Advertisement

Microbial Ecology

, Volume 72, Issue 1, pp 197–206 | Cite as

Infection with a Shoot-Specific Fungal Endophyte (Epichloë) Alters Tall Fescue Soil Microbial Communities

  • Xavier Rojas
  • Jingqi Guo
  • Jonathan W. Leff
  • David H. McNearJr.
  • Noah Fierer
  • Rebecca L. McCulley
Plant Microbe Interactions

Abstract

Tall fescue (Schedonorus arundinaceus) is a widespread grass that can form a symbiotic relationship with a shoot-specific fungal endophyte (Epichloë coenophiala). While the effects of fungal endophyte infection on fescue physiology and ecology have been relatively well studied, less attention has been given to how this relationship may impact the soil microbial community. We used high-throughput DNA sequencing and phospholipid fatty acid analysis to determine the structure and biomass of microbial communities in both bulk and rhizosphere soils from tall fescue stands that were either uninfected with E. coenophiala or were infected with the common toxic strain or one of several novel strains of the endophyte. We found that rhizosphere and bulk soils harbored distinct microbial communities. Endophyte presence, regardless of strain, significantly influenced soil fungal communities, but endophyte effects were less pronounced in prokaryotic communities. E. coenophiala presence did not change total fungal biomass but caused a shift in soil and rhizosphere fungal community composition, increasing the relative abundance of taxa within the Glomeromycota phylum and decreasing the relative abundance of genera in the Ascomycota phylum, including Lecanicillium, Volutella, Lipomyces, Pochonia, and Rhizoctonia. Our data suggests that tripartite interactions exist between the shoot endophyte E. coenophiala, tall fescue, and soil fungi that may have important implications for the functioning of soils, such as carbon storage, in fescue-dominated grasslands.

Keywords

Epichloë coenophiala Mycorrhizae Neotyphodium Plant-microbe interactions Schedonorus arundinaceus Soil microbes 

Notes

Acknowledgments

We thank Joe Kupper, Jim Nelson, and Elizabeth Carlisle for field assistance, and Tim Phillips for allowing us to sample his grazing trial material. This research was supported by grants from the USDA-NRI (Award #’s 2011-67019-30392 and 2008-35107-04504), a cooperative agreement with the USDA-ARS Forage Animal Production Research Unit (58-6440-7-135), and the Kentucky Agricultural Experiment Station (KY006045).

Supplementary material

248_2016_750_MOESM1_ESM.docx (19 kb)
ESM 1 Supplemental Table 1: Results of the multifactor ANOVA testing the effect of sample type (bulk vs. rhizosphere soils), tall fescue cultivar (PDF vs. 97TF1), and endophyte status (E-, CTE+, AR542E+, AR584E+) on bacterial biomass (nmol g soil−1), fungal biomass (nmol g soil−1), the ratio of bacterial to fungal biomass, and the amount of 16:1ω5c (nmol g soil−1). Significant effects (P < 0.05) are bolded. Supplemental Table 2: Pair-wise PERMANOVA comparisons of the effect of different endophyte statuses on soil prokaryotic and fungal communities by tall fescue cultivar (PDF vs. 97TF1) and across soil type. Endophyte statuses whose microbial communities strongly differed from each other are bolded (P < 0.01). Supplemental Table 3: Pair-wise PERMANOVA comparisons of the effect of different endophyte statuses on soil prokaryotic and fungal communities by soil type (bulk vs. rhizosphere) and across cultivar. There were no endophyte statuses whose microbial communities strongly (P < 0.01) differed from each other in these comparisons. (DOCX 18 kb)

References

  1. 1.
    Schantz HL (1954) The place of grasslands in the earth’s cover of vegetation. Ecology 35:43–145Google Scholar
  2. 2.
    Wedin WF, Fales SL (2009) Grassland: quietness and strength for a new American agriculture. ASA-CSSA-SSSA, MadisonGoogle Scholar
  3. 3.
    Leuchtmann A (1992) Systematics, distribution, and host specificity of grass endophytes. Nat Toxins 1:150–162CrossRefPubMedGoogle Scholar
  4. 4.
    Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127CrossRefPubMedGoogle Scholar
  5. 5.
    Rudgers JA, Clay K (2007) Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biol Rev 21:107–124CrossRefGoogle Scholar
  6. 6.
    Omacini M, Semmartin M, Pérez LI, Gundel PE (2012) Grass–endophyte symbiosis: a neglected aboveground interaction with multiple belowground consequences. Appl Soil Ecol 61:273–279CrossRefGoogle Scholar
  7. 7.
    Ball DM, Pederson JF, Lacefield GD (1993) The tall-fescue endophyte. Am Sci 81:370–379Google Scholar
  8. 8.
    Leuchtmann A, Bacon CW, Schardl CL, White JF, Tadych M (2014) Nomenclature realignment of Neotyphodium species with genus Epichloë. Mycologia 106:202–215CrossRefPubMedGoogle Scholar
  9. 9.
    West CP (1994) Physiology and drought tolerance of endophyte-infected grasses. In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton, pp 87–99Google Scholar
  10. 10.
    Marks S, Clay K (1996) Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol 133:727–733CrossRefGoogle Scholar
  11. 11.
    Elmi AA, West CP, Robbins RT, Kirkpatrick TL (2000) Endophyte effects on reproduction of a root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue. Grass Forage Sci 55:166–172CrossRefGoogle Scholar
  12. 12.
    Newman JA, Abner ML, Dado RG, Gibson DJ, Brookings A, Parsons AJ (2003) Effects of elevated CO2, nitrogen and fungal endophyte-infection on tall fescue: growth, photosynthesis, chemical composition and digestibility. Global Change Biol 9:425–437CrossRefGoogle Scholar
  13. 13.
    Richardson MD, Hoveland CS, Bacon CW (1993) Photosynthesis and stomatal conductance of symbiotic and nonsymbiotic tall fescue. Crop Sci 33:145–149CrossRefGoogle Scholar
  14. 14.
    Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940CrossRefGoogle Scholar
  15. 15.
    Bush LP, Wilkinson HH, Schardl CS (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114:1–7PubMedPubMedCentralGoogle Scholar
  16. 16.
    Hoveland CS (1993) Importance and economic-significance of the Acremonium endophytes to performance of animals and grass plant. Agr Ecosyst Environ 44:3–12CrossRefGoogle Scholar
  17. 17.
    Stuedemann JA, Hoveland CS (1988) Fescue endophyte: history and impact on animal agriculture. J Prod Agric 1:39–44CrossRefGoogle Scholar
  18. 18.
    Lemons A, Clay K, Rudgers JA (2005) Connecting plant-microbial interactions above and belowground: a fungal endophyte affects decomposition. Oecologia 145:595–604CrossRefPubMedGoogle Scholar
  19. 19.
    Siegrist JA, McCulley RL, Bush LP, Phillips TD (2010) Alkaloids may not be responsible for endophyte-associated reductions in tall fescue decomposition rates. Funct Ecol 24:460–468CrossRefGoogle Scholar
  20. 20.
    Franzluebbers AJ, Hill NS (2005) Soil carbon, nitrogen, and ergot alkaloids with short-and long-term exposure to endophyte-infected and endophyte-free tall fescue. Soil Sci Soc Am J 69:404–412CrossRefGoogle Scholar
  21. 21.
    McNear DH Jr, McCulley RL (2012) Influence of the Neotyphodium-tall fescue symbiosis on belowground processes. In: Young CA, Aiken GE, Strickland JR, Schardl CL (eds) Epichloae, endophytes of cool season grasses: implications, utilization and biology. Proceedings of the 7th International Symposium on Fungal Endophytes of Grasses. Samuel Roberts Noble Foundation, Ardmore, pp 94–99Google Scholar
  22. 22.
    Timper P (2009) Nematodes. In: Fribourg HA, Hannaway DB, West CP (eds) Tall fescue for the twenty-first century. ASA-CSSA-SSSA Monograph, Madison 53:151–156Google Scholar
  23. 23.
    Rostás M, Cripps MG, Silcock P (2015) Aboveground endophyte effects root volatile emission and host plant selection of a belowground insect. Oecologia 177:487–497CrossRefPubMedGoogle Scholar
  24. 24.
    Young CA, Hume DE, McCulley RL (2013) Fungal endophytes of tall fescue and perennial ryegrass: pasture friend or foe? J Anim Sci 91:2379–2394CrossRefPubMedGoogle Scholar
  25. 25.
    Bouton JH, Latch G, Hill NS, Hoveland CS, McCann MA, Watson RH, Thompson FN (2002) Reinfection of tall fescue cultivars with non-ergot alkaloid–producing endophytes. Agron J 94:567–574CrossRefGoogle Scholar
  26. 26.
    Hunt MG, Newman JA (2005) Reduced herbivore resistance from a novel grass-endophyte association. J Appl Ecol 42(4):762–769CrossRefGoogle Scholar
  27. 27.
    Belesky DP, Bacon CW (2009) Tall fescue and associated mutualistic toxic fungal endophytes in agroecosystems. Toxin Rev 28:102–117CrossRefGoogle Scholar
  28. 28.
    Iqbal J, Siegrist JA, Nelson JA, McCulley RL (2012) Fungal endophyte infection increases carbon sequestration potential of southeastern USA tall fescue stands. Soil Biol Biochem 44:81–92CrossRefGoogle Scholar
  29. 29.
    Buyer JS, Zuberer DA, Nichols KA, Franzluebbers AJ (2011) Soil microbial community function, structure, and glomalin in response to tall fescue endophyte infection. Plant Soil 339:401–412CrossRefGoogle Scholar
  30. 30.
    Jenkins MB, Franzluebbers AJ, Humayoun SB (2006) Assessing short-term responses of prokaryotic communities in bulk and rhizosphere soils to tall fescue endophyte infection. Plant Soil 289:309–320CrossRefGoogle Scholar
  31. 31.
    Van Hecke MM, Treonis AM, Kaufman JR (2005) How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plant Soil 275:101–109CrossRefGoogle Scholar
  32. 32.
    Handayani IP, Coyne MS, Phillips TD (2011) Soil organic carbon fractions differ in two contrasting tall fescue systems. Plant Soil 338:43–50CrossRefGoogle Scholar
  33. 33.
    Iqbal J, Nelson JA, McCulley RL (2013) Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes. Plant Soil 364:15–27CrossRefGoogle Scholar
  34. 34.
    Guo J (2014) The influence of tall fescue cultivar and endophyte status on root exudate chemistry and rhizosphere processes. Dissertation, University of Kentucky, Lexington, http://uknowledge.uky.edu/pss_etds/50 Google Scholar
  35. 35.
    Hopkins AA, Young CA, Butler TJ, Bouton JH (2011) Registration of ‘Texoma’ MaxQ II tall fescue. J Plant Registrations 5:14–18CrossRefGoogle Scholar
  36. 36.
    Buyer JS, Sasser M (2012) High throughput phospholipid fatty acid analysis of soils. Appl Soil Ecol 61:127–130CrossRefGoogle Scholar
  37. 37.
    Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310CrossRefGoogle Scholar
  38. 38.
    Crowther TW, Maynard DS, Leff JW, Oldfield EE, McCulley RL, Fierer N, Bradford MA (2014) Predicting the responsiveness of soil biodiversity to deforestation: a cross-biome study. Global Change Biol 20:2983–2994CrossRefGoogle Scholar
  39. 39.
    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998CrossRefPubMedGoogle Scholar
  40. 40.
    Ramirez KS, Leff JW, Barberan A, Bates ST, Betley J, Crowther TW, Kelly EF, Oldfield EE, Shaw EA, Steenbock C, Bradford MA, Wall DH, Fierer N (2014) Biogeographic patterns in below-ground diversity in New York City’s Central Park are similar to those observed globally. Royal Proc B 281:20141988CrossRefGoogle Scholar
  41. 41.
    McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Hugenholtz P (2011) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Kõljalg U (2010) The UNITE database for molecular identification of fungi–recent updates and future perspectives. New Phytol 186:281–285CrossRefPubMedGoogle Scholar
  43. 43.
    R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  44. 44.
    Clarke K, Gorley R (2006) PRIMER v6: user manual/tutorialGoogle Scholar
  45. 45.
    Wilson GW, Rice CW, Rillig MC, Springer A, Hartnett DC (2009) Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452–461CrossRefPubMedGoogle Scholar
  46. 46.
    Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  47. 47.
    Chu-Chou M, Guo B, An ZQ, Hendrix JW, Ferriss RS, Siegel MR, Burrus PB (1992) Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biol Biochem 24:633–637CrossRefGoogle Scholar
  48. 48.
    Guo BZ, Hendrix JW, An Z-Q, Ferriss RS (1992) Role of Acremonium endophyte of fescue on inhibition of colonization and reproduction of mycorrhizal fungi. Mycologia 84:882–885CrossRefGoogle Scholar
  49. 49.
    Mack KM, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320CrossRefGoogle Scholar
  50. 50.
    Liu Q, Parsons AJ, Xue H, Fraser K, Ryan GD, Newman JA, Rasmussen S (2011) Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Funct Ecol 25:910–920CrossRefGoogle Scholar
  51. 51.
    Hodge KT (2003) Clavicipitaceous anamorphs. In: White JF, Bacon CW, Hywel-Jones NL, Spatafora JW (eds) Clavicipitalean fungi. Evolutionary biology, chemistry, and biocontrol, and cultural impacts. Marcel-Dekker, New York, pp 75–123Google Scholar
  52. 52.
    Nonaka K, Kaifuchi S, Omura S, Masuma R (2013) Three new Pochonia taxa (Clavicipitaceae) from soils in Japan. Mycologia 105:1202–1218Google Scholar
  53. 53.
    Bacetty AA, Snook ME, Glenn AE, Noe JP, Hill N, Culbreath A, Timper P, Nagabhyru P, Bacon CW (2009) Toxicity of endophyte-infected tall fescue alkaloids and grass metabolites on Pratylenchus scribneri. Nematology 99:1336–1345Google Scholar
  54. 54.
    Behie SW, Bidochka MJ (2014) Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: an additional branch of the soil nitrogen cycle. Appl Environ Microb 80:1553–1560CrossRefGoogle Scholar
  55. 55.
    Roberts P (1999) Rhizoctonia-forming fungi: a taxonomic guide. Herbarium, Royal Botanic Gardens, Surrey, pp. 239Google Scholar
  56. 56.
    Botha A (2011) The importance and ecology of yeasts in soil. Soil Biol Biochem 43:1–8CrossRefGoogle Scholar
  57. 57.
    Babu AG, Kim SW, Yadav DR, Adhikari M, Kim C, Lee HB, Lee YS (2015) A new record of Volutella ciliate isolated from crop field soil in Korea. Mycobiology 43:71–74CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Ogoshi A (1987) Ecology and pathogenicity of anastomosis and intraspecific groups of Rhizoctonia solani Kühn. Annu Rev Phytopathol 25:125–143CrossRefGoogle Scholar
  59. 59.
    Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297CrossRefGoogle Scholar
  60. 60.
    Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569CrossRefGoogle Scholar
  61. 61.
    Wakelin S, Harrison S, Mander C, Dignam B, Rasmussen S, Monk S, Fraser K, O’Callaghan M (In Press) Impacts of endophyte infection of ryegrass on rhizosphere metabolome and microbial community. Crop & Pasture SciGoogle Scholar
  62. 62.
    Roberts EL, Ferraro A (2015) Rhizosphere microbiome selection by Epichloe endophytes of Festuca arundinacea. Plant Soil. doi:  10.1007/s11104-015-2585-3
  63. 63.
    Antunes PM, Miller J, Carvalho LM, Klironomos JN, Newman JA (2008) Even after death the endophytic fungus of Schedonorus phoenix reduces the arbuscular mycorrhizas of other plants. Funct Ecol 22:912–918CrossRefGoogle Scholar
  64. 64.
    Takach JE, Young CA (2014) Alkaloid genotype diversity of tall fescue endophytes. Crop Sci 54:667–678CrossRefGoogle Scholar
  65. 65.
    Panaccione DG, Kotcon JB, Schardl CL, Johnson RD, Morton JB (2006) Ergot alkaloids are not essential for endophytic fungus-associated population suppression of the lesion nematode, Pratylenchus scribneri, on perennial ryegrass. Nematology 8:583–590CrossRefGoogle Scholar
  66. 66.
    Guo J, McCulley RL, McNear DH (2015) Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition. Frontiers in Plant Science, in press.Google Scholar
  67. 67.
    Casas C, Omacini M, Montecchia MS, Correa OS (2011) Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant Soil 340:347–355CrossRefGoogle Scholar
  68. 68.
    Novas MV, Cabral D, Godeas AM (2005) Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis 40:23–30Google Scholar
  69. 69.
    Novas MV, Iannone LJ, Godeas AM, Cabral D (2009) Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass. Mycol Prog 8:75–81CrossRefGoogle Scholar
  70. 70.
    Arachevaleta M, Bacon CW, Hoveland CS, Radcliff DE (1989) Effect of the tall fescue endophyte on plant response to environmental stress. Agron J 81:83–90CrossRefGoogle Scholar
  71. 71.
    Karathanasis AD (1991) Phosphate mineralogy and equilibria in two Kentucky alfisols derived from Ordovician limestones. Soil Sci Soc Am J 55:1774–1782CrossRefGoogle Scholar
  72. 72.
    Ferreira WPM, Priddy TK, Souza DF, Matthews J (2010) Trends in precipitation and air temperature time series in Lexington, KY, USA. ASABE Annu Int Meet 1009768:3–13Google Scholar
  73. 73.
    Varela-Cervero S, Vasar M, Davison J, Barea JM, Opik M, Azcon-Aguilar C (2015) The composition of arbuscular mycorrhizal fungal communities differs among the roots, spores and extraradical mycelia associated with five Mediterranean plant species. Environ Microbiol. doi:  10.1111/1462-2920.12810
  74. 74.
    McCaig AE, Glover LA, Prosser JI (1999) Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures. Appl Environ Microb 65:1721–1730Google Scholar
  75. 75.
    Axelrood PE, Chow ML, Radomski CC, McDermott JM, Davies J (2002) Molecular characterization of bacterial diversity from British Columbia forest soils subjected to disturbance. Can J Microbiol 48:655–674CrossRefPubMedGoogle Scholar
  76. 76.
    Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364CrossRefPubMedGoogle Scholar
  77. 77.
    Minz D, Ofek M, Hadar Y (2013) Plant rhizosphere microbial communities. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, pp 56--84Google Scholar
  78. 78.
    Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Xavier Rojas
    • 1
  • Jingqi Guo
    • 2
    • 3
  • Jonathan W. Leff
    • 1
  • David H. McNearJr.
    • 2
  • Noah Fierer
    • 1
  • Rebecca L. McCulley
    • 2
    • 4
  1. 1.Department of Ecology and Evolutionary Biology, Cooperative Institute for Research in Environmental SciencesUniversity of Colorado at BoulderBoulderUSA
  2. 2.Department of Plant and Soil SciencesUniversity of KentuckyLexingtonUSA
  3. 3.Soil and Crop Nutrient ManagementTexas AgriLife Research and Extension CenterBeaumontUSA
  4. 4.N-222D Ag Science NorthUniversity of KentuckyLexingtonUSA

Personalised recommendations