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Responses of soil microbial and nematode communities to aluminum toxicity in vegetated oil-shale-waste lands

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Abstract

Both soil nematodes and microorganisms have been shown to be sensitive bioindicators of soil recovery in metal-contaminated habitats; however, the underlying processes are poorly understood. We investigated the relationship among soil microbial community composition, nematode community structure and soil aluminum (Al) content in different vegetated aluminum-rich ecosystems. Our results demonstrated that there were greater soil bacterial, fungal and arbuscular mycorrhizal fungal biomass in Syzygium cumini plantation, greater abundance of soil nematodes in Acacia auriculiformis plantation, and greater abundance of soil predatory and herbivorous nematodes in Schima wallichii plantation. The concentration of water-soluble Al was normally greater in vegetated than non-vegetated soil. The residual Al and total Al concentrations showed a significant decrease after planting S. cumini plantation onto the shale dump. Acid extractable, reducible and oxidisable Al concentrations were greater in S. wallichii plantation. Stepwise linear regression analysis suggests the concentrations of water-soluble Al and total Al content explain the most variance associated with nematode assembly; whereas, the abundance of early-successional nematode taxa was explained mostly by soil moisture, soil organic C and total N rather than the concentrations of different forms of Al. In contrast, no significant main effects of either Al or soil physico-chemical characteristics on soil microbial biomass were observed. Our study suggests that vegetation was the primary driver on soil nematodes and microorganisms and it also could regulate the sensitivity of bio-indicator role mainly through the alteration of soil Al and physico-chemical characteristics, and S. cumini is effective for amending the Al contaminated soils.

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References

  • Anderson RV, Coleman DC, Cole CV, Elliot ET (1981) Effects of the nematodes Acrobeloides spp. and Mesodiplogaster lherithieri on substrate utilization and nitrogen and phosphorus mineralization in soil. Ecology 62:549–555

    Article  CAS  Google Scholar 

  • Banitz T, Wick LY, Fetzer I, Frank K, Harms H, Johst K (2011) Dispersal networks for enhancing bacterial degradation in heterogeneous environments. Environ Pollut 159:2781–2788

    Article  CAS  Google Scholar 

  • Barker KR (1985) Nematode extraction and bioassays. In: Barker KR, Carter CC, Sasser JN (eds) An advanced treatise on Meloidogyne, vol 2. North Carolina State University Graphics, North Carolina, pp 19–35

    Google Scholar 

  • Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19

    Article  Google Scholar 

  • Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10:239–251

    Article  Google Scholar 

  • Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14:224–228

    Article  Google Scholar 

  • Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278

    Article  CAS  Google Scholar 

  • Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12

    Article  CAS  Google Scholar 

  • Clark RB (1997) Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant Soil 192:15–22

    Article  CAS  Google Scholar 

  • Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of soil ecology, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Collignon C, Boudot JP, Turpault MP (2012) Time change of aluminium toxicity in the acid bulk soil and the rhizosphere in Norway spruce (Picea abies (L.) Karst.) and beech (Fagus sylvatica L.) stands. Plant Soil. doi:10.1007/s11104-012-1154-2

  • Ekschmitt K, Bakonyi G, Bongers M, Bongers T, Boström S, Dogan H, Harrison A, Nagy P, O’Donnell AG, Papatheodorou EM, Sohlenius B, Stamou GP, Wolters V (2001) Nematode community structure as indicator of soil functioning in European grassland soils. Eur J Soil Biol 37:263–268

    Article  Google Scholar 

  • Ferris H, Bongers T (2006) Nematode indicators of organic enrichment. J Nematol 38:3–12

    Google Scholar 

  • Ferris H, Matute MM (2003) Structural and functional succession in the nematode fauna of a soil food web. Appl Soil Ecol 23:93–110

    Article  Google Scholar 

  • Ferris H, Bongers T, de Goede RGM (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13–29

    Article  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Freckman DW (1988) Bacterivorous nematodes and organic-matter decomposition. Agric Ecosyst Environ 24:195–217

    Article  Google Scholar 

  • Fu SL, Cheng WX (2004) Defoliation affects rhizosphere respiration and rhizosphere priming effect on decomposition of soil organic matter under a sunflower species: Helianthus annuus. Plant Soil 263:345–352

    Article  CAS  Google Scholar 

  • Fu SL, Coleman DC, Hendrix PF, Crossley DA Jr (2000) Responses of trophic groups of soil nematodes to residue application under conventional tillage and no-till regimes. Soil Biol Biochem 32:1731–1741

    Article  CAS  Google Scholar 

  • Fu SL, Ferris H, Brown D, Plant R (2005) Does the positive feedback effect of nematodes on the biomass and activity of their bacteria prey vary with nematode species and population size? Soil Biol Biochem 37:1979–1987

    Article  CAS  Google Scholar 

  • Georgieva SS, McGrath SP, Hooper DJ, Chambers BS (2002) Nematode communities under stress: the long-term effects of heavy metals in soil treated with sewage sludge. Appl Soil Ecol 20:27–42

    Article  Google Scholar 

  • Goralczyk K (1998) Nematodes in a coastal dune succession: indicators of soil properties. Appl Soil Ecol 9:471–475

    Article  Google Scholar 

  • Joner EJ, Eldhuset TD, Lange TD, Frostegård Å (2005) Changes in the microbial community in a forest soil amended with aluminium in situ. Plant Soil 275:295–304

    Article  CAS  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol 46:237–260

    Article  CAS  Google Scholar 

  • Korthals GW, van de Ende A, van Megen H, Lexmond TM, Kammenga JE, Bongers T (1996) Short-term effects of cadmium, copper, nickel and zinc on soil nematodes from different feeding and life-history strategy groups. Appl Soil Ecol 4:107–117

    Article  Google Scholar 

  • Kowalchuk GA, de Bruijn FJ, Head IM, Akkermans ADL, van Elsas JD (2004) Molecular microbial ecology manual, 2nd edn, vol 1. Kluwer Academic Publishers, Dordrecht

  • Liu GS, Jiang NH, Zhang LD, Liu ZL (1996) Soil physical and chemical analysis and description of soil profiles. Standards Press of China, Beijing (in Chinese)

    Google Scholar 

  • Madsen EL, Sinclair JL, Ghiorse WC (1991) In situ biodegradation: microbiological patterns in a contaminated aquifer. Science (Washington DC) 252:830–833

    Article  CAS  Google Scholar 

  • McGrath SP, Cunliffe CH (1985) A simplified method for the extraction of the heavy metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co and Mn from soils and sewage sludges. J Sci Food Agric 36:794–798

    Article  CAS  Google Scholar 

  • Meharg AA, Cairney JWG (2000) Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv Ecol Res 30:70–112

    Google Scholar 

  • Mikola J, Setälä H (1998) No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 79:153–164

    Article  Google Scholar 

  • Neher D (2001) Role of nematodes in soil health and their use as indicators. J Nematol 33:161–168

    CAS  Google Scholar 

  • Neher D, Weicht TR, Barbercheck ME (2012) Linking invertebrate communities to decomposition rate and nitrogen availability in pine forest soils. Appl Soil Ecol 54:14–23

    Google Scholar 

  • Olsson PA, Bath E, Jakobsen I, Söderström B (1995) The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99:623–629

    Article  CAS  Google Scholar 

  • Quevauviller PH, Rauret G, Griepink B (1993) Single and sequential extraction in sediments and soils. Int J Environ Anal Chem 51:231–235

    Article  Google Scholar 

  • Rufyikiri G, Declerck S, Dufey JE, Delvaux B (2000) Arbuscular mycorrhizal fungi might alleviate aluminum toxicity in banana plants. New Phytol 148:343–352

    Article  CAS  Google Scholar 

  • Sánchez-Moreno S, Camargo JA, Navas A (2006) Ecotoxicological assessment of the impact of residual heavy metals on soil nematodes in the Guadiamar river basin (Southern Spain). Environ Monit Assess 116:245–262

    Article  Google Scholar 

  • Sánchez-Moreno S, Ferris H, Guil N (2008) Role of tardigrades in the suppressive service of a soil food web. Agric Ecosyst Environ 124:187–192

    Article  Google Scholar 

  • Sánchez-Moreno S, Ferris H, Nicola NL, Zalom FG (2009) Effects of agricultural management on nematode—mite assemblages: soil food web indices as predictors of mite community composition. Appl Soil Ecol 41:107–117

    Article  Google Scholar 

  • Scheu S, Ruess L, Bonkowski M (2005) Interactions between micro-organisms and soil micro- and mesofauna. In: Buscot F, Varma A (eds) Microorganisms in soils: roles in genesis and function. Springer-Verlag, New York, pp 253–275

  • Shao YH, Zhang WX, Shen JC, Zhou LX, Xia HP, Shu WS, Ferris H, Fu SL (2008) Nematodes as indicators of soil recovery in tailings of a lead/zinc mine. Soil Biol Biochem 40:2040–2046

    Article  CAS  Google Scholar 

  • Sylvain ZA, Wall DH (2011) Linking soil biodiversity and vegetation: implications for a changing planet. Amer J Bot 98:517–527

    Article  Google Scholar 

  • Van der Putten WH, Vet LEM, Harvey JA, Wäckers FL (2001) Linking aboveand belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554

    Article  Google Scholar 

  • Walter I, Martínez F, Cala V (2006) Heavy metal speciation and phytotoxic effects of three representative sewage sludges for agricultural uses. Environ Pollut 139:507–514

    Article  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  Google Scholar 

  • Williams PL, Dusenbery DB (1990) Aquatic toxicity testing using the nematode, Caenorhabditis elegans. Environ Toxicol Chem 9:1285–1290

    CAS  Google Scholar 

  • Wu FY (2008) Colonization and species diversity of arbuscular mycorrhizal fungi and their effects on metal tolerance and metal accumulation in two metal hyperaccumulators, Pteris vittata L. and Sedum alfredii Hance. Dissertation, Hong Kong Baptist University

  • Xia HP (2004) Ecological rehabilitation and phytoremediation with four grasses in oil shale mined land. Chemosphere 54:345–353

    Article  CAS  Google Scholar 

  • Xia HP, Huang J, Kong GH (2004) Ecological restoration of oil shale waste dumps. Acta Ecol Sin 24:2887–2893 (in Chinese)

    Google Scholar 

  • Yang TY, Liu GL, Li YC, Zhu SM, Zou AL, Qi JL, Yang YH (2012) Rhizosphere microbial communities and organic acids secreted by aluminum-tolerant and aluminum-sensitive soybean in acid soil. Biol Fertil Soils 48:97–108

    Article  CAS  Google Scholar 

  • Yeates GW, Bongers T (1999) Nematode diversity in agroecosystems. Agric Ecosyst Environ 74:113–135

    Article  Google Scholar 

  • Yeates GW, Bongers T, De Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315–331

    CAS  Google Scholar 

  • Zhao J, Wang XL, Shao YH, Xu GL, Fu SL (2011) Effects of vegetation removal on soil properties and decomposer organisms. Soil Biol Biochem 43:954–960

    Article  CAS  Google Scholar 

  • Zullini A, Peretti E (1986) Lead pollution and moss-inhabiting nematodes of an industrial area. Water Air Soil Pollut 27:403–441

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Prof. Guohui Kong for field sampling and Dr. Paul Kardol, Professor Howard Ferris, and two anonymous reviewers for their helpful comments. This study was financially supported by the program of “Ex situ plant conservation and soil biotic interactions” sponsored by Chinese Academy of Sciences (Y121021001, Y121021004), Natural Science Fund (31100385) sponsored by Natural Science Foundation of China and Natural Science Fund for Distinguished Young Scholars sponsored by Natural Science Foundation of China.

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Correspondence to Shenglei Fu.

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Shao, Y., Zhang, W., Liu, Z. et al. Responses of soil microbial and nematode communities to aluminum toxicity in vegetated oil-shale-waste lands. Ecotoxicology 21, 2132–2142 (2012). https://doi.org/10.1007/s10646-012-0966-4

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