Abstract
Background and aims
A major concern in developing microbially-assisted phytoextraction (MAP) is that the effects of introduced microbes on indigenous soil microbial community are profound and irreversible. To date, however, the microbial properties of soils subjected to MAP remain poorly understood. Therefore, we explored the effects of inoculation with a bacterial consortium enriched from acid mine drainage on not only the cadmium (Cd) phytoextraction efficiency of Averrhoa carambola but also the microbial properties of the Cd-contaminated soil.
Methods
We conducted a field experiment and characterized the microbial community in the contaminated soil using next generation sequencing technology (Illumina MiSeq).
Results
The bacterial inoculation increased the Cd concentration in A. carambola shoot tissues by 20%–65%, leading to a relatively high Cd removal efficiency (4.63% annually). Meanwhile, there were no significant differences between the treatments in soil bacterial diversity and community composition one year after the initiation of the bacterial inoculation treatment. The most abundant genera of the introduced bacteria were found to either disappear from, or be present in similar relative abundance, in the soils of the different treatments, except Sulfobacillus.
Conclusions
Collectively, our results provide evidence that MAP could be practiced with minor effects on indigenous soil microbial community.
Similar content being viewed by others
References
Adriano DC (2001) Trace elements in the terrestrial environment. Springer, New York
Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152
Braud A, Jézéquel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Chen L, Luo S, Li X, Wan Y, Chen J, Liu C (2014) Interaction of Cd-hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake. Soil Biol Biochem 68:300–308
Chesworth W (2008) Encyclopedia of soil science. Springer, Dordrecht
De Boer W, Kowalchuk GA (2001) Nitrification in acid soils: micro-organisms and mechanisms. Soil Biol Biochem 33:853–866
Di Gregorio S, Barbafieri M, Lampis S, Sanangelantoni AM, Tassi E, Vallini G (2006) Combined application of triton X-100 and Sinorhizobium sp. Pb002 inoculum for the improvement of lead phytoextraction by Brassica juncea in EDTA amended soil. Chemosphere 63:293–299
Ding CY, Zheng Y, Ren XM, Chen ZJ (2016) Changes in bacterial community composition during the remediation of Cd-contaminated soils of bioenergy crops. Acta Sci Circumst 36:3009–3016
Dopson M, Baker-Austin C, Hind A, Bowman JP, Bond PL (2004) Characterization of Ferroplasma isolates and Ferroplasma acidarmanus sp. nov., extreme acidophiles from acid mine drainage and industrial bioleaching environments. Appl Environ Microbiol 70:2079–2088
Farwell AJ, Vesely S, Nero V, Rodriguez H, McCormack K, Shah S, Dixon DG, Glick BR (2007) Tolerance of transgenic canola plants (Brassica napus) amended with plant growth-promoting bacteria to flooding stress at a metal-contaminated field site. Environ Pollut 147:540–545
Huang JW, Chen JJ, Berti WR, Cunningham SD (1997) Phytoremediation of lead-contaminated soils: role of synthetic chelates in lead phytoextraction. Environ Sci Technol 31:800–805
Jankong P, Visoottiviseth P, Khokiattiwong S (2007) Enhanced phytoremediation of arsenic contaminated land. Chemosphere 68:906–1912
Karavaiko GI, Kondrat’eva TF, Tsaplina IA, Egorova MA, Krasil’nikova EN, Zakharchuk LM (2005) Reclassification of ‘Sulfobacillus thermosulfidooxidans subsp. thermotolerans’ strain K1 as Alicyclobacillus tolerans sp. nov. and Sulfobacillus disulfidooxidans Dufresne et al. 1996 as Alicyclobacillus disulfidooxidans comb. Nov., and emended description of the genus Alicyclobacillus. Int J Syst Evol Microbiol 55:941–947
Kock D, Schippers A (2008) Quantitative microbial community analysis of three different sulfidic mine tailing dumps generating acid mine drainage. Appl Environ Microbiol 74:5211–5219
Krämer U (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Curr Opin Biotechnol 16:133–141
Langella F, Grawunder A, Stark R, Weist A, Merten D, Haferburg G, Büchel G, Kothe E (2014) Microbially assisted phytoremediation approaches for two multi-element contaminated sites. Environ Sci Pollut Res 21:6845–6858
Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522
Li JT, Liao B, Dai ZY, Zhu R, Shu WS (2009) Phytoextraction of Cd-contaminated soil by carambola (Averrhoa carambola) in field trials. Chemosphere 76:1233–1239
Li JT, Baker AJM, Ye ZH, Wang HB, Shu WS (2012) Phytoextraction of Cd-contaminated soils: current status and future challenges. Crit Rev Environ Sci Technol 42:2113–2152
Lin H, Shi J, Chen X, Yang J, Chen Y, Zhao Y, Hu T (2010) Effects of lead upon the actions of sulfate-reducing bacteria in the rice rhizosphere. Soil Biol Biochem 42:1038–1044
Lindsay WL, Norvell WA (1978) Development of a DTPA test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428
Liu JS, Xie XH, Xiao SM, Wang XM, Zhao WJ, Tian ZL (2007) Isolation of Leptospirillum ferriphilum by single-layered solid medium. J Cent S Univ Technol 14:467–473
Liu YR, Wang JJ, Zheng YM, Zhang LM, He JZ (2014) Patterns of bacterial diversity along a long-term mercury-contaminated gradient in the paddy soils. Microb Ecol 68:575–583
Lu RK (2000) Analytical methods of soil and agricultural chemistry. China Agricultural Science and Technology Press, Beijing
Marhual NP, Pradhan N, Kar RN, Sukla LB, Mishra BK (2008) Differential bioleaching of copper by mesophilic and moderately thermophilic acidophilic consortium enriched from same copper mine water sample. Bioresour Technol 99:8331–8336
McLaughlin MJ, Parker DR, Clarke JM (1999) Metal and micronutrientsdfood safety issues. Field Crop Res 60:143–163
Phieler R, Merten D, Roth M, Büchel G, Kothe E (2015) Phytoremediation using microbially mediated metal accumulation in Sorghum bicolor. Environ Sci Pollut Res 22:19408–19416
Prapagdee B, Khonsue N (2015) Bacterial-assisted cadmium phytoremediation by Ocimum gratissimum L. in polluted agricultural soil: a field trial experiment. Int J Environ Sci Technol 12:3843–3852
Robinson BH, Anderson CWN, Dickinson NM (2015) Phytoextraction: where’s the action? J Geochem Explor 151:34–40
Rodriguez-Leiva M, Tributsch H (1988) Morphology of bacterial leaching patterns by Thiobacillus ferrooxidans on synthetic pyrite. Arch Microbiol 149:401–405
Salt DE, Blaylock M, Kumar NP, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Nat Biotechnol 13:468–474
Schippers A, Breuker A, Blazejak A, Bosecker K, Kock D, Wright TL (2010) The biogeochemistry and microbiology of sulfidic mine waste and bioleaching dumps and heaps, and novel Fe(II)-oxidizing bacteria. Hydrometallurgy 104:342–350
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194
Shokralla S, Spall JL, Gibson JF, Hajibabaei M (2012) Next-generation sequencing technologies for environmental DNA research. Mol Ecol 21:1794–1805
Silverman MP, Lundgren DG (1959) Studies on the chemoautotrophic iron bacterium Ferrobacillus ferrooxidans: I. An improved medium and harvesting procedure for securing high cell yields. J Bacteriol 77:642–647
Sun M, Xiao T, Ning Z, Xiao E, Sun W (2015) Microbial community analysis in rice paddy soils irrigated by acid mine drainage contaminated water. Appl Microbiol Biotechnol 99:2911–2922
Teixeira C, Almeida CMR, Nunes da Silva M, Bordalo AA, Mucha AP (2014) Development of autochthonous microbial consortia for enhanced phytoremediation of salt-marsh sediments contaminated with cadmium. Sci Total Environ 493:757–765
US EPA (1996) Method 3052: microwave assisted acid digestion of siliceous and organically based matrice. US EPA, Washington, DC
Wang FY, Lin XG, Yin R (2005) Heavy metal uptake by arbuscular mycorrhizas of Elsholtzia splendens and the potential for phytoremediation of contaminated soil. Plant Soil 269:225–232
Wang FY, Lin XG, Yin R (2007a) Role of microbial inoculation and chitosan in phytoextraction of Cu, Zn, Pb and Cd by Elsholtzia splendens - a field case. Environ Pollut 147:248–255
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007b) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
WHO (1992a) Cadmium. Environmental health criteria, vol. 134. WHO, Geneva
WHO (1992b) Cadmium─environmental aspects. Environmental health criteria, vol. 135. WHO, Geneva
Xiang Y, Wu P, Zhu N, Zhang T, Liu W, Wu J, Li P (2010) Bioleaching of copper from waste printed circuit boards by bacterial consortium enriched from acid mine drainage. J Hazard Mater 184:812–818
Xu BB (2012) Bioleaching of heavy metals from contaminated soils using microbes from acid mine drainage. M.S. Dissertation, Sun Yat-sen University
Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997
Zhang X, Xia H, Li Z, Zhuang P, Gao B (2010) Potential of four forage grasses in remediation of Cd and Zn contaminated soils. Bioresour Technol 101:2063–2066
Zhao FJ, Ma Y, Zhu YG, Tang Z, McGrath SP (2015) Soil contamination in China: current status and mitigation strategies. Environ Sci Technol 49:750–759
Acknowledgements
We thank Prof. Alan Baker of the University of Melbourne for his insightful comments that have helped to improve the quality of the manuscript. This work was funded by the National Natural Science Foundation of China (Nos. 31100372 and 41471257), the Pearl River Nova Program of Guangzhou (No. 2014 J2200100), the Fok Ying Tong Education Foundation (No. 142025), the Guangdong Provincial Natural Science Foundation (No. 10451027501005629), and the Specialized Research Fund for the Doctoral Program of Higher Education (No. 20110171120042).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Fangjie Zhao.
Rights and permissions
About this article
Cite this article
Li, Jt., Liang, Zw., Jia, P. et al. Effects of a bacterial consortium from acid mine drainage on cadmium phytoextraction and indigenous soil microbial community. Plant Soil 415, 347–358 (2017). https://doi.org/10.1007/s11104-016-3170-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-016-3170-0