Advertisement

Mycorrhiza

, Volume 28, Issue 7, pp 621–634 | Cite as

Arbuscular mycorrhizal fungal communities under gradients of grazing in Mongolian grasslands of different aridity

  • Ryota Kusakabe
  • Takeshi Taniguchi
  • Altansukh Goomaral
  • Jamsran Undarmaa
  • Norikazu Yamanaka
  • Masahide Yamato
Original Article
  • 223 Downloads

Abstract

Communities of arbuscular mycorrhizal (AM) fungi in Mongolian grassland were characterized under gradients of grazing intensity at three study sites of different aridity: mountain forest steppe at Hustai National Park (Hustai), and desert steppe at Mandalgovi and Bulgan. Grazing intensity was classified into three categories: lightly grazed (LG), moderately grazed (MG), and heavily grazed (HG). With regard to floristic composition, grazing decreased the shoot biomass of Poaceae species, especially Stipa spp. Distinctness of the AM fungal communities was observed among the three study sites, but most of the AM fungal operational taxonomic units (OTUs) that comprised over 1.0% of the total reads were ubiquitous. This result indicates that the AM fungal communities may be derived from similar AM fungal floras in correspondence with environmental factors. The composition of AM fungal communities differed significantly among the grazing intensities at all study sites. The relative abundance of the most dominant AM fungal OTU of the LG plots decreased with an increase in grazing intensity at all study sites. The mean proportions of the most dominant AM fungal OTUs also decreased with increased grazing intensity at Hustai. Dominance by a single AM fungal taxon may be a typical ecological feature of the AM fungal symbiosis, and grazing disturbs AM fungal community structure.

Keywords

Dryland Glomeraceae Glomeromycotina SSU rDNA Steppe Stipa 

Notes

Acknowledgements

Mongolian soil and plant samples used for the analysis were transported to Japan with the permission of the General Agency for Specialized Inspection, Mineral Resource Authority, Ministry of Environment and Tourism in Mongolia, and the Plant Protection Station, Ministry of Agriculture, Forestry and Fisheries in Japan. This study was supported by a Grant-in-Aid for Scientific Research (26304046) from the Ministry of Education, Culture, Sports, Science, and Technology, Japan, and the Joint Research Program of Arid Land Research Center, Tottori University (2014-2015). We thank Robert McKenzie, PhD, from Edanz Group (www.edanzediting.com/ac), for editing a draft of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

572_2018_855_Fig5_ESM.png (97 kb)
Fig. S1

Rarefaction curves of arbuscular mycorrhizal fungal OTUs against the number of reads after rarefication to 1000 reads per sample in each root sample of the three grazing intensities, lightly grazed (LG; Green), moderately grazed (MG; Blue), and heavily grazed (HG; Red) at three study site, a) Hustai, b) Mandalgovi, and c) Bulgan (PNG 96 kb)

572_2018_855_MOESM1_ESM.tif (15.8 mb)
High resolution image (TIF 16177 kb)
572_2018_855_MOESM2_ESM.xlsx (50 kb)
Table S1 (XLSX 50 kb)
572_2018_855_MOESM3_ESM.xlsx (41 kb)
Table S2 (XLSX 40 kb)
572_2018_855_MOESM4_ESM.xlsx (42 kb)
Table S3 (XLSX 42 kb)
572_2018_855_MOESM5_ESM.xlsx (38 kb)
Table S4 (XLSX 37 kb)

References

  1. Allen MF, Richards JH, Busso CA (1989) Influence of clipping and soil water status on vesicular-arbuscular mycorrhizae of twosemi-arid tussock grasses. Biol Fertil Soils 8:285–289CrossRefGoogle Scholar
  2. Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19:5555–5556CrossRefGoogle Scholar
  3. An GH, Miyakawa S, Kawahara A, Osaki M, Ezawa T (2008) Community structure of arbuscular mycorrhizal fungi associated with pioneer grass species Miscanthus sinensis in acid sulfate soils: habitat segregation along pH gradients. Soil Sci Plant Nutr 54:517–528CrossRefGoogle Scholar
  4. 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 352:143–156CrossRefGoogle Scholar
  5. 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 23:289–301CrossRefGoogle Scholar
  6. Bethlenfalvay GJ, Dakessian S (1984) Grazing effects on mycorrhizal colonization and floristic composition of the vegetation on semiarid range in Northern Nevada. J Range Manag 37:312–316CrossRefGoogle Scholar
  7. Bethlenfalvay GJ, Evans RA, Lesperance AL (1985) Mycorrhizal colonization of crested wheatgrass as influenced by grazing. Agron J 77:233–236CrossRefGoogle Scholar
  8. Bever JD, Morton JB, Antonovics J, Schultz PA (1996) Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J Ecol 84:71–82CrossRefGoogle Scholar
  9. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Pena A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  10. Chagnon PL, Bainard LD (2014) Is root DNA a reliable proxy to assess arbuscular mycorrhizal community structure? Can J Microbiol 60:619–624CrossRefGoogle Scholar
  11. de Caritat P, Cooper M, Wilford J (2011) The pH of Australian soils: field results from a national survey. Soil Res 49:173–182CrossRefGoogle Scholar
  12. Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fiter AH (2010) Idiosyncrasy and overdominance in the structure of natural communities of arbuscular mycorrhizal fungi: is there a role for stochastic process? J Ecol 98:419–428CrossRefGoogle Scholar
  13. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefGoogle Scholar
  14. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefGoogle Scholar
  15. Eom AH, Wilson GWT, Hartnett DC (2001) Effects of ungulate grazers on arbuscular mycorrhizal symbiosis and fungal community structure in tallgrass prairie. Mycologia 93:233–242CrossRefGoogle Scholar
  16. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  17. Goomaral A, Iwase K, Undarmaa J, Matsumoto T, Yamato M (2013a) Communities of arbuscular mycorrhizal fungi in Stipa krylovii (Poaceae) in the Mongolian steppe. Mycoscience 54:122–129CrossRefGoogle Scholar
  18. Goomaral A, Undarmaa J, Matsumoto T, Yamato M (2013b) Effect of plant species on communities of arbuscular mycorrhizal fungi in the Mongolian steppe. Mycoscience 54:362–367CrossRefGoogle Scholar
  19. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers allow hundreds of samples to be pyrosequenced in multiplex. Nat Methods 5:235–237CrossRefGoogle Scholar
  20. Haynes RJ, Williams PH (1992) Changes in soil solution composition and pH in urine-affected areas of pasture. Eur J Soil Sci 43:323–324CrossRefGoogle Scholar
  21. Hiiesalu I, Pärtel M, Davison J, Gerhold P, Metsis M, Moora M, Öpik M, Vasar M, Zobel M, Wilson SD (2014) Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytol 203:233–244CrossRefGoogle Scholar
  22. Jigjidsuren S, Johnson DA (2003) Forage plants of Mongolia. Admon Publishing, UlaanbaatarGoogle Scholar
  23. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882CrossRefGoogle Scholar
  24. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  25. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  26. Lugo MA, Maza MWG, Cabello MN (2003) Arbuscular mycorrhizal fungi in a mountain grassland II: seasonal variation of colonization studied, along with its relation to grazing and metabolic host type. Mycologia 95:407–415CrossRefGoogle Scholar
  27. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748CrossRefGoogle Scholar
  28. Medina-Roldán E, Arredondo JT, Huber-Sannwald E, Chapa-Vargas L, Olalde-Portugal V (2008) Grazing effects on fungal root symbionts and carbon and nitrogen storage in a shortgrass steppe in Central Mexico. J Arid Environ 72:546–556CrossRefGoogle Scholar
  29. Oksanen J, Blanachet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens HH, Szoecs E, Wagner H (2017) Package ‘vegan’ community ecology package version 2.4–4 (https://cran.ism.ac.jp/web/packages/vegan/vegan.pdf)
  30. Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Rejer Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241CrossRefGoogle Scholar
  31. Pringle A, Bever JD (2008) Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field. New Phytol 180:162–175CrossRefGoogle Scholar
  32. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:404–425Google Scholar
  33. Sasaki T, Okayasu T, Takeuchi K, Undarmaa J, Jadambaa S (2005) Patterns of floristic composition under different grazing intensities in Bulgan, South Gobi, Mongolia. Grassl Sci 51:235–241CrossRefGoogle Scholar
  34. Sasaki T, Okayasu T, Shirato Y, Undarmaa J, Okubo S, Takeuchi K (2008) Can edaphic factors demonstrate landscape-scale differences in vegetation responses to grazing? Plant Ecol 194:51–66CrossRefGoogle Scholar
  35. 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 electrophorsis. Grassl Sci 51:179–181CrossRefGoogle Scholar
  36. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New YorkGoogle Scholar
  37. Su YY, Guo LD (2007) Arbuscular mycorrhizal fungi in non-grazed, restored and over-graed grassland in the Inner Mongolia steppe. Mycorrhiza 17:689–693CrossRefGoogle Scholar
  38. Tester M, Smith SE, Smith FA (1987) The phenomenon of “nonmycorrhizal” plants. Can J Bot 65:419–431CrossRefGoogle Scholar
  39. Tian H, Gai JP, Zhang JL, Christie P, Li XL (2009) Arbuscular mycorrhizal fungi in degraded typical steppe of Inner Mongolia. Land Degrad Dev 20:41–54CrossRefGoogle Scholar
  40. Ulziikhutag N (1989) Review of flora of Mongolia, Ulaanbaatar, UlaanbaatarGoogle Scholar
  41. Undarmaa J, Tamura K, Luvsan N, Yamanaka N (2018) Rangeland ecosystems of Mongolia. Munkhiin Useg, UlaanbaartarGoogle Scholar
  42. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  43. Van Geel M, Busschaert P, Honnay O, Lievens B (2014) Evaluation of six primer pairs targeting the nuclear rRNA operon for characterization of arbuscular mycorrhizal fungal (AMF) communities using 454 pyrosequencing. J Microbiol Methods 106:93–100CrossRefGoogle Scholar
  44. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363CrossRefGoogle Scholar
  45. Wang L, Seki K, Miyazaki T, Ishihama Y (2009) The causes of soil alkalinization in the Songnen plain of Northeast China. Paddy Water Environ 7:259–270CrossRefGoogle Scholar
  46. Yamato M, Takahashi H, Shimono A, Kusakabe R, Yukawa T (2016) Distribution of Petrosavia sakuraii (Petrosaviaceae), a rare mycoheterotrophic plant, may be determined by the abundance of its mycobionts. Mycorrhiza 26:417–427CrossRefGoogle Scholar
  47. Yoshimura Y, Ido A, Iwase K, Matsumoto T, Yamato M (2013) Communities of arbuscular mycorrhizal fungi in the roots of Pyrus pyrifolia var. culta (Japanese pear) in orchards with variable amount of soil-available phosphorus. Microbes Environ 28:105–111CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ryota Kusakabe
    • 1
  • Takeshi Taniguchi
    • 2
  • Altansukh Goomaral
    • 3
  • Jamsran Undarmaa
    • 4
  • Norikazu Yamanaka
    • 2
  • Masahide Yamato
    • 5
  1. 1.Graduate School of EducationChiba UniversityChibaJapan
  2. 2.Arid Land Research CenterTottori UniversityTottoriJapan
  3. 3.Department of Biotechnology and BreedingMongolian State University of Life SciencesUlaanbaatarMongolia
  4. 4.Center for Ecosystem StudiesMongolian State University of Life SciencesUlaanbaatarMongolia
  5. 5.Faculty of EducationChiba UniversityChibaJapan

Personalised recommendations