Variation in soil microbial communities: elucidating relationships with vegetation and soil properties, and testing sampling effectiveness

Abstract

Understanding the extent of heterogeneity in soil microbial community structure and function at different scales within vegetation communities is critical to designing appropriate sampling protocols. Environmental factors (e.g. disturbance) make sampling in the riparian zone particularly challenging as vegetation communities are highly heterogeneous. To assess whether heterogeneity in soil and vegetation factors is reflected in microbial communities, a study was conducted in a riparian area in southern Australia. Nine quadrats were established encompassing different environmental conditions. Within quadrats physical, chemical and biological soil properties were analysed at two depths (top-soil = 0–10 cm and sub-soil = 20–30 cm), and floristic composition of ground cover, sub-canopy and canopy vegetation assessed. Soil biological analyses included microbial community composition (genetic analysis using ITS and 16S regions), and function (microbial metabolic activity using EcoPlates). Variation in soil microbial communities (fungi, bacteria, archaea) was related to differences in vegetation factors, particularly sub-canopy, and to a lesser extent, soil chemical properties. Relationships between variation in microbial communities and vegetation composition were stronger in top-soil than sub-soil. These observations were consistent for fungal communities excluding the phylum Glomeromycota, where the relationship was stronger with ground cover and only for top-soil. Variation in soil microbial community function was not related to variation in microbial community composition, soil physicochemical properties or vegetation factors. Our findings suggest there is little variation in the composition of soil microbial communities within areas with similar vegetation, and a small sampling effort would be needed to adequately describe the characteristics of such soil communities.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Aponte C, Garcia LV, Maranon T, Gardes M (2010a) Indirect host effect on ectomycorrhizal fungi: Leaf fall and litter quality explain changes in fungal communities on the roots of co-occurring Mediterranean oaks. Soil Biol Biochem 42:788–796

    CAS  Google Scholar 

  2. Aponte C, Marañón T, García LV (2010b) Microbial C, N and P in soils of Mediterranean oak forests: influence of season, canopy cover and soil depth. Biogeochemistry 101:77–92

    CAS  Google Scholar 

  3. Aponte C, Matías L, González-Rodríguez V, Castro J, García LV, Villar R, Marañón T (2014) Soil nutrients and microbial biomass in three contrasting Mediterranean forests. Plant Soil 380:57–72

    CAS  Google Scholar 

  4. Baudoin E, Benizri E, Guckert A (2001) Metabolic fingerprint of microbial communities from distinct maize rhizosphere compartments. Eur J Soil Biol 37:85–93

    Google Scholar 

  5. Beauchamp VB, Swan CM, Szlavecz K, Hu J (2015) Riparian community structure and soil properties of restored urban streams. Ecohydrology 8:880–895

    Google Scholar 

  6. Bissett A, Fitzgerald A, Meintjes T, Mele PM, Reith F, Dennis PG, Breed MF, Brown B, Brown MV, Brugger J, Byrne M, Caddy-Retalic S, Carmody B, Coates DJ, Correa C, Ferrari BC, Gupta VVSR, Hamonts K, Haslem A, Hugenholtz P, Karan M, Koval J, Lowe AJ, Macdonald S, McGrath L, Martin D, Morgan M, North KI, Paungfoo-Lonhienne C, Pendall E, Phillips L, Pirzl R, Powell JR, Ragan MA, Schmidt S, Seymour N, Snape I, Stephen JR, Stevens M, Tinning M, Williams K, Yeoh YK, Zammit CM, Young A (2016) Introducing BASE: the biomes of Australian soil environments soil microbial diversity database. GigaScience 5:1–11

    Google Scholar 

  7. Bogar LM, Peay KG (2017) Processes maintaining the coexistence of ectomycorrhizal fungi at a fine spatial scale. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer International Publishing, Switzerland, pp 79–106

    Google Scholar 

  8. Breed MF, Harrison PA, Blyth C, Byrne M, Gaget V, Gellie NJC, Groom SVC, Hodgson R, Mills JG, Prowse TAA, Steane DA, Mohr JJ (2019) The potential of genomics for restoring ecosystems and biodiversity. Nat Rev Genet 20:615–628

    CAS  PubMed  Google Scholar 

  9. Brundrett MC (2017) Distribution and evolution of mycorrhizal types and other specialised roots in Australia. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer International Publishing, Switzerland, pp 361–394

    Google Scholar 

  10. Caldwell SK, Valett HM, Peipoch M (2015) Spatial drivers of ecosystem structure and function in a floodplain riverscape: Springbrook nutrient dynamics. Freshw Sci 34:233–244

    Google Scholar 

  11. Calvo-Polanco M, Sánchez-Castro I, Cantos M, García JL, Azcón R, Ruiz-Lozano JM, Beuzón CR, Aroca R (2016) Effects of different arbuscular mycorrhizal fungal backgrounds and soils on olive plants growth and water relation properties under well-watered and drought conditions. Plant, Cell Environ 39:2498–2514

    CAS  Google Scholar 

  12. Canfield RH (1941) Application of the line interception method in sampling range vegetation. J For 39:388–394

    Google Scholar 

  13. Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans Royal Soc B 366:2351–2363

    Google Scholar 

  14. Climate-Data.org. (2018) Climate Warburton.

  15. Cottam G, Curtis JT (1956) The use of distance measures in phytosociological sampling. Ecology 37:451–460

    Google Scholar 

  16. Dassen S, Cortois R, Martens H, de Hollander M, Kowalchuk GA, van der Putten WH, De Deyn GB (2017) Differential responses of soil bacteria, fungi, archaea and protists to plant species richness and plant functional group identity. Mol Ecol 26:4085–4098

    CAS  PubMed  Google Scholar 

  17. DeBellis T, Kernaghan G, Bradley R, Widden P (2006) Relationships between stand composition and ectomycorrhizal community structure in boreal mixed-wood forests. Microb Ecol 52:114–126

    CAS  PubMed  Google Scholar 

  18. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    CAS  PubMed  Google Scholar 

  19. Edgar RC, Flyvbjerg H (2015) Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31:3476–3482

    CAS  PubMed  Google Scholar 

  20. Eilers KG, Debenport S, Anderson S, Fierer N (2012) Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biol Biochem 50:58–65

    CAS  Google Scholar 

  21. Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183

    Google Scholar 

  22. Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176

    CAS  Google Scholar 

  23. Frey S (2014) Spatial distribution of soil biota. In: Paul EA (ed) Soil microbiology, ecology and biochemistry. Academic press, Cambridge, pp 223–241

    Google Scholar 

  24. 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

    CAS  PubMed  Google Scholar 

  25. Garland JL (1997) Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol Ecol 24:289–300

    CAS  Google Scholar 

  26. Glassman SI, Wang IJ, Bruns TD (2017) Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales. Mol Ecol 26:6960–6973

    CAS  PubMed  Google Scholar 

  27. Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, Dangerfield M, Gillings M, Beattie AJ (2004) Spatial scaling of microbial eukaryote diversity. Nature 432:747–750

    CAS  PubMed  Google Scholar 

  28. Hansel CM, Fendorf S, Jardine PM, Francis CA (2008) Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl Environ Microbiol 74:1620–1633

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Harner MJ, Opitz N, Geluso K, Tockner K, Rillig MC (2011) Arbuscular mycorrhizal fungi on developing islands within a dynamic river floodplain: an investigation across successional gradients and soil depth. Aquat Sci 73:35–42

    CAS  Google Scholar 

  30. Henry C, Raivoarisoa J-F, Razafimamonjy AR, Heriniaina R, Andrianaivomahefa P, Selosse M-A, Ducousso M (2015) Asteropeia mcphersonii, a potential mycorrhizal facilitator for ecological restoration in Madagascar wet tropical rainforests. For Ecol Manage 358:202–211

    Google Scholar 

  31. Hermans SM, Buckley HL, Case BS, Curran-Cournane F, Taylor M, Lear G (2017) Bacteria as emerging indicators of soil condition. Appl Environ Microbiol 83:e02826–e12816

    CAS  PubMed  Google Scholar 

  32. Hill MO (1973) The intensity of spatial pattern in plant communities. J Ecol 61:225–235

    Google Scholar 

  33. Hiraoka S, Yang C-C, Iwasaki W (2016) Metagenomics and bioinformatics in microbial ecology: current status and beyond. Microbe Environ 31:204–212

    Google Scholar 

  34. Humboldt AV (1856) Cosmos: a Sketch or a Physical Description of the Universe. Translated by EC Otté. New York: Harper & Brothers.

  35. Kasel S, Bennett LT, Aponte C, Fedrigo M, Nitschke CR (2017) Environmental heterogeneity promotes floristic turnover in temperate forests of south-eastern Australia more than dispersal limitation and disturbance. Landscape Ecol 32:1613–1629

    Google Scholar 

  36. Kasel S, Bennett LT, Tibbits J (2008) Land use influences soil fungal community composition across central Victoria, south-eastern Australia. Soil Biol Biochem 40:1724–1732

    CAS  Google Scholar 

  37. Koide RT, Schreiner RP (1992) Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Ann Rev Plant Biol 43:557–581

    CAS  Google Scholar 

  38. Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166

    Google Scholar 

  39. Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 125–175

    Google Scholar 

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

    PubMed  Google Scholar 

  41. Ma Y, Li J, Wu J, Kong Z, Feinstein LM, Ding X, Ge G, Wu L (2018) Bacterial and fungal community composition and functional activity associated with lake wetland water level gradients. Sci Rep 8:760

    PubMed  PubMed Central  Google Scholar 

  42. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    PubMed  PubMed Central  Google Scholar 

  43. Mardhiah U, Caruso T, Gurnell A, Rillig MC (2014) Just a matter of time: fungi and roots significantly and rapidly aggregate soil over four decades along the Tagliamento River, NE Italy. Soil Biol Biochem 75:133–142

    CAS  Google Scholar 

  44. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Computat Biol 10(4):1-12

    Google Scholar 

  45. Mordelet P, Le Roux X (2006) Tree/grass interactions Lamto. Springer, New York, pp 139–161

    Google Scholar 

  46. Naiman RJ, Bechtold JS, Drake DC, Latterell JJ, O'keefe TC, Balian EV (2005) Origins, patterns, and importance of heterogeneity in riparian systems, Ecosystem Function in Heterogeneous Landscapes. Springer, pp. 279–309.

  47. Naiman RJ, Decamps H, Pollock M (1993) The role of riparian corridors in maintaining regional biodiversity. Ecol Appl 3:209–212

    PubMed  Google Scholar 

  48. Nicol GW, Glover LA, Prosser JI (2003) Spatial analysis of archaeal community structure in grassland soil. Appl Environ Microbiol 69:7420–7429

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Nilsson RH, Larsson K-H, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L (2018) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–D264

    PubMed Central  Google Scholar 

  50. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) Vegan: Community ecology package. R package version 1.17-4. https://CRAN.R-project.org/package=vegan

  51. Osborne CA, Zwart AB, Broadhurst LM, Young AG, Richardson AE (2011) The influence of sampling strategies and spatial variation on the detected soil bacterial communities under three different land-use types. FEMS Microbiol Ecol 78:70–79

    CAS  PubMed  Google Scholar 

  52. Ossola A, Aponte C, Hahs AK, Livesley SJ (2017) Contrasting effects of urban habitat complexity on metabolic functional diversity and composition of litter and soil bacterial communities. Urban Ecosyst 20:595–607

    Google Scholar 

  53. Pagano MC, Cabello MN (2012) Mycorrhizas in natural and restored riparian zones. In: Pagano MC (ed) Mycorrhiza: occurrence in natural and restored environments. Nova Science Publications, New York, pp 291–316

    Google Scholar 

  54. Peay KG, Kennedy PG, Bruns TD (2011) Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation? Fungal Ecol 4:233–240

    Google Scholar 

  55. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    PubMed  PubMed Central  Google Scholar 

  56. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  57. Ramirez KS, Snoek LB, Koorem K, Geisen S, Bloem LJ, ten Hooven F, Kostenko O, Krigas N, Manrubia M, Caković D (2019) Range-expansion effects on the belowground plant microbiome. Nat Ecol Evol 3:604–611

    PubMed  PubMed Central  Google Scholar 

  58. Revillini D, Gehring CA, Johnson NC (2016) The role of locally adapted mycorrhizas and rhizobacteria in plant–soil feedback systems. Funct Ecol 30:1086–1098

    Google Scholar 

  59. Smith T, Huston M, (1990) A theory of the spatial and temporal dynamics of plant communities. Progress in theoretical vegetation science. Springer, pp 49–69.

  60. Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Taylor JE, Thomson JA (1990) Allelopathic activity of frond run-off from Pteridium esculentum. AIAS Occasional Publ 40:203–208

    Google Scholar 

  62. Thies JE (2014) Molecular methods for studying soil ecology. In: Paul EA (ed) Soil microbiology, ecology and biochemistry. Academic Press, Cambridge, pp 85–118

    Google Scholar 

  63. Tiedje JM, Asuming-Brempong S, Nüsslein K, Marsh TL, Flynn SJ (1999) Opening the black box of soil microbial diversity. Appl Soil Ecol 13:109–122

    Google Scholar 

  64. van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998a) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091

    Google Scholar 

  65. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P (1998b) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Google Scholar 

  66. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    CAS  PubMed  PubMed Central  Google Scholar 

  67. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications, 18, pp 315-322

  68. Wiens JA (1989) Spatial scaling in ecology. Funct Ecol 3:385–397

    Google Scholar 

Download references

Acknowledgements

We thank Lisa Wittick, Sascha Andrusiak, Nicholas Osborne for technical support, Sabine Kasel for advice on statistical analyses, and field assistants Cordula Gutekunst, Ana Bermudez Contreras, Sarah Fischer, Tony Lovell, Kathy Russell, Robert Dabal, Anu Singh and Scott McKendrick. Our work was supported by Melbourne Water, Holsworth Wildlife Research Endowment and Ecological Society of Australia, and the Madeleine Selwyn Smith Memorial Scholarship. Vicky Waymouth was a recipient of a Research Training Program scholarship. We would like to acknowledge the contributions of the Biomes of Australian Soil Environments (BASE) and Australian Microbiome consortiums to the generation of genetic data for this study. The Australian Microbiome initiative is supported by funding from Bioplatforms Australia and the Integrated Marine Observing System (IMOS) through the Australian Government’s National Collaborative Research Infrastructure Strategy (NCRIS), Parks Australia through the Bush Blitz program funded by the Australian Government and BHP, and the CSIRO.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Vicky Waymouth.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Miranda Hart.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11258_2020_1029_MOESM1_ESM.docx

Supplementary file1 (DOCX 44 kb)

11258_2020_1029_MOESM2_ESM.docx

Supplementary file2 (DOCX 41 kb)

11258_2020_1029_MOESM3_ESM.docx

Supplementary file3 (DOCX 17 kb)

11258_2020_1029_MOESM4_ESM.docx

Supplementary file4 (DOCX 49 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Waymouth, V., Miller, R.E., Ede, F. et al. Variation in soil microbial communities: elucidating relationships with vegetation and soil properties, and testing sampling effectiveness. Plant Ecol 221, 837–851 (2020). https://doi.org/10.1007/s11258-020-01029-w

Download citation

Keywords

  • Community-level physiological profile (CLPP)
  • Soil physicochemical properties
  • Mycorrhizae
  • Archaea
  • Bacteria
  • Spatial variation
  • Riparian vegetation