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Grazing Intensity Rather than Host Plant’s Palatability Shapes the Community of Arbuscular Mycorrhizal Fungi in a Steppe Grassland

  • Environmental Microbiology
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Abstract

Arbuscular mycorrhizal fungi (AMF) are the predominant type of mycorrhizal fungi in roots and rhizosphere soil of grass species worldwide. Grasslands are currently experiencing increasing grazing pressure, but it is not yet clear how grazing intensity and host plant grazing preference by large herbivores interact with soil- and root-associated AMF communities. Here, we tested whether the diversity and community composition of AMF in the roots and rhizosphere soil of two dominant perennial grasses, grazed differently by livestock, change in response to grazing intensity. We conducted a study in a long-term field experiment in which seven levels of field-manipulated grazing intensities were maintained for 13 years in a typical steppe grassland in northern China. We extracted DNA from the roots and rhizosphere soil of two dominant grasses, Leymus chinense (Trin.) Tzvel. and Stipa grandis P. Smirn, with contrasting grazing preference by sheep. AMF DNA from root and soil samples was then subjected to molecular analysis. Our results showed that AMF α-diversity (richness) at the virtual taxa (VT) level varied as a function of grazing intensity. Different VT showed completely different responses along the gradient, one increasing, one decreasing, and others showing no response. Glomeraceae was the most abundant AMF family along the grazing gradient, which fits well with the theory of disturbance tolerance of this group. In addition, sheep-grazing preference for host plants did not explain much of the variation in AMF α-diversity. However, the two grass species exhibited different AMF community composition in their roots and rhizosphere soils. Roots exhibited a lower α-diversity and higher β-diversity within the AMF community than soils. Overall, our results suggest that long-term grazing intensity might have changed the abundance of functionally diverse AMF taxa in favor of those with disturbance-tolerant traits. We suggest our results would be useful in informing the choice of mycorrhizal fungi indicator variables when assessing the impacts of grassland management choices on grassland ecosystem functioning.

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References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  Google Scholar 

  2. Ambrosino ML, Cabello MN, Busso CA, Velázquez MS, Torres YA, Cardillo DS et al (2018) Communities of arbuscular mycorrhizal fungi associated with perennial grasses of different forage quality exposed to defoliation. J Arid Environ 154:61–69

    Article  Google Scholar 

  3. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693

    Article  Google Scholar 

  4. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. In: Babraham Bioinformatics. Babraham Institute, Cambridge. http://www.bioinformatics.babraham.ac.uk/projects/fastqc

  5. Asmelash F, Bekele T, Birhane E (2016) The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Front Microbiol 7:1095

    Article  Google Scholar 

  6. Ba L, Ning J, Wang D, Facelli E, Facelli JM, Yang Y, Zhang L (2012) The relationship between the diversity of arbuscular mycorrhizal fungi and grazing in a meadow steppe. Plant Soil 352:143–156

    Article  CAS  Google Scholar 

  7. Bai G, Bao Y, Du G, Qi Y (2013) Arbuscular mycorrhizal fungi associated with vegetation and soil parameters under rest grazing management in a desert steppe ecosystem. Mycorrhiza 23:289–301

    Article  Google Scholar 

  8. Barton K (2018) MuMIn: multi-model inference. R package version 1.40.4. https://CRAN.R-project.org/package=MuMIn

  9. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    Article  CAS  Google Scholar 

  10. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33(2):261–304

  11. Cavagnaro RA, Pero E, Dudinszky N, Golluscio RA, Grimoldi AA (2019) Under pressure from above: overgrazing decreases mycorrhizal colonization of both preferred and unpreferred grasses in the Patagonian steppe. Fungal Ecol 40:92–97

    Article  Google Scholar 

  12. Chagnon P-L, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491

    Article  CAS  Google Scholar 

  13. Chen Y-L, Zhang X, Ye J-S, Han H-Y, Wan S-Q, Chen B-D (2014) Six-year fertilization modifies the biodiversity of arbuscular mycorrhizal fungi in a temperate steppe in Inner Mongolia. Soil Biol Biochem 69:371–381

    Article  CAS  Google Scholar 

  14. Conant RT (2010) Challenges and Opportunities for Carbon Sequestration in Grassland Systems: A Technical Report on Grassland Management and Climate Change Mitigation’, Integrated Crop Management, 9 (Rome: FAO).

  15. Cottingham KL, Lennon JT, Brown BL (2005) Knowing when to draw the line: designing more informative ecological experiments. Front Ecol Environ 3(3):145–152

  16. Davison J, García de León D, Zobel M, Moora M, Bueno CG, Barceló M et al (2020) Plant functional groups associate with distinct arbuscular mycorrhizal fungal communities. New Phytol 226:1117–1128

    Article  Google Scholar 

  17. Dudinszky N, Cabello MN, Grimoldi AA, Schalamuk S, Golluscio RA (2019) Role of grazing intensity on shaping arbuscular mycorrhizal fungi communities in patagonian semiarid steppes. Rangel Ecol Manage 72:692–699

    Article  Google Scholar 

  18. Ewels P, Magnusson M, Lundin S, Käller M (2016) MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32:3047–3048

    Article  CAS  Google Scholar 

  19. Faggioli VS, Cabello MN, Grilli G, Vasar M, Covacevich F, Öpik M, Environment, (2019) Root colonizing and soil borne communities of arbuscular mycorrhizal fungi differ among soybean fields with contrasting historical land use. J Agriculture, Ecosystems 269:174–182

    Article  Google Scholar 

  20. Faghihinia M, Zou Y, Bai Y, Marrs R, Staddon PL (2020) Seasonal variation in the response of arbuscular mycorrhizal fungi to grazing intensity. Mycorrhiza 30:635–646

    Article  CAS  Google Scholar 

  21. Faghihinia M, Zou Y, Chen Z, Bai Y, Li W, Marrs R, Staddon PL (2020) The response of grassland mycorrhizal fungal abundance to a range of long-term grazing intensities. Rhizosphere 13:100178

    Article  Google Scholar 

  22. Faghihinia M, Zou Y, Chen Z, Bai Y, Li W, Marrs R, Staddon PL (2020) Environmental drivers of grazing effects on arbuscular mycorrhizal fungi in grasslands. Applied Soil Ecology 153:103591

    Article  Google Scholar 

  23. González JB, Petipas RH, Franken O, Kiers ET, Veblen KE, Brody AK (2018) Herbivore removal reduces influence of arbuscular mycorrhizal fungi on plant growth and tolerance in an East African savanna. Oecologia 187:123–133

    Article  Google Scholar 

  24. Guo Y, Du Q, Li G, Ni Y, Zhang Z, Ren W, Hou X (2016) Soil phosphorus fractions and arbuscular mycorrhizal fungi diversity following long-term grazing exclusion on semi-arid steppes in Inner Mongolia. Geoderma 269:79–90

    Article  CAS  Google Scholar 

  25. Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344

    Article  Google Scholar 

  26. Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938

    Article  CAS  Google Scholar 

  27. Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci 107:2093–2098

    Article  CAS  Google Scholar 

  28. Kreyling J, Schweiger AH, Bahn M, Ineson P, Migliavacca M, Morel‐Journel T, Christiansen JR, Schtickzelle N, Larsen KS (2018) To replicate, or not to replicate–that is the question: how to tackle nonlinear responses in ecological experiments. Ecol Lett 21(11):1629–1638

  29. Kusakabe R, Taniguchi T, Goomaral A, Undarmaa J, Yamanaka N, Yamato M (2018) Arbuscular mycorrhizal fungal communities under gradients of grazing in Mongolian grasslands of different aridity. Mycorrhiza 28:621–634

    Article  Google Scholar 

  30. Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  CAS  Google Scholar 

  31. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  32. Li S, Shakoor A, Wubet T, Zhang N, Liang Y, Ma K (2018) Fine-scale variations of fungal community in a heterogeneous grassland in Inner Mongolia: Effects of the plant community and edaphic parameters. Soil Biol Biochem 122:104–110

    Article  CAS  Google Scholar 

  33. Li W, Xu F, Zheng S, Taube F, Bai Y (2017) Patterns and thresholds of grazing-induced changes in community structure and ecosystem functioning: species-level responses and the critical role of species traits. J Appl Ecol 54:963–975

    Article  Google Scholar 

  34. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet journal 17:10–12

    Article  Google Scholar 

  35. Martínez-García LB, Richardson SJ, Tylianakis JM, Peltzer DA, Dickie IA (2015) Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development. New Phytol 205:1565–1576

    Article  Google Scholar 

  36. Mendoza R, Cabello M, Anchorena J, García I, Marbán L (2011) Soil parameters and host plants associated with arbuscular mycorrhizae in the grazed Magellanic steppe of Tierra del Fuego. Agr Ecosyst Environ 140:411–418

    Article  Google Scholar 

  37. Moora M, Zobel M (2010) Arbuscular mycorrhizae and plant-plant interactions. Positive plant interactions and community dynamics, pp 79–98

  38. Murray TR, Frank DA, Gehring CA (2010) Ungulate and topographic control of arbuscular mycorrhizal fungal spore community composition in a temperate grassland. Ecology 91:815–827

    Article  Google Scholar 

  39. O’Mara FP (2012) The role of grasslands in food security and climate change. Ann Bot 110:1263–1270

    Article  CAS  Google Scholar 

  40. Oehl F, Sieverding E, Ineichen K, Maeder P, Wiemken A, Boller T (2009) Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agr Ecosyst Environ 134:257–268

    Article  Google Scholar 

  41. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2018) nlme: linear and nonlinear mixed effects models. R package version 3.1-137. https://CRAN.R-project.org/package=nlme

  42. R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  43. Ren H, Eviner VT, Gui W, Wilson GW, Cobb AB, Yang G et al (2018) Livestock grazing regulates ecosystem multifunctionality in semi-arid grassland. Funct Ecol 32:2790–2800

    Article  Google Scholar 

  44. Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. J PeerJ 4:e2584

    Article  Google Scholar 

  45. Sato K, Suyama Y, Saito M, Sugawara K (2005) A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassland Sci 51:179–181

    Article  CAS  Google Scholar 

  46. Sepp SK, Davison J, Jairus T, Vasar M, Moora M, Zobel M, Öpik M (2019) Non-random association patterns in a plant–mycorrhizal fungal network reveal host–symbiont specificity. Mol Ecol 28:365–378

    Article  CAS  Google Scholar 

  47. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic press, San Diego

    Google Scholar 

  48. Staddon PL, Ramsey CB, Ostle N, Ineson P, Fitter AH (2003) Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of 14C. Science 300:1138–1140

    Article  CAS  Google Scholar 

  49. Stevens BM, Propster JR, Öpik M, Wilson GW, Alloway SL, Mayemba E, Johnson NC, (2020) Arbuscular mycorrhizal fungi in roots and soil respond differently to biotic and abiotic factors in the Serengeti. Mycorrhiza 30(1):79–95

  50. Stover HJ, Naeth MA, Boldt-Burisch K (2018) Soil disturbance changes arbuscular mycorrhizal fungi richness and composition in a fescue grassland in Alberta Canada. Appl Soil Ecol 131:29–37

    Article  Google Scholar 

  51. Vályi K, Rillig MC, Hempel S (2015) Land-use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants. New Phytol 205:1577–1586

    Article  Google Scholar 

  52. van der Heyde M, Bennett JA, Pither J, Hart M (2017) Longterm effects of grazing on arbuscular mycorrhizal fungi. Agr Ecosyst Environ 243:27–33

    Article  Google Scholar 

  53. van der Heyde M, Ohsowski B, Abbott LK, Hart M (2017) Arbuscular mycorrhizal fungus responses to disturbance are context-dependent. Mycorrhiza 27:431–440

    Article  Google Scholar 

  54. van der Heyde M, Abbott LK, Gehring C, Kokkoris V, Hart MM (2019) Reconciling disparate responses to grazing in the arbuscular mycorrhizal symbiosis. Rhizosphere 11:100167

  55. Větrovský T, Baldrian P (2013) Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biol Fertil Soils 49:1027–1037

    Article  Google Scholar 

  56. Wang Q, Bao Y, Liu X, Du G (2014) Spatio-temporal dynamics of arbuscular mycorrhizal fungi associated with glomalin-related soil protein and soil enzymes in different managed semiarid steppes. Mycorrhiza 24:525–538

    Article  CAS  Google Scholar 

  57. Yan L, Zhou G, Zhang F (2013) Effects of different grazing intensities on grassland production in China: a meta-analysis. PLoS One 8:e81466

    Article  Google Scholar 

  58. Yang X, Chen J, Shen Y, Dong F, Chen J (2020) Global negative effects of livestock grazing on arbuscular mycorrhizas: a meta-analysis. Sci Total Environ 708:134553

    Article  CAS  Google Scholar 

  59. Zhu L (2005) Monte Carlo Tests. In: Zhu L (ed) Nonparametric Monte Carlo Tests and Their Applications. Springer New York, New York, pp 1–9

    Google Scholar 

  60. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects modelling for nested data. In: Mixed effects models and extensions in ecology with R. Springer, New York, NY, pp 101–142

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Acknowledgements

We acknowledge the kind cooperation of the staff in the Inner Mongolia Grassland Ecosystem Research Station (IMGERS) led by Chinese Academy of Sciences to provide equipment and facilities. Particular thanks to our research team Chuanyu Zhou, Zirui Hu, Ye Wang, Hanyu Jian, Shasha Zou, Fanjing Liu and Yuwei He for their collaborative effort during data collection.

Funding

This work has been funded by the Xian-Jiatong-Liverpool University Research Development Fund (RDF-15-02-13).

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Authors and Affiliations

  1. Department of Health and Environmental Sciences, Xi’an Jiaotong-Liverpool University, Suzhou, 215123, Jiangsu, China

    Maede Faghihinia, Yi Zou & Philip L. Staddon

  2. School of Environmental Sciences, University of Liverpool, Liverpool, L69 3GP, UK

    Maede Faghihinia & Rob Marrs

  3. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Yongfei Bai

  4. Institute of Microbiology, Academy of Sciences of the Czech Republic, Vídeňská 1083 Praha 4 - Krč, Prague, Czech Republic

    Martin Dudáš

  5. Countryside and Community Research Institute, University of Gloucestershire, Cheltenham, GL50 4AZ, UK

    Philip L. Staddon

  6. School for Agriculture, Food and the Environment, Royal Agricultural University, Cirencester, GL7 6JS, UK

    Philip L. Staddon

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  1. Maede Faghihinia
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  2. Yi Zou
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Correspondence to Yi Zou.

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Faghihinia, M., Zou, Y., Bai, Y. et al. Grazing Intensity Rather than Host Plant’s Palatability Shapes the Community of Arbuscular Mycorrhizal Fungi in a Steppe Grassland. Microb Ecol 84, 1062–1071 (2022). https://doi.org/10.1007/s00248-021-01920-7

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