Advertisement

Mycorrhiza

pp 1–13 | Cite as

Initial microbial status modulates mycorrhizal inoculation effect on rhizosphere microbial communities

  • Frédérique ChangeyEmail author
  • Hacène Meglouli
  • Joël Fontaine
  • Maryline Magnin-Robert
  • Benoit Tisserant
  • Thomas Z. Lerch
  • Anissa Lounès-Hadj Sahraoui
Original Article
  • 51 Downloads

Abstract

Arbuscular mycorrhizal fungi (AMF) play a central role in rhizosphere functioning as they interact with both plants and soil microbial communities. The conditions in which AMF modify plant physiology and microbial communities in the rhizosphere are still poorly understood. In the present study, four different plant species, (clover, alfalfa, ryegrass, tall fescue) were cultivated in either sterilized (γ ray) or non-sterilized soil and either inoculated with a commercial AMF (Glomus LPA Val 1.) or not. After 20 weeks of cultivation, the mycorrhizal rate and shoot and root biomasses were measured. The abundance and composition of bacteria, archaea, and fungi were analyzed, respectively, by quantitative PCR (qPCR) and fingerprinting techniques. Whilst sterilization did not change the AMF capacity to modify plant biomass, significant changes in microbial communities were observed, depending on the taxon and the associated plant. AMF inoculation decreases both bacterial and archaeal abundance and diversity, with a greatest extent in sterilized samples. These results also show that AMF exert different selections on soil microbial communities according to the plant species they are associated with. This study suggests that the initial abundance and diversity of rhizosphere microbial communities should be considered when introducing AMF to cultures.

Keywords

Rhizosphere Sterilization Soil microbial communities Arbuscular mycorrhizal fungi Archaea 

Notes

Funding information

This work has been carried out in the Halluin3R project, which is financed by the European Union (FEDER), the French Region of Hauts-de-France, and the French Environment and Energy Management Agency (ADEME) and in the framework of the Alibiotech project which is financed by the European Union, the French State, and the French Region of Hauts-de-France.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

572_2019_914_MOESM1_ESM.doc (266 kb)
ESM 1 (DOC 265 kb)

References

  1. Albertsen A, Ravnskov S, Green H, Jensen DF, Larsen J (2006) Interactions between the external mycelium of the mycorrhizal fungus Glomus intraradices and other soil microorganisms as affected by organic matter. Soil Biol Biochem 38(5):1008–1014CrossRefGoogle Scholar
  2. Andrade G, Mihara K, Linderman R, Bethlenfalvay G (1997) Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi. Plant Soil 192:71–79CrossRefGoogle Scholar
  3. Andrade G, Linderman RG, Bethlenfalvay GJ (1998a) Bacterial associations with the mycorrhizosphere and hyphosphere of the arbuscular mycorrhizal fungus Glomus mosseae. Plant Soil 202(1):79–87CrossRefGoogle Scholar
  4. Andrade G, Mihara KL, Linderman RG, Bethlenfalvay GJ (1998b) Soil aggregation status and rhizobacteria in the mycorrhizosphere. Plant Soil 202(1):89–96CrossRefGoogle Scholar
  5. Artursson V (2005) Bacterial-fungal interactions highlighted using microbiomics. Uppsala : Sveriges lantbruksuniv. Acta Universitatis Agriculturae Sueciae, vol 2005. No. 127Google Scholar
  6. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11(1):3–42CrossRefGoogle Scholar
  7. Azcón R, Rubio R, Barea JM (1991) Selective interactions between different species of mycorrhizal fungi and Rhizobium meliloti strains, and their effects on growth, N2-fixation (15N) and nutrition of Medicago sativa L. New Phytol 117(3):399–404CrossRefGoogle Scholar
  8. Baldwin IL, Fred EB (1929) Nomenclature of the root-nodule bacteria of the Leguminosae. J Bacteriol 17(2):141Google Scholar
  9. Balser TC, Kinzig AP, Firestone MK (2002) Linking soil microbial communities and ecosystem functioning. In: The functional consequences of biodiversity: empirical progress and theoretical extensions. Princeton University Press, Princeton, pp 265–293Google Scholar
  10. Battini F, Cristani C, Giovannetti M, Agnolucci M (2016) Multifunctionality and diversity of culturable bacterial communities strictly associated with spores of the plant beneficial symbiont Rhizophagus intraradices. Microbiol Res 183:68–79CrossRefGoogle Scholar
  11. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13CrossRefGoogle Scholar
  12. Biró B, Köves-Péchy K, Vörös I, Takács T, Eggenberger P, Strasser RJ (2000) Interrelations between Azospirillum and rhizobium nitrogen-fixers and arbuscular mycorrhizal fungi in the rhizosphere of alfalfa in sterile, AMF-free or normal soil conditions. Appl Soil Ecol 15(2):159–168CrossRefGoogle Scholar
  13. Blaud A, Phoenix GK, Osborn AM (2015) Variation in bacterial, archaeal and fungal community structure and abundance in high Arctic tundra soil. Polar Biol 38(7):1009–1024CrossRefGoogle Scholar
  14. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48CrossRefGoogle Scholar
  15. Bowen HJM, Cawse PA (1964) Some effects of gamma radiation on the composition of the soil solution and soil organic matter. Soil Sci 98(6):358–361CrossRefGoogle Scholar
  16. Brulé C, Frey-Klett P, Pierrat JC, Courrier S, Gérard F, Lemoine MC, Garbaye J (2001) Survival in the soil of the ectomycorrhizal fungus Laccaria bicolor and the effects of a mycorrhiza helper Pseudomonas fluorescens. Soil Biol Biochem 33(12–13):1683–1694CrossRefGoogle Scholar
  17. Burns JH, Anacker BL, Strauss SY, Burke DJ (2015) Soil microbial community variation correlates most strongly with plant species identity, followed by soil chemistry, spatial location and plant genus. AoB Plants 7Google Scholar
  18. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427(6976):731–733CrossRefGoogle Scholar
  19. Campos-Soriano L, García-Martínez J, San Segundo B (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13(6):579–592.13:579CrossRefGoogle Scholar
  20. Camprubi A, Calvet C, Estaun V (1995) Growth enhancement of Citrus reshni after inoculation with Glomus intraradices and Trichoderma aureoviride and associated effects on microbial populations and enzyme activity in potting mixes. Plant Soil 173(2):233–238CrossRefGoogle Scholar
  21. Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM, Schenk PM (2015) Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol Plant-Microbe Interact 28(9):1049–1058CrossRefGoogle Scholar
  22. Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282(1–2):209–225CrossRefGoogle Scholar
  23. Cecatto AP, Calvete EO, Escosteguy PAV, De Nardi FS, dos Santos FL (2014) Effect of substrate sterilization with mycorrhizal inoculation on strawberry growth. Vii Congreso Iberico De Agroingenieria Y Ciencias Horticolas: Innovar Y Producir Para El Futuro Innovating and Producing for the Future, pp 1681–1685Google Scholar
  24. Changey F, Bagard M, Souleymane M, Lerch TZ (2018) Cascading effects of elevated ozone on wheat rhizosphere microbial communities depend on temperature and cultivar sensitivity. Environ Pollut 242:113–125CrossRefGoogle Scholar
  25. Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959CrossRefGoogle Scholar
  26. Deveau A (2016) How does the tree root microbiome assemble? Influence of ectomycorrhizal species on Pinus sylvestris root bacterial communities. Environ Microbiol 18:1303–1305CrossRefGoogle Scholar
  27. Duponnois R, Galiana A, Prin Y (2008) The mycorrhizosphere effect: a multitrophic interaction complex improves mycorrhizal symbiosis and plant growth. In: Mycorrhizae: sustainable agriculture and forestry. Springer, Dordrecht, pp 227–240CrossRefGoogle Scholar
  28. Eom AH, Hartnett DC, Wilson GW (2000) Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122(3):435–444CrossRefGoogle Scholar
  29. Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci 109(52):21390–21395CrossRefGoogle Scholar
  30. Fitzpatrick CR, Copeland J, Wang PW, Guttman DS, Kotanen PM, Johnson MT (2018) Assembly and ecological function of the root microbiome across angiosperm plant species. Proc Natl Acad Sci 115(6):E1157–E1165CrossRefGoogle Scholar
  31. Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35(6):837–843CrossRefGoogle Scholar
  32. Franklin RB, Garland JL, Bolster CH, Mills AL (2001) Impact of dilution on microbial community structure and functional potential: comparison of numerical simulations and batch culture experiments. Appl Environ Microbiol 67:702–712CrossRefGoogle Scholar
  33. Frey-Klett P, Garbaye JA, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176(1):22–36CrossRefGoogle Scholar
  34. Garbaye J (1994) Tansley review no. 76 helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210CrossRefGoogle Scholar
  35. Gavito ME, Jakobsen I, Mikkelsen TN, Mora F (2019) Direct evidence for modulation of photosynthesis by an arbuscular mycorrhiza-induced carbon sink strength. New PhytolGoogle Scholar
  36. Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339CrossRefGoogle Scholar
  37. Graham JH (1982) Effect of citrus root exudates on germination of chlamydospores of the vesicular-arbuscular mycorrhizal fungus, Glomus epigaeum. Mycologia 74(5):831–835CrossRefGoogle Scholar
  38. Halsey JA, de Cássia Pereira ESM, Andreote FD (2016) Bacterial selection by mycospheres of Atlantic rainforest mushrooms. Antonie Van Leeuwenhoek 109(10):1353–1365CrossRefGoogle Scholar
  39. Hiltner L (1904) Uber neure Erfahrungen und probleme auf dem gebeit der bodenbackteriologie und unter besonderer berucksichtigung der grundungung und brache. ArbGoogle Scholar
  40. Hodge A (2000) Microbial ecology of the arbuscular mycorrhiza. FEMS Microbiol Ecol 32(2):91–96CrossRefGoogle Scholar
  41. Horii S, Ishii T (2006) Identification and function of Gigaspora margarita growth-promoting microorganisms. Symbiosis 41:135–141Google Scholar
  42. Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea J-M (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16Google Scholar
  43. Johnson D, Ijdo M, Genney DR, Anderson IC, Alexander IJ (2005) How do plants regulate the function, community structure, and diversity of mycorrhizal fungi? J Exp Bot 56(417):1751–1760CrossRefGoogle Scholar
  44. Karlsson AE, Johansson T, Bengtson P (2012) Archaeal abundance in relation to root and fungal exudation rates. FEMS Microbiol Ecol 80(2):305–311CrossRefGoogle Scholar
  45. Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41(6):1233–1244CrossRefGoogle Scholar
  46. Koske R, Gemma J (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488CrossRefGoogle Scholar
  47. Kumar R, Pandey S, Pandey A (2006) Plant roots and carbon sequestration. Curr Sci 91:885–890Google Scholar
  48. Lennon JT, Aanderud ZT, Lehmkuhl BK, Schoolmaster DR Jr (2012) Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 93(8):1867–1879CrossRefGoogle Scholar
  49. Linderman R (1988) Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. J Phytopathol 78:366–371Google Scholar
  50. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50(3):529–544CrossRefGoogle Scholar
  51. López-Gutiérrez JC, Henry S, Hallet S, Martin-Laurent F, Catroux G, Philippot L (2004) Quantification of a novel group of nitrate-reducing bacteria in the environment by real-time PCR. J Microbiol Methods 57(3):399–407CrossRefGoogle Scholar
  52. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556CrossRefGoogle Scholar
  53. Marschner P, Timonen S (2006) Bacterial community composition and activity in rhizosphere of roots colonized by arbuscular mycorrhizal fungi. In: Microbial activity in the Rhizoshere. Springer, Berlin, Heidelberg, pp 139–154CrossRefGoogle Scholar
  54. McGonigle T, Miller M, Evans D, Fairchild G, Swan J (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501CrossRefGoogle Scholar
  55. McNamara N, Black H, Beresford N, Parekh NJASE (2003) Effects of acute gamma irradiation on chemical, physical and biological properties of soils. Appl Soil Ecol 24(2):117–132CrossRefGoogle Scholar
  56. Meglouli H, Sahraoui ALH, Magnin-Robert M, Tisserant B, Hijri M, Fontaine J (2018) Arbuscular mycorrhizal inoculum sources influence bacterial, archaeal, and fungal communities’ structures of historically dioxin/furan-contaminated soil but not the pollutant dissipation rate. Mycorrhiza 28(7):635CrossRefGoogle Scholar
  57. Morris SJ, Boerner REJ (1999) Spatial distribution of fungal and bacterial biomass in southern Ohio hardwood forest soils: scale dependency and landscape patterns. Soil Biol Biochem 31:887–902CrossRefGoogle Scholar
  58. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3):695–700Google Scholar
  59. Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5(9):787–797CrossRefGoogle Scholar
  60. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55(1):158–IN18CrossRefGoogle Scholar
  61. Qin H, Brookes PC, Xu J (2016) Arbuscular mycorrhizal fungal hyphae alter soil bacterial community and enhance polychlorinated biphenyls dissipation. Front Microbiol 7:939Google Scholar
  62. Ramsay AJ, Bawden AD (1983) Effects of sterilization and storage on respiration, nitrogen status and direct counts of soil bacteria using acridine orange. Soil Biol Biochem 15(3):263–268CrossRefGoogle Scholar
  63. Rousk J, Bååth E (2007) Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiol Ecol 62:258–267CrossRefGoogle Scholar
  64. Rousk J, Demoling LA, Bahr A, Bååth E (2008) Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol Ecol 63(3):350–358CrossRefGoogle Scholar
  65. Ryan MH, Graham JH (2002) Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant Soil 244:263–271CrossRefGoogle Scholar
  66. Saia S, Ruisi P, Fileccia V, Di Miceli G, Amato G, Martinelli F (2015) Metabolomics suggests that soil inoculation with arbuscular mycorrhizal fungi decreased free amino acid content in roots of durum wheat grown under N-limited, P-rich field conditions. PLoS One 10:e0129591CrossRefGoogle Scholar
  67. Scheublin TR, Sanders IR, Keel C, Van Der Meer JR (2010) Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME J 4(6):752–763CrossRefGoogle Scholar
  68. Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic pressGoogle Scholar
  69. Söderberg KH, Olsson PA, Bååth E (2002) Structure and activity of the bacterial community in the rhizosphere of different plant species and the effect of arbuscular mycorrhizal colonisation. FEMS Microbiol Ecol 40(3):223–231CrossRefGoogle Scholar
  70. Solís-Domínguez FA, Valentín-Vargas A, Chorover J, Maier RM (2011) Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Sci Total Environ 409(6):1009–1016CrossRefGoogle Scholar
  71. Song YY, Cao M, Xie LJ, Liang XT, Zeng RS, Su YJ, Huang JH, Wang RL, Luo SM (2011) Induction of DIMBOA accumulation and systemic defense responses as a mechanism of enhanced resistance of mycorrhizal corn (Zea mays L.) to sheath blight. Mycorrhiza 21:721–731CrossRefGoogle Scholar
  72. Srivastava R, Khalid A, Singh US, Sharma AK (2010) Evaluation of arbuscular mycorrhizal fungus, fluorescent Pseudomonas and Trichoderma harzianum formulation against Fusarium oxysporum f. sp. lycopersici for the management of tomato wilt. Biol Control 53(1):24–31CrossRefGoogle Scholar
  73. Sylvia DM, Williams SE (1992) Vesicular–arbuscular mycorrhizae and environmental stresses. In: Bethlenfalvay GJ, Linderman RG (eds) Mycorrhizae in sustainable agriculture. ASA no 54, Madison, pp 101–124Google Scholar
  74. Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61(2):295–304CrossRefGoogle Scholar
  75. Tuason MMS, Arocena JM (2009) Root organic acid exudates and properties of rhizosphere soils of white spruce (Picea glauca) and subalpine fir (Abies lasiocarpa). Can J Soil Sci 89(3):287–300CrossRefGoogle Scholar
  76. 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(8):1555–1564CrossRefGoogle Scholar
  77. Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26(1):379–407CrossRefGoogle Scholar
  78. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for hylogenetics. PCR Protocols: A Guide to Methods and Applications 18:315–322.Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Unité de Chimie Environnementale et Interactions sur le Vivant) (UCEIV), EA 4492, SFR Condorcet FR CNRS 3417Université du Littoral Côte d’OpaleCalaisFrance
  2. 2.Paris Institute of Ecology and Environnemental Sciences (IEES-Paris), UMR 7518 (CNRS- SU-INRA-UPEC- Paris Diderot-IRD)Université Paris-Est CréteilCréteil CedexFrance

Personalised recommendations