The relationship between successional vascular plant assemblages and associated microbial communities on coal mine spoil heaps

Abstract

The aim of the study was to investigate the relationships between the vascular plant species and the associated soil microbial properties at various stages of vegetation development on unclaimed hard coal mine spoil heaps in Upper Silesia (south Poland). The spontaneous vegetation, soil chemistry as well as the activity and structure of microbial communities were recorded on this specific habitat. The colliery heaps were divided into four age classes and the plant species composition and cover abundance were recorded on established plots (2 m × 2 m). The soil microbial activity under the vegetation patches was assessed using fluorescein diacetate hydrolytic activity (FDHA) and the soil microbial biomass and community composition were determined by phospholipid fatty acid (PLFA) biomarkers. Total microbial biomass in soils from the older vegetation plots was significantly higher than those in soils from the younger plots. In all studied samples, microbial communities consisted primarily of bacteria with the dominance of Gram negative bacteria over Gram positive and aerobic microorganisms were more dominant than anaerobic ones. Statistical analysis revealed a correlation between the type of vegetation and microbial community structure.

Abbreviations

Co-CA:

Co-Correspondence Analysis

DCA:

Detrended Correspondence Analysis

FDHA-, PCA:

Principal Component Analysis

PLFA-, RDA:

Redundancy Analysis

References

  1. Adam, G. and H. Duncan. 2001. Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol. Biochem. 33: 943–951.

    Article  CAS  Google Scholar 

  2. Adamczyk, B., V. Kitunen and A. Smolander 2008. Protein precipitation by tannins in soil organic horizon and vegetation in relation to tree species. Biol. Fertil. Soils. 45: 55–64.

    Article  CAS  Google Scholar 

  3. Bezemer, T.M., C.S. Lawson, K. Hedlund, A.R. Edwards, A.J. Brook, J.M. Igual, S.R. Mortimer and W.H. van der Putten. 2006. Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands. J. Ecol. 94: 893–904.

    Article  CAS  Google Scholar 

  4. Bird, J.A., D.J. Herman, and M.K. Firestone. 2011 Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol. Biochem. 43:718–725.

    Article  CAS  Google Scholar 

  5. Chakravorty, R.N. and R.J. Kolada. 1988. Prevention and control of spontaneous combustion in coal mines. Mining Engineering 40: 952–956.

    CAS  Google Scholar 

  6. Chmura, D., P. Adamski and Z. Denisiuk. 2013. How do plant communities and fower visitors relate? A case study of semi-natural xerothermic grasslands. Acta Soc Bot Pol. 82(2): 99–105.

    Article  Google Scholar 

  7. Chmura, D. and T. Molenda. 2012. Influence of thermally polluted water on the growth of helophytes in the vicinity of a colliery waste. Water, Air and Soil Pollution 223(9): 5877–5884.

    Article  CAS  Google Scholar 

  8. Chmura D., T. Molenda, A. Błońska and G. Woźniak. 2011. Sites of leachate infows on coalmine heaps as refuges of rare mountainous species. Polish Journal of Environmental Studies 20(3): 551–557.

    CAS  Google Scholar 

  9. Chodak, M. and M. Niklińska. 2010. Effect of texture and tree species on microbial properties of mine soils. Appl. Soil Ecol. 46: 268–275.

    Article  Google Scholar 

  10. Chodak, M., M. Pietrzykowski and M. Niklińska. 2009. Development of microbial properties in a chronosequence of sandy mine soils. Appl Soil Ecol. 41: 259–268.

    Article  Google Scholar 

  11. Cohn, E.V., A. Rostański, B. Tokarska-Guzik, I.C. Trueman and G. Woźniak. 2001. The flora and vegetation of an old solvay process tip in Jaworzno (Upper Silesia, Poland). Acta Soc Bot Pol. 70(1): 47–60.

    Article  Google Scholar 

  12. De Deyn, G.B., H. Quirk and R.D. Bardgett. 2011. Plant species richness, identity and productivity differentially infuence key groups of microbes in grassland soils of contrasting fertility. Biology Letters 7(1): 75–78.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Denslow, J. S. 1980. Patterns of plant species diversity during succession under different disturbance regimes. Oecologia 46(1): 18–21.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Dobrzański, B., S. Udziak, Z. Klimowicz and J. Melke. 1987. Badanie gleb w laboratorium i w polu. Przewodnik do ćwiczeń z glebo-znawstwa dla studentów biologii i geografi. Wyd. Uniwersytetu Marii Curie-Skłodowskiej, Lublin, pp. 329.

    Google Scholar 

  15. Dzwonko, Z., Loster, S. 2007. A functional analysis of vegetation dynamics in abandoned and restored limestone grasslands J. Veg. Sci. 18 (2): 203–212.

    Article  Google Scholar 

  16. Ehlers, K., L.R. Bakken, Å. Frostegård, E. Frossard, and E.K. Bünemann. 2010. Phosphorus limitation in a Ferralsol: Impact on microbial activity and cell internal P pools. Soil Biol. Biochem. 42: 558–566.

    Article  CAS  Google Scholar 

  17. Ehrenfeld, J.G., B. Ravit and K. Elgersma. 2005. Feedback in the plant-soil system. Annu. Rev. Environ. Resour. 30: 75–115.

    Article  Google Scholar 

  18. Elgersma, K.J., and J.G. Ehrenfeld. 2011. Linear and non-linear impacts of a non-native plant invasion on soil microbial community structure and function. Biol. Invasions 13: 757–768.

    Article  Google Scholar 

  19. Elhottova, D., V. Kristufek, S. Maly and J. Frouz. 2009. Rhizosphere effect of colonizer plant species on the development of soil mi-crobial community during primary succession on post mining sites. Commun. Soil Sci. Plan. 40: 758–770.

    Article  CAS  Google Scholar 

  20. Faliński, J. 2003. Long term studies on vegetation dynamics: some notes on concepts, fundamentals and conditions. Community Ecol. 4(1): 107–113.

    Article  Google Scholar 

  21. Fotyma, E, G. Wilkos and C. Pietruch. 1998. Test glebowy azotu mineralnego możliwości praktycznego wykorzystania. IUNG, Puławy. pp. 48.

  22. Frostegård Å., and E. Bååth. 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol. Fertil. Soil. 22: 59–65.

    Article  Google Scholar 

  23. Frostegård, Å., A. Tunlid and E. Bååth. 1993. Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl. Environ. Microbiol. 59(11): 3605–3617.

    Google Scholar 

  24. Frouz, J., B. Keplin, V. Pižl, K. Tajovský, J. Starý, J.A. Lukešová, A. Nováková, V. Balík, L. Háněl, J. Materna, C. Düker, J. Chalupský, J. Rusek, and T. Heinkele. 2001. Soil biota and upper soil layers development in two contrasting post-mining chrono-sequences. Ecol. Eng. 17: 275–284.

    Article  Google Scholar 

  25. Frouz, J. and A. Nováková. 2005. Development of soil microbial properties in top soil layer during spontaneous succession in heaps after brown coal mining in relation to soil microstructure development. Geoderma 129: 54–64.

    Article  Google Scholar 

  26. Frouz, J., V. Pil, E. Cienciala and J. Kalcík. 2009. Carbon storage in post-mining forest soil, the role of tree biomass and soil biotur-bation. Biogeochemistry 94: 111–121.

    Article  CAS  Google Scholar 

  27. Garcia, C, A. Roldan and T. Hernandez. 2005. Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma 124: 193–202.

    Article  CAS  Google Scholar 

  28. García-Palacios, P., M. Bowker, S. Chapman, F. Maestre and S. Soliveres. 2011. Early-successional vegetation changes after roadside prairie restoration modify processes related with soil functioning by changing microbial functional diversity. Soil Biology and Biochemistry 43(6): 1245–1253.

    Article  CAS  Google Scholar 

  29. Grayston, S.J., G.S. Griffith, J.L. Mawdsley, CD. Campbell and R.D. Bardgett. 2001. Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol. Biochem. 33: 533–551.

    Article  CAS  Google Scholar 

  30. Hatfield, R.G. and G. LeBuhn. 2007. Patch and landscape factors shape community assemblage of bumble bees, Bombus spp. (Hymenoptera: Apidae), in montane Meadows. Biol. Conserv. 139: 150–158.

    Article  Google Scholar 

  31. Helingerová M., Frouz J. and H. Šantrůčková. 2010. Microbial activity in reclaimed and unreclaimed post-mining sites near Sokolov (Czech Republic). Ecol. Eng. 36: 768–776.

    Article  Google Scholar 

  32. Huguet, V. and J.A. Rudgers. 2010. Covariation of soil bacterial composition with plant rarity. Appl. Environ. Microbiol. 76: 7665– 7667.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Kiikkilä, O., V. Kitunen and A. Smolander. 2006. Dissolved soil organic matter from surface organic horizons under birch and conifers: degradation in relation to chemical characteristics. Soil Biol. Biochem. 38: 737–746.

    Article  CAS  Google Scholar 

  34. Koranda, M., J. Schnecker, C. Kaiser, L. Fuchslueger, B. Kitzler, C.F. Stange, A. Sessitsch, S. Zechmeister-Boltenstern and A. Richter 2011. Microbial processes and community composition in the rhizosphere of European beech - The influence of plant C exudates. Soil Biol. Biochem. 43: 551–558.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kozdrój J. 2000. Microfora of technogeous wastes characterised by fatty acid profiling. Microb. Res. 155: 149–156.

    Article  Google Scholar 

  36. Liu, Z., G. Liu, B. Fu and X. Zheng. 2008. Relationship between plant species diversity and soil microbial functional diversity along a longitudinal gradient in temperate grasslands of Hulunbeir, Inner Mongolia, China. Ecol. Res. 23: 511–518.

    Article  Google Scholar 

  37. Mendez M.O. and R.M. Maier. 2008. Phytostabilization of mine tailings in arid and semiarid environments - an engineering remediation technology. Environ. Health Perspect. 116(3): 278–283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Mendez M.O. Glenn E.P and R.M. Meier. 2007. Phytostabilization potential of quailbush for mine tailings: growth, metal accumulation and microbial community changes. J. Environ. Qual. 36: 245–253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mirek, Z., H. Piękoś-Mirkowa, A. Zając and M. Zając. 2002. Flowering plants and pteridophytes of Poland a checklist. W. Szafer Institute of Botany PAN. Kraków. pp. 442.

    Google Scholar 

  40. Mitchell, R.J., A.J. Hester, CD. Campbell, S.J. Chapman, CM. Cameron, R.L. Hewison and J.M. Potts. 2010. Is vegetation composition or soil chemistry the best predictor of the soil microbial community? Plant Soil. 333: 417–430.

    Article  CAS  Google Scholar 

  41. Mitchell, R.J., CD. Campbell, S.J. Chapman, G.H. Osler, A.J. Vanbergen, L.R. Ross, CM. Cameron and L. Cole 2007. The cascading effects of birch on heather moorland: a test for the top-down control of an ecosystem engineer. J. Ecol. 95: 540–554.

    Article  CAS  Google Scholar 

  42. Moynahan OS., C.A. Zabinski and J.E. Gannon. 2002. Microbial community structure and carbon-utilization diversity in a mine tailings revegetation study. Restor. Ecol. 10: 77–87.

    Article  Google Scholar 

  43. Muller, T. and H. Hoper. 2004. Soil organic matter turnover as a function of the soil clay content: consequences for model applications. Soil Biol. Biochem. 36: 877–888.

    Article  CAS  Google Scholar 

  44. Nannipieri, P., J. Ascher, M.T. Ceccherini, L. Landi, G. Pietramellara and G. Renella. 2003. Microbial diversity and soil function. Eur. J. Soil Sci. 54: 655–70.

    Article  Google Scholar 

  45. Patel A.K. and N. Behera. 2011. Genetic diversity of coal mine spoil by metagenomes using random amplifed polymorphic DNA (RAPD) marker. Ind. J. Biotechnol. 10: 90–96.

    CAS  Google Scholar 

  46. Pennanen, T., A. Frostegård, H. Fritze and E. Bååth. 1996. Phospolipid fatty acid composition and heavy metal tolerance of soil micro-bial communities along two heavy metal-polluted gradients in coniferous forests. Appl. Environ. Microbiol. 62: 420–428.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Pokorny, M., R. Sheley, C. Zabinski, R. Engel, T. Svejcar and J. Borkowski. 2005. Plant functional group diversity as a mechanism for invasion resistance. Restoration Ecol. 13: 448–459.

    Article  Google Scholar 

  48. Priha, O. and A. Smolander. 1997. Microbial biomass and activity in soil and litter under Pinus sylvestris, Picea abies and Betula pendula at originally similar field afforestation sites. Biol. Fertil. Soils. 24: 45–51.

    Article  CAS  Google Scholar 

  49. Rahmonov, O. 2009. The chemical composition of plant liter of black locust (Robinia pseudoacacia L.) and its ecological role in sandy ecosystems. Acta Ecologica Sinica 29(4): 237–243.

    Article  Google Scholar 

  50. Rahmonov, O., M.A. Rzętała, M. Rahmonov, E. Kozyreva, A. Jagus and M., Rzętała. 2011. The formation of soil chemistry and the development of fertility islands under plant canopies in sandy areas. Research Journal of Chemistry and Environment 15(2): 823–829.

    CAS  Google Scholar 

  51. Rostański, A. 2005. Specific features of the flora of colliery spoil heaps in selected European regions. Polish Botanical Studies 19: 97–103.

    Google Scholar 

  52. Rostański, A. and G. Woźniak. 2007. Grasses (Poacae) on post-industrial waste sites in course of spontaneous succesion. Fragmenta Floristica et Geobotanica 9: 31–42.

    Google Scholar 

  53. Schaaf, W., O. Bens, A. Fischer, H.H. Gerke, W. Gerwin, U. Grünewald, H.M. Holländer , I. Kögel-Knabner, M. Mutz, M. Schloter, R. Schulin, M. Veste, S. Winter and R.F. Hüttl. 2011. Patterns and processes of initial terrestrial-ecosystem development. J. Plant Nutr. Soil Sci. 174: 229–239.

    Article  CAS  Google Scholar 

  54. Scherer-Lorenzen, M. 2008. Functional diversity affects decomposition processes in experimental grasslands. Functional Ecol. 22: 547–555.

    Article  Google Scholar 

  55. Simpson, G.L. 2009. cocorresp: Co-correspondence analysis ordination methods. (R package version 0.1-9). (http://cran.r-project. org/package=analogue).

  56. Sinha, S., R.E. Masto, L.C. Ram, V.A .Selvi, N.K. Srivastava, R.C. Tripathi and J. George. 2009. Rhizosphere soil microbial index of tree species in a coal mining ecosystem. Soil Biol Biochem. 41: 1824–1832.

    Article  CAS  Google Scholar 

  57. Skarżyńska, K.M. 1997. Odpady powęglowe i ich zastosowanie w inżynierii lądowej i wodnej. Wydawnictwo Akademii Rolniczej. Krakow. pp. 110.

    Google Scholar 

  58. ter Braak, C.J. and A.P. Schaffers. 2004. Co-correspondence analysis: a new ordination method to relate two community compositions. Ecology 85: 834–846.

    Article  Google Scholar 

  59. Treonis, A.M., N.J. Ostle, A.W. Stott, R. Primrose, S.J. Grayston and P. Ineson. 2004. Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs. Soil Biol. Biochem. 36: 533–537.

    Article  CAS  Google Scholar 

  60. Tropek, R., L. Spitzer and M. Konvicka. 2008. Two groups of epigeic arthropods differ in colonising of piedmont quarries: the necessity of multi-taxa and life-history traits approaches in the monitoring studies. Community Ecol. 9: 177–184.

    Article  Google Scholar 

  61. Urbanová, M., J. Kopecký, V. Valásková, M. Ságová-Marecková, D. Elhottová, M. Kyselková, Y. Moënne-Loccoz and P. Baldrian. 2011. Development of bacterial community during spontaneous succession on spoil heaps after brown coal mining. FEMS Microbiology Ecology 78, 59–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. van der Heijden, M., J. Klironomos, M. Ursic, P. Moutoglis, R. Streitwolf-Engel, T. Boller, A. Wiemken and I. Sanders. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72.

    Article  CAS  Google Scholar 

  63. van der Heijden, M.G., R.D. Bardgett and N.M. van Straalen. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett. 11: 296– 310.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Warembourg, F.R., C. Roumet and F. Lafont. 2003. Differences in rhizosphere carbon partitioning among plant species of different families. Plant Soil. 256: 347–357.

    Article  CAS  Google Scholar 

  65. Williams, M.A., K. Jangid, S.G. Shanmugam and W.B. Whitman. 2013. Bacterial communities in soil mimic patterns of vegetative succession and ecosystem climax but are resilient to change between seasons. Soil Biol. Biochem. 57:749–757.

    Article  CAS  Google Scholar 

  66. Woźniak, G. 2010. Diversity of vegetation on coal-mine heaps of the Upper Silesia (Poland). W. Szafer Institute of Botany, Polish Academy of Sciences. Krakow.

    Google Scholar 

  67. Woźniak, G. and E.V. Cohn. 2007. Monitoring of spontaneous vegetation dynamics on post coal mining waste sites in Upper Silesia, Poland. In: R.W. Sarsby and A. Felton (eds.), Geotechnical and Environmental Aspects of Waste Disposal Sites. Taylor and Francis Group. London. pp. 289–294.

    Google Scholar 

  68. Woźniak, G., D. Chmura, A. Błońska, E. Sierka and B. Tokarska-Guzik. 2011. Applicability of the concept of functional groups for analysis of spatiotemporal vegetation changes on manmade habitats. Polish Journal of Environmental Studies 20(3): 623– 631.

    Google Scholar 

  69. Zelles, L. 1999. Fatty acid patterns of phospholipids and lipopolysac-charides in the characterization of microbial communities in soil: a review. Biol. Fertil. Soils 29: 111–129.

    Article  CAS  Google Scholar 

  70. Zhang, Ch, G. Liu, S. Xue and Z. Song. 2011. Rhizosphere soil mi-crobial activity under different vegetation types on the Loess Plateau, China. Geoderma 161: 115–125.

    Article  CAS  Google Scholar 

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Woźniak, G., Markowicz, A., Borymski, S. et al. The relationship between successional vascular plant assemblages and associated microbial communities on coal mine spoil heaps. COMMUNITY ECOLOGY 16, 23–32 (2015). https://doi.org/10.1556/168.2015.16.1.3

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Keywords

  • Dominant species
  • Microbe-plant relation
  • Microbial communities
  • Post-industrial sites
  • Vegetation development

Nomenclature

  • for vascular plants Mirek et al. (2002)