scholar]
  58. Jousset A, Schmid B, Scheu S, Eisenhauer N 2011a. Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol. Lett. 14:537–45
    [Google Scholar]
  59. Jousset A, Schulz W, Scheu S, Eisenhauer N 2011b. Intraspecific genotypic richness and relatedness predict the invasibility of microbial communities. ISME J 5:1108–14
    [Google Scholar]
  60. Kiers ET, Denison RF. 2008. Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu. Rev. Ecol. Evol. Syst. 39:215–36
    [Google Scholar]
  61. Kim W, Levy SB. 2008. Increased fitness of Pseudomonas fluorescens Pf0–1 leucine auxotrophs in soil. Appl. Environ. Microbiol. 74:3644–51
    [Google Scholar]
  62. Kinkel LL, Schlatter DC, Xiao K, Baines AD 2014. Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes. ISME J 8:249–56
    [Google Scholar]
  63. Koechler S, Farasin J, Cleiss-Arnold J, Arsène-Ploetze F 2015. Toxic metal resistance in biofilms: diversity of microbial responses and their evolution. Res. Microbiol. 166:764–73
    [Google Scholar]
  64. Krause S, Le Roux X, Niklaus PA, Van Bodegom PM, Lennon JT et al. 2014a. Trait-based approaches for understanding microbial biodiversity and ecosystem functioning. Front. Microbiol. 5:251
    [Google Scholar]
  65. Krause S, van Bodegom PM, Cornwell WK, Bodelier PLE 2014b. Weak phylogenetic signal in physiological traits of methane-oxidizing bacteria. J. Evol. Biol. 27:1240–47
    [Google Scholar]
  66. Lawrence D, Fiegna F, Behrends V, Bundy JG, Phillimore AB et al. 2012. Species interactions alter evolutionary responses to a novel environment. PLOS Biol 10:e1001330
    [Google Scholar]
  67. Li M, Wei Z, Wang J, Jousset A et al. 2019. Facilitation promotes invasions in plant‐associated microbial communities. Ecol. Lett. 22:149–58
    [Google Scholar]
  68. Ling N, Zhu C, Xue C, Chen H, Duan Y et al. 2016. Insight into how organic amendments can shape the soil microbiome in long-term field experiments as revealed by network analysis. Soil Biol. Biochem. 99:137–49
    [Google Scholar]
  69. Locey KJ, Fisk MC, Lennon JT 2017. Microscale insight into microbial seed banks. Front. Microbiol. 7:2040
    [Google Scholar]
  70. Lori M, Symnaczik S, Mäder P, Deyn GD, Gattinger A 2017. Organic farming enhances soil microbial abundance and activity—a meta-analysis and meta-regression. PLOS ONE 12:e0180442
    [Google Scholar]
  71. Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541–56
    [Google Scholar]
  72. Lupatini M, Korthals GW, de Hollander M, Janssens TKS, Kuramae EE 2017. Soil microbiome is more heterogeneous in organic than in conventional farming system. Front. Microbiol. 7:2064
    [Google Scholar]
  73. Meng L, Sun T, Li M, Saleem M, Zhang Q, Wang C 2019. Soil-applied biochar increases microbial diversity and wheat plant performance under herbicide fomesafen stress. Ecotox. Environ. Saf. 171:75–83
    [Google Scholar]
  74. McDaniel MD, Tiemann LK, Grandy AS 2014. Does agricultural crop diversity enhance soil microbial biomass and organic matter dynamics? A meta-analysis. Ecol. Appl. 24:560–70
    [Google Scholar]
  75. Mehrabi Z, McMillan VE, Clark IM, Canning G, Hammond-Kosack KE et al. 2016. Pseudomonas spp. diversity is negatively associated with suppression of the wheat take-all pathogen. Sci. Rep. 6:29905
    [Google Scholar]
  76. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–100
    [Google Scholar]
  77. Messiha NAS, van Bruggen AHC, Franz E, Janse JD, Schoeman-Weerdesteijn ME et al. 2009. Effects of soil type, management type and soil amendments on the survival of the potato brown rot bacterium Ralstonia solanacearum. Appl. Soil Ecol 43:206–15
    [Google Scholar]
  78. Netzker T, Fischer J, Weber J, Mattern DJ, König CC et al. 2015. Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front. Microbiol. 6:299
    [Google Scholar]
  79. Pang G, Cai F, Li R, Zhao Z, Li R et al. 2017. Trichoderma-enriched organic fertilizer can mitigate microbiome degeneration of monocropped soil to maintain better plant growth. Plant Soil 416:181–92
    [Google Scholar]
  80. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH 2013a. Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11:789–99
    [Google Scholar]
  81. Philippot L, Spor A, Hénault C, Bru D, Bizouard F et al. 2013b. Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–19
    [Google Scholar]
  82. Pineda A, Kaplan I, Bezemer TM 2017. Steering soil microbiomes to suppress aboveground insect pests. Trends Plant Sci 22:770–78
    [Google Scholar]
  83. Prabhukarthikeyan R, Saravanakumar D, Raguchander T 2014. Combination of endophytic Bacillus and Beauveria for the management of Fusarium wilt and fruit borer in tomato. Pest Manag. Sci. 70:1742–50
    [Google Scholar]
  84. Raaijmakers JM, Mazzola M. 2016. Soil immune responses. Science 352:1392–93
    [Google Scholar]
  85. Rabbi SMF, Daniel H, Lockwood PV, Macdonald C, Pereg L et al. 2016. Physical soil architectural traits are functionally linked to carbon decomposition and bacterial diversity. Sci. Rep. 6:33012
    [Google Scholar]
  86. Ravanbakhsh M, Sasidharan R, Voesenek LACJ, Kowalchuk GA, Jousset A 2017. ACC deaminase–producing rhizosphere bacteria modulate plant responses to flooding. J. Ecol. 105:979–86
    [Google Scholar]
  87. Reich PB, Tilman D, Isbell F, Mueller K, Hobbie SE et al. 2012. Impacts of biodiversity loss escalate through time as redundancy fades. Science 336:589–92
    [Google Scholar]
  88. Ren D, Madsen JS, Sørensen SJ, Burmølle M 2015. High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. ISME J 9:81–89
    [Google Scholar]
  89. Rillig MC, Aguilar‐Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A 2015. Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–88
    [Google Scholar]
  90. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F et al. 2015. Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ. Microbiol. 17:316–31
    [Google Scholar]
  91. Saleem M, Arshad M, Hussain S, Bhatti AS 2007. Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. Microbiol. Biotechnol. 34:635–48
    [Google Scholar]
  92. Saleem M, Fetzer I, Dormann CF, Harms H, Chatzinotas A 2012. Predator richness increases the effect of prey diversity on prey yield. Nat. Commun. 3:1305
    [Google Scholar]
  93. Saleem M, Fetzer I, Harms H, Chatzinotas A 2013. Diversity of protists and bacteria determines predation performance and stability. ISME J 7:1912–21
    [Google Scholar]
  94. Saleem M, Fetzer I, Harms H, Chatzinotas A 2016a. Trophic complexity in aqueous systems: bacterial species richness and protistan predation regulate dissolved organic carbon and dissolved total nitrogen removal. Proc. R. Soc. B 283:20152724
    [Google Scholar]
  95. Saleem M, Law AD, Moe LA 2016b. Nicotiana roots recruit rare rhizosphere taxa as major root-inhabiting microbes. Microb. Ecol. 71:469–72
    [Google Scholar]
  96. Saleem M, Law AD, Sahib MR, Pervaiz ZH, Zhang Q 2018. Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere 6:47–51
    [Google Scholar]
  97. Saleem M, Meckes N, Pervaiz ZH, Traw MB 2017. Microbial interactions in the phyllosphere increase plant performance under herbivore biotic stress. Front. Microbiol. 8:41
    [Google Scholar]
  98. Saleem M, Moe LA. 2014. Multitrophic microbial interactions for eco- and agro-biotechnological processes: theory and practice. Trends Biotechnol 32:529–37
    [Google Scholar]
  99. Saleem M, Pervaiz ZH, Traw MB 2015. Theories, mechanisms and patterns of microbiome species coexistence in an era of climate change. Microbiome Community Ecology: Fundamentals and Applications M Saleem 13–53 Berlin: Springer
    [Google Scholar]
  100. Scherer-Lorenzen M. 2005. Biodiversity and ecosystem functioning: basic principles. Biodiversity: Structure and Function W Barthlott, E Linsenmair, S Porembski 68–88 Oxford, UK: EOLSS
    [Google Scholar]
  101. Schindler DE, Armstrong JB, Reed TE 2015. The portfolio concept in ecology and evolution. Front. Ecol. Environ. 13:257–63
    [Google Scholar]
  102. Schlatter D, Kinkel L, Thomashow L, Weller D, Paulitz T 2017. Disease suppressive soils: new insights from the soil microbiome. Phytopathology 107:1284–97
    [Google Scholar]
  103. Seth EC, Taga ME. 2014. Nutrient cross-feeding in the microbial world. Front. Microbiol. 5:350
    [Google Scholar]
  104. Shoemaker WR, Locey KJ, Lennon JT 2017. A macroecological theory of microbial biodiversity. Nat. Ecol. Evol. 1:0107
    [Google Scholar]
  105. Singh BK, Quince C, Macdonald CA, Khachane A, Thomas N et al. 2014. Loss of microbial diversity in soils is coincident with reductions in some specialized functions. Environ. Microbiol. 16:2408–20
    [Google Scholar]
  106. Singh M, Awasthi A, Soni SK, Singh R, Verma RK, Kalra A 2015. Complementarity among plant growth promoting traits in rhizospheric bacterial communities promotes plant growth. Sci. Rep. 5:15500
    [Google Scholar]
  107. Slade EM, Kirwan L, Bell T, Philipson CD, Lewis OT, Roslin T 2017. The importance of species identity and interactions for multifunctionality depends on how ecosystem functions are valued. Ecology 98:2626–39
    [Google Scholar]
  108. Steinbauer MJ, Field R, Fernández‐Palacios JM, Irl SDH, Otto R et al. 2016. Biogeographic ranges do not support niche theory in radiating Canary Island plant clades. Glob. Ecol. Biogeogr. 25:792–804
    [Google Scholar]
  109. Tang J, Zhou S. 2011. The importance of niche differentiation for coexistence on large scales. J. Theor. Biol. 273:32–36
    [Google Scholar]
  110. Thijs S, Weyens N, Sillen W, Gkorezis P, Carleer R, Vangronsveld J 2014. Potential for plant growth promotion by a consortium of stress-tolerant 2,4-dinitrotoluene-degrading bacteria: isolation and characterization of a military soil. Microb. Biotechnol. 7:294–306
    [Google Scholar]
  111. Tiemann LK, Grandy AS, Atkinson EE, Marin-Spiotta E, McDaniel MD 2015. Crop rotational diversity enhances belowground communities and functions in an agroecosystem. Ecol. Lett. 18:761–71
    [Google Scholar]
  112. Tsoi R, Wu F, Zhang C, Bewick S, Karig D, You L 2018. Metabolic division of labor in microbial systems. PNAS 115:2526–31
    [Google Scholar]
  113. Tyc O, van den Berg M, Gerards S, van Veen JA, Raaijmakers JM et al. 2014. Impact of interspecific interactions on antimicrobial activity among soil bacteria. Front. Microbiol. 5:567
    [Google Scholar]
  114. Tyc O, Zweers H, de Boer W, Garbeva P 2015. Volatiles in inter-specific bacterial interactions. Front. Microbiol. 6:1412
    [Google Scholar]
  115. van der Plas F, Manning P, Allan E, Scherer-Lorenzen M, Verheyen K et al. 2016. Jack-of-all-trades effects drive biodiversity–ecosystem multifunctionality relationships in European forests. Nat. Commun. 7:11109
    [Google Scholar]
  116. van Elsas JD, Chiurazzi M, Mallon CA, Elhottovā D, Krištůfek V, Salles JF 2012. Microbial diversity determines the invasion of soil by a bacterial pathogen. PNAS 109:1159–64
    [Google Scholar]
  117. Wagg C, Bender SF, Widmer F, van der Heijden MGA 2014. Soil biodiversity and soil community composition determine ecosystem multifunctionality. PNAS 111:5266–70
    [Google Scholar]
  118. Wagner MR, Lundberg DS, Coleman-Derr D, Tringe SG, Dangl JL, Mitchell-Olds T 2014. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecol. Lett. 17:717–26
    [Google Scholar]
  119. Wei F, Hu X, Xu X 2016. Dispersal of Bacillus subtilis and its effect on strawberry phyllosphere microbiota under open field and protection conditions. Sci. Rep. 6:22611
    [Google Scholar]
  120. Wei Z, Yang T, Friman V-P, Xu Y, Shen Q, Jousset A 2015. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6:8413
    [Google Scholar]
  121. Weidner S, Koller R, Latz E, Kowalchuk G, Bonkowski M et al. 2015. Bacterial diversity amplifies nutrient-based plant-soil feedbacks. Funct. Ecol. 29:1341–49
    [Google Scholar]
  122. Weisser WW, Roscher C, Meyer ST, Ebeling A, Luo G et al. 2017. Biodiversity effects on ecosystem functioning in a 15-year grassland experiment: patterns, mechanisms, and open questions. Basic Appl. Ecol. 23:1–73
    [Google Scholar]
  123. Williams LJ, Paquette A, Cavender-Bares J, Messier C, Reich PB 2017. Spatial complementarity in tree crowns explains overyielding in species mixtures. Nat. Ecol. Evol. 1:0063
    [Google Scholar]
  124. Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D et al. 2009. Initial community evenness favours functionality under selective stress. Nature 458:623–26
    [Google Scholar]
  125. Wood SA, Bradford MA, Gilbert JA, McGuire KL, Palm CA et al. 2015. Agricultural intensification and the functional capacity of soil microbes on smallholder African farms. J. Appl. Ecol. 52:744–52
    [Google Scholar]
  126. Xiong W, Guo S, Jousset A, Zhao Q, Wu H et al. 2017. Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biol. Biochem. 114:238–47
    [Google Scholar]
  127. Yachi S, Loreau M. 1999. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. PNAS 96:1463–68
    [Google Scholar]
  128. Yang T, Han G, Yang Q, Friman V-P, Gu S et al. 2018. Resource stoichiometry shapes community invasion resistance via productivity-mediated species identity effects. Proc. R. Soc. B 285:20182035
    [Google Scholar]
  129. Yang T, Wei Z, Friman V-P, Xu Y, Shen Q et al. 2017. Resource availability modulates biodiversity–invasion relationships by altering competitive interactions. Environ. Microbiol. 19:2984–91
    [Google Scholar]
  130. Yang W, Xu X, Li Y, Wang Y, Li M et al. 2016. Rutin-mediated priming of plant resistance to three bacterial pathogens initiating the early SA signal pathway. PLOS ONE 11:e0146910
    [Google Scholar]
  131. Zavaleta ES, Pasari JR, Hulvey KB, Tilman GD 2010. Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. PNAS 107:1443–46
    [Google Scholar]
  132. Zhang Q, Saleem M, Wang C 2017. Probiotic strain Stenotrophomonas acidaminiphila BJ1 degrades and reduces chlorothalonil toxicity to soil enzymes, microbial communities and plant roots. AMB Express 7:227
    [Google Scholar]
  133. Zolla G, Badri DV, Bakker MG, Manter DK, Vivanco JM 2013. Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis.. Appl. Soil Ecol 68:1–9
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-110617-062605
Loading
/content/journals/10.1146/annurev-ecolsys-110617-062605
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error