Location, Root Proximity, and Glyphosate-Use History Modulate the Effects of Glyphosate on Fungal Community Networks of Wheat

Abstract

Glyphosate is the most-used herbicide worldwide and an essential tool for weed control in no-till cropping systems. However, concerns have been raised regarding the long-term effects of glyphosate on soil microbial communities. We examined the impact of repeated glyphosate application on bulk and rhizosphere soil fungal communities of wheat grown in four soils representative of the dryland wheat production region of Eastern Washington, USA. Further, using soils from paired fields, we contrasted the response of fungal communities that had a long history of glyphosate exposure and those that had no known exposure. Soil fungal communities were characterized after three cycles of wheat growth in the greenhouse followed by termination with glyphosate or manual clipping of plants. We found that cropping system, location, year, and root proximity were the primary drivers of fungal community compositions, and that glyphosate had only small impacts on fungal community composition or diversity. However, the taxa that responded to glyphosate applications differed between rhizosphere and bulk soil and between cropping systems. Further, a greater number of fungal OTUs responded to glyphosate in soils with a long history of glyphosate use. Finally, fungal co-occurrence patterns, but not co-occurrence network characteristics, differed substantially between glyphosate-treated and non-treated communities. Results suggest that most fungi influenced by glyphosate are saprophytes that likely feed on dying roots.

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References

  1. 1.

    Frey S, Elliott E, Paustian K (1999) Bacterial and fungal abundance and biomass in conventional and no-tillage agroecosystems along two climatic gradients. Soil Biol Biochem 31:573–585. https://doi.org/10.1016/S0038-0717(98)00161-8

    Article  CAS  Google Scholar 

  2. 2.

    Peay KG, Kennedy PG, Talbot JM (2016) Dimensions of biodiversity in the Earth mycobiome. Nat Rev Microbiol 14:434–447. https://doi.org/10.1038/nrmicro.2016.59

    Article  PubMed  CAS  Google Scholar 

  3. 3.

    Schappe T, Albornoz FE, Turner BL et al (2017) The role of soil chemistry and plant neighbourhoods in structuring fungal communities in three Panamanian rainforests. J Ecol 105:569–579. https://doi.org/10.1111/1365-2745.12752

    Article  Google Scholar 

  4. 4.

    Sharma-Poudyal D, Schlatter D, Yin C et al (2017) Long-term no-till: a major driver of fungal communities in dryland wheat cropping systems. PLoS One 12:e0184611. https://doi.org/10.1371/journal.pone.0184611

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. 5.

    Huggins DR, Reganold JP (2008) No-till: the quiet revolution. Sci Am 299:70–77

    Article  PubMed  Google Scholar 

  6. 6.

    Benbrook CM (2016) Trends in glyphosate herbicide use in the United States and globally. Environ Sci Eur. https://doi.org/10.1186/s12302-016-0070-0

  7. 7.

    Bockus WW, Wiese MV (2010) Compendium of wheat diseases and pests. 3rd ed. APS Press, St. Paul

  8. 8.

    Duke SO, Lydon J, Koskinen WC et al (2012) Glyphosate effects on plant mineral nutrition, crop rhizosphere microbiota, and plant disease in glyphosate-resistant crops. J Agric Food Chem 60:10375–10397. https://doi.org/10.1021/jf302436u

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. 9.

    Borggaard OK, Gimsing AL (2008) Fate of glyphosate in soil and the possibility of leaching to ground and surface waters: a review. Pest Manag Sci 64:441–456. https://doi.org/10.1002/ps.1512

    Article  PubMed  CAS  Google Scholar 

  10. 10.

    Zobiole LHS, Kremer RJ, Oliveira RS, Constantin J (2011) Glyphosate affects micro-organisms in rhizospheres of glyphosate-resistant soybeans: glyphosate affects micro-organisms in rhizospheres. J Appl Microbiol 110:118–127. https://doi.org/10.1111/j.1365-2672.2010.04864.x

    Article  PubMed  CAS  Google Scholar 

  11. 11.

    Kremer RJ, Means NE (2009) Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms. Eur J Agron 31:153–161. https://doi.org/10.1016/j.eja.2009.06.004

    Article  CAS  Google Scholar 

  12. 12.

    Tanney JB, Hutchison LJ (2010) The effects of glyphosate on the in vitro linear growth of selected microfungi from a boreal forest soil. Can J Microbiol 56:138–144. https://doi.org/10.1139/W09-122

    Article  PubMed  CAS  Google Scholar 

  13. 13.

    Sailaja KK, Satyaprasad K (2006) Degradation of glyphosate in soil and its effect on fungal population. J Environ Sci Eng 48:189–190

    PubMed  CAS  Google Scholar 

  14. 14.

    Massalha H, Korenblum E, Tholl D, Aharoni A (2017) Small molecules below-ground: the role of specialized metabolites in the rhizosphere. Plant J 90:788–807. https://doi.org/10.1111/tpj.13543

    Article  PubMed  CAS  Google Scholar 

  15. 15.

    Hammerschmidt R (2017) How glyphosate affects plant disease development: it is more than enhanced susceptibility: glyphosate and plant disease. Pest Manag Sci. https://doi.org/10.1002/ps.4521

  16. 16.

    Lévesque CA, Rahe JE (1992) Herbicide interactions with fungal root pathogens, with special reference to glyphosate. Annu Rev Phytopathol 30:579–602. https://doi.org/10.1146/annurev.py.30.090192.003051

    Article  PubMed  Google Scholar 

  17. 17.

    Babiker EM, Hulbert SH, Schroeder KL, Paulitz TC (2011) Optimum timing of preplant applications of glyphosate to manage Rhizoctonia root rot in barley. Plant Dis 95:304–310. https://doi.org/10.1094/PDIS-05-10-0354

    Article  Google Scholar 

  18. 18.

    Bakker MG, Moorman TB, Kaspar TC, Manter DK (2017) Isolation of cultivation-resistant Oomycetes, first detected as amplicon sequences, from roots of herbicide-terminated winter rye. Phytobiomes 1:24–35. https://doi.org/10.1094/PBIOMES-10-16-0011-R

    Article  Google Scholar 

  19. 19.

    Nye M, Hoilett N, Ramsier C et al (2014) Microbial community structure in soils amended with glyphosate-tolerant soybean residue. Appl Ecol Environ Sci 2:74–81. 10.12691/aees-2-3-1

    Article  Google Scholar 

  20. 20.

    Lane M, Lorenz N, Saxena J et al (2012) The effect of glyphosate on soil microbial activity, microbial community structure, and soil potassium. Pedobiologia 55:335–342. https://doi.org/10.1016/j.pedobi.2012.08.001

    Article  CAS  Google Scholar 

  21. 21.

    Zabaloy MC, Gómez E, Garland JL, Gómez MA (2012) Assessment of microbial community function and structure in soil microcosms exposed to glyphosate. Appl Soil Ecol 61:333–339. https://doi.org/10.1016/j.apsoil.2011.12.004

    Article  Google Scholar 

  22. 22.

    Lancaster SH, Hollister EB, Senseman SA, Gentry TJ (2010) Effects of repeated glyphosate applications on soil microbial community composition and the mineralization of glyphosate. Pest Manag Sci 66:59–64. https://doi.org/10.1002/ps.1831

    Article  PubMed  CAS  Google Scholar 

  23. 23.

    Sviridov AV, Shushkova TV, Ermakova IT et al (2015) Microbial degradation of glyphosate herbicides (review). Appl Biochem Microbiol 51:188–195. https://doi.org/10.1134/S0003683815020209

    Article  CAS  Google Scholar 

  24. 24.

    Newman MM, Hoilett N, Lorenz N et al (2016) Glyphosate effects on soil rhizosphere-associated bacterial communities. Sci Total Environ 543:155–160. https://doi.org/10.1016/j.scitotenv.2015.11.008

    Article  PubMed  CAS  Google Scholar 

  25. 25.

    Druille M, García-Parisi PA, Golluscio RA et al (2016) Repeated annual glyphosate applications may impair beneficial soil microorganisms in temperate grassland. Agric Ecosyst Environ 230:184–190. https://doi.org/10.1016/j.agee.2016.06.011

    Article  CAS  Google Scholar 

  26. 26.

    Cherni AE, Trabelsi D, Chebil S et al (2015) Effect of glyphosate on enzymatic activities, Rhizobiaceae and total bacterial communities in an agricultural Tunisian soil. Water Air Soil Pollut. https://doi.org/10.1007/s11270-014-2263-8

  27. 27.

    Weaver MA, Krutz LJ, Zablotowicz RM, Reddy KN (2007) Effects of glyphosate on soil microbial communities and its mineralization in a Mississippi soil. Pest Manag Sci 63:388–393. https://doi.org/10.1002/ps.1351

    Article  PubMed  CAS  Google Scholar 

  28. 28.

    Hart MM, Powell JR, Gulden RH et al (2009) Separating the effect of crop from herbicide on soil microbial communities in glyphosate-resistant corn. Pedobiologia 52:253–262. https://doi.org/10.1016/j.pedobi.2008.10.005

    Article  CAS  Google Scholar 

  29. 29.

    Ratcliff AW, Busse MD, Shestak CJ (2006) Changes in microbial community structure following herbicide (glyphosate) additions to forest soils. Appl Soil Ecol 34:114–124. https://doi.org/10.1016/j.apsoil.2006.03.002

    Article  Google Scholar 

  30. 30.

    Barriuso J, Marín S, Mellado RP (2011) Potential accumulative effect of the herbicide glyphosate on glyphosate-tolerant maize rhizobacterial communities over a three-year cultivation period. PLoS One 6:e27558. https://doi.org/10.1371/journal.pone.0027558

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. 31.

    Imparato V, Santos SS, Johansen A et al (2016) Stimulation of bacteria and protists in rhizosphere of glyphosate-treated barley. Appl Soil Ecol 98:47–55. https://doi.org/10.1016/j.apsoil.2015.09.007

    Article  Google Scholar 

  32. 32.

    Mijangos I, Becerril JM, Albizu I et al (2009) Effects of glyphosate on rhizosphere soil microbial communities under two different plant compositions by cultivation-dependent and -independent methodologies. Soil Biol Biochem 41:505–513. https://doi.org/10.1016/j.soilbio.2008.12.009

    Article  CAS  Google Scholar 

  33. 33.

    Haney RL, Senseman SA, Hons FM, Zuberer DA (2000) Effect of glyphosate on soil microbial activity and biomass. Weed Sci 48:89–93. https://doi.org/10.1614/0043-1745(2000)048[0089:EOGOSM]2.0.CO;2

    Article  CAS  Google Scholar 

  34. 34.

    Sheng M, Hamel C, Fernandez MR (2012) Cropping practices modulate the impact of glyphosate on arbuscular mycorrhizal fungi and rhizosphere bacteria in agroecosystems of the semiarid prairie. Can J Microbiol 58:990–1001. https://doi.org/10.1139/w2012-080

    Article  PubMed  CAS  Google Scholar 

  35. 35.

    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  PubMed  CAS  Google Scholar 

  36. 36.

    White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protoc. Guide Mehtods Appl. Academic Press, New York, pp 315–322

    Google Scholar 

  37. 37.

    Nguyen NH, Smith D, Peay K, Kennedy P (2015) Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol 205:1389–1393. https://doi.org/10.1111/nph.12923

    Article  PubMed  CAS  Google Scholar 

  38. 38.

    Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics 30:614–620. https://doi.org/10.1093/bioinformatics/btt593

    Article  PubMed  CAS  Google Scholar 

  39. 39.

    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604

    Article  PubMed  CAS  Google Scholar 

  40. 40.

    Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. Peer J 4:e2584. https://doi.org/10.7717/peerj.2584

    Article  PubMed  Google Scholar 

  41. 41.

    Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. 42.

    Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349. https://doi.org/10.2307/1942268

    Article  Google Scholar 

  43. 43.

    Oksanen J, Blanchette FG, Friendly M, et al (2016) Vegan: community ecology package

  44. 44.

    Shannon CE, Weaver W (1975) The mathematical theory of communication. University of Illinois Press, Urbana

    Google Scholar 

  45. 45.

    Simpson EH (1949) Measurement of diversity. Nature 163:688–688. https://doi.org/10.1038/163688a0

    Article  Google Scholar 

  46. 46.

    Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. https://doi.org/10.1186/s13059-014-0550-8

  47. 47.

    Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput Biol 8:e1002687. https://doi.org/10.1371/journal.pcbi.1002687

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. 48.

    Kurtz ZD, Müller CL, Miraldi ER et al (2015) Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol 11:e1004226. https://doi.org/10.1371/journal.pcbi.1004226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. 49.

    Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695

  50. 50.

    Humphries MD, Gurney K (2008) Network “small-world-ness”: a quantitative method for determining canonical network equivalence. PLoS One 3:e0002051. https://doi.org/10.1371/journal.pone.0002051

    Article  PubMed  CAS  Google Scholar 

  51. 51.

    Kleinberg JM (1999) Authoritative sources in a hyperlinked environment. J ACM 46:604–632. https://doi.org/10.1145/324133.324140

    Article  Google Scholar 

  52. 52.

    Wardle DA, Parkinson D (1990) Influence of the herbicide glyphosate on soil microbial community structure. Plant Soil 122:29–37. https://doi.org/10.1007/BF02851907

    Article  CAS  Google Scholar 

  53. 53.

    Krzysko-Lupicka T, Sudol T (2008) Interactions between glyphosate and autochthonous soil fungi surviving in aqueous solution of glyphosate. Chemosphere 71:1386–1391. https://doi.org/10.1016/j.chemosphere.2007.11.006

    Article  PubMed  CAS  Google Scholar 

  54. 54.

    Castro JV, Peralba MCR, Ayub MAZ (2007) Biodegradation of the herbicide glyphosate by filamentous fungi in platform shaker and batch bioreactor. J Environ Sci Health Part B 42:883–886. https://doi.org/10.1080/03601230701623290

    Article  CAS  Google Scholar 

  55. 55.

    Sharma U (1989) Effect of glyphosate herbicide on pseudothecia formation by Pyrenophora tritici-repentis in infested wheat straw. Plant Dis 73:647. https://doi.org/10.1094/PD-73-0647

    Article  CAS  Google Scholar 

  56. 56.

    Fernandez MR, Zentner RP, Basnyat P et al (2009) Glyphosate associations with cereal diseases caused by Fusarium spp. in the Canadian prairies. Eur J Agron 31:133–143. https://doi.org/10.1016/j.eja.2009.07.003

    Article  CAS  Google Scholar 

  57. 57.

    Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. 1st edn. Blackwell Pub, Ames

  58. 58.

    Hibbett D, Abarenkov K, Kõljalg U et al (2016) Sequence-based classification and identification of fungi. Mycologia 108:1049–1068. https://doi.org/10.3852/16-130

    PubMed  Article  Google Scholar 

  59. 59.

    Shrestha P, Szaro TM, Bruns TD, Taylor JW (2011) Systematic search for cultivatable fungi that best deconstruct cell walls of Miscanthus and sugarcane in the field. Appl Environ Microbiol 77:5490–5504. https://doi.org/10.1128/AEM.02996-10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. 60.

    Meriles JM, Vargas Gil S, Haro RJ, et al (2006) Glyphosate and previous crop residue effect on deleterious and beneficial soil-borne fungi from a peanut-corn-soybean rotations

  61. 61.

    Bachelot B, Uriarte M, Zimmerman JK et al (2016) Long-lasting effects of land use history on soil fungal communities in second-growth tropical rain forests. Ecol Appl 26:1881–1895. https://doi.org/10.1890/15-1397.1

    Article  PubMed  Google Scholar 

  62. 62.

    Schlatter DC, Yin C, Hulbert S et al (2017) Impacts of repeated glyphosate use on wheat-associated bacteria are small and depend on glyphosate-use history. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01354-17

  63. 63.

    Zaller JG, Heigl F, Ruess L, Grabmaier A (2015) Glyphosate herbicide affects belowground interactions between earthworms and symbiotic mycorrhizal fungi in a model ecosystem. Sci Rep. https://doi.org/10.1038/srep05634

  64. 64.

    Watts DJ, Strogatz SH (1998) Collective dynamics of “small-world” networks. Nature 393:440–442. https://doi.org/10.1038/30918

    Article  PubMed  CAS  Google Scholar 

  65. 65.

    Barabási A-L, Oltvai ZN (2004) Network biology: understanding the cell’s functional organization. Nat Rev Genet 5:101–113. https://doi.org/10.1038/nrg1272

    Article  PubMed  CAS  Google Scholar 

  66. 66.

    Poudel R, Jumpponen A, Schlatter DC et al (2016) Microbiome networks: a systems framework for identifying candidate microbial assemblages for disease management. Phytopathology 106:1083–1096. https://doi.org/10.1094/PHYTO-02-16-0058-FI

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Timothy Paulitz.

Electronic supplementary material

Supplemental Figure 1

Networks of both positive (blue edges) and negative (red edges) (GIF 198 kb)

High resolution image (TIFF 355 kb)

Supplemental Figure 2

Networks of both positive (blue edges) and negative (red edges) associations in rhizosphere soil. Nodes (OTUs) are colored by the phyla to which they were classified. (GIF 207 kb)

High resolution image (TIFF 444 kb)

Supplemental Figure 3

Networks of positive co-associations in bulk soil as described in Figure 8, with nodes labeled with OTU identifiers. (GIF 258 kb)

High resolution image (TIFF 327 kb)

Supplemental Figure 4

Networks of negative co-associations in bulk soil with nodes labeled with OTU identifiers. Edges specific to each network are colored red where those shared between networks in the same cropping system are colored gray. Nodes are colored by the module to which they belong in the corresponding NG network. (GIF 219 kb)

High resolution image (TIFF 461 kb)

Supplemental Figure 5

Networks of positive co-associations in rhizosphere soil as described in Figure 9, with nodes labeled with OTU identifiers. (GIF 296 kb)

High resolution image (TIFF 1.00 MB)

Supplemental Figure 6

Networks of negative co-associations in rhizosphere soil with nodes labeled with OTU identifiers. Edges in specific to each network are colored red where those shared between networks in the same cropping system are colored gray. Nodes are colored by the module to which they belong in the corresponding NG network. (GIF 290 kb)

High resolution image (TIFF 854 kb)

Supplemental Table 1

Soil analyses of locations. (XLSX 1.50 MB)

Supplemental Table 2

Forward and reverse primer designs for ITS illumina sequencing. (DOCX 13 kb)

Supplemental Table 3

ANOVA F-statistics and p-values for fungal richness and diversity indices among treatments in 2015 and 2016. (DOCX 14 kb)

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Schlatter, D.C., Yin, C., Burke, I. et al. Location, Root Proximity, and Glyphosate-Use History Modulate the Effects of Glyphosate on Fungal Community Networks of Wheat. Microb Ecol 76, 240–257 (2018). https://doi.org/10.1007/s00248-017-1113-9

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Keywords

  • Glyphosate
  • Fungi
  • Networks
  • Wheat
  • Triticum aestivum
  • Microbiome