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Microbial Diversity of Chromium-Contaminated Soils and Characterization of Six Chromium-Removing Bacteria

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Abstract

Three soil samples obtained from different sites adjacent to a chromium slag heap in a steel alloy factory were taken to examine the effect of chromium contamination on soil bacterial diversity as determined by construction of 16S rDNA clone libraries and sequencing of selected clones based on restriction fragment length polymorphism (RFLP) analysis. Results revealed that Betaproteobacteria, Gammaproteobacteria, Firmicutes, and Alphaproteobacteria occurred in all three soil samples, although the three samples differed in their total diversity. Sample 1 had the highest microbial diversity covering 12 different classes, while Sample 3 had the lowest microbial diversity. Strains of six different species were successfully isolated, one of which was identified as Zobellella denitrificans. To our knowledge, this is the first report of a strain belonging to the genus Zobellella able to resist and reduce chromium. Among all isolates studied, Bacillus odysseyi YH2 exhibited the highest Cr(VI)-reducing capability, with a total removal of 23.5 % of an initial Cr(VI) concentration of 350 mg L−1.

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References

  • Araya R, Tani K, Takagi T, Yamaguchi N, Nasu M (2003) Bacterial activity and community composition in stream water and biofilm from an urban river determined by fluorescent in situ hybridization and DGGE analysis. Fems Microbiol Ecol 43:111–119

    Article  CAS  Google Scholar 

  • Badar U, Ahmed N, Beswick A, Pattanapipitpaisal P, Macaskie L (2000) Reduction of chromate by microorganisms isolated from metal contaminated sites of Karachi. Pakistan Biotechnol Lett 22:829–836

    Article  CAS  Google Scholar 

  • Balci N, Vardar N, Yelboga E, Karaguler NG (2012) Bacterial community composition of sediments from Artificial Lake Maslak, Istanbul, Turkey. Environ Monit Assess 184:5641–5650. doi:10.1007/s10661-011-2368-0

    Article  CAS  Google Scholar 

  • Basu S, Dasgupta M, Chakraborty B (2014) Removal of Chromium (VI) by Bacillus subtilis Isolated from East Calcutta Wetlands, West Bengal, India. Int J biosci, biochem and bioinformatics 4:7–10

    Article  CAS  Google Scholar 

  • Blakemore LC, Searle PL, Daly BK, Bureau S (1977) Methods for chemical analysis of soils. Soil Bureau, Department of Scientific and Industrial Research

  • Branco R, Chung AP, Verissimo A, Morais PV (2005) Impact of chromium-contaminated wastewaters on the microbial community of a river. Fems Microbiol Ecol 54:35–46. doi:10.1016/j.femsec.2005.02.014

    Article  CAS  Google Scholar 

  • Brümmer I, Fehr W, Wagner-Döbler I (2000) Biofilm community structure in polluted rivers: abundance of dominant phylogenetic groups over a complete annual cycle. Appl Environ Microb 66:3078–3082

    Article  Google Scholar 

  • Byers SC, Mills EL, Stewart PL (1978) A comparison of methods of determining organic carbon in marine sediments, with suggestions for a standard method. Hydrobiologia 58:43–47

    Article  CAS  Google Scholar 

  • Camargo FAO, Okeke BC, Bento FM, Frankenberger WT (2005) Diversity of chromium-resistant bacteria isolated from soils contaminated with dichromate. Appl Soil Ecol 29:193–202. doi:10.1016/j.apsoil.2004.10.006

    Article  Google Scholar 

  • Cang L, Zhou D-M, Alshawabkeh AN, Chen H-F (2007) Effects of sodium hypochlorite and high pH buffer solution in electrokinetic soil treatment on soil chromium removal and the functional diversity of soil microbial community. J Hazard Mater 142:111–117

    Article  CAS  Google Scholar 

  • Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Loza-Tavera H, Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms and plants Fems. Microbiol Rev 25:335–347

    CAS  Google Scholar 

  • Chandhuru J, Harshitha S, Sujitha K, Kumar DM (2012) Isolation of chromium resistant Bacillus sp. MRKV and reduction of hexavalent chromium potassium dichromate. J Acad Indus Res 1:317–319

    Google Scholar 

  • Chen J, Tang YQ, Wu XL (2012) Bacterial community shift in two sectors of a tannery plant and its Cr (VI) removing potential. Geomicrobiol J 29:226–235. doi:10.1080/01490451.2011.558562

    Article  Google Scholar 

  • Chen J, He F, Zhang X, Sun X, Zheng J, Zheng J (2014) Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiol Ecol 87:164–181

    Article  CAS  Google Scholar 

  • Coreño-Alonso A et al (2014) Mechanisms of interaction of chromium with Aspergillus niger var tubingensis strain Ed8. Bioresource Technol 158:188–192

    Article  Google Scholar 

  • Desai C, Parikh RY, Vaishnav T, Shouche YS, Madamwar D (2009) Tracking the influence of long-term chromium pollution on soil bacterial community structures by comparative analyses of 16S rRNA gene phylotypes. Res Microbiol 160:1–9. doi:10.1016/j.resmic.2008.10.003

    Article  CAS  Google Scholar 

  • Dhal B, Thatoi H, Das N, Pandey BD (2010) Reduction of hexavalent chromium by Bacillus sp. isolated from chromite mine soils and characterization of reduced product. J Chem Technol Biot 85:1471–1479. doi:10.1002/jctb.2451

    CAS  Google Scholar 

  • Elangovan R, Abhipsa S, Rohit B, Ligy P, Chandraraj K (2006) Reduction of Cr (VI) by a Bacillus sp. Biotechnol Lett 28:247–252

    Article  CAS  Google Scholar 

  • Fendorf SE (1995) Surface reactions of chromium in soils and waters. Geoderma 67:55–71

    Article  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. doi:10.1890/05-1839

    Article  Google Scholar 

  • Focardi S, Pepi M, Landi G, Gasperini S, Ruta M, Di Biasio P, Focardi SE (2012) Hexavalent chromium reduction by whole cells and cell free extract of the moderate halophilic bacterial strain Halomonas sp. TA-04. Int Biodeter Biodegr 66:63–70. doi:10.1016/j.ibiod.2011.11.003

    Article  CAS  Google Scholar 

  • Francisco R, Alpoim MC, Morais PV (2002) Diversity of chromium-resistant and -reducing bacteria in a chromium-contaminated activated sludge. J Appl Microbiol 92:837–843. doi:10.1046/j.1365-2672.2002.01591.x

    Article  CAS  Google Scholar 

  • Frey B, Stemmer M, Widmer F, Luster J, Sperisen C (2006) Microbial activity and community structure of a soil after heavy metal contamination in a model forest ecosystem. Soil Biol Biochem 38:1745–1756

    Article  CAS  Google Scholar 

  • Garbisu C, Alkorta I, Llama MJ, Serra JL (1998) Aerobic chromate reduction by Bacillus subtilis. Biodegradation 9:133–141

    Article  CAS  Google Scholar 

  • He ZG, Gao FL, Sha T, Hu YH, He C (2009) Isolation and characterization of a Cr(VI)-reduction Ochrobactrum sp strain CSCr-3 from chromium landfill. J Hazard Mater 163:869–873. doi:10.1016/j.jhazmat.2008.07.041

    Article  CAS  Google Scholar 

  • He Z, Li S, Wang L, Zhong H (2014) Characterization of five chromium-removing bacteria isolated from chromium-contaminated. Soil Water Air Soil Pollut 225:1–10. doi:10.1007/s11270-014-1904-2

    Google Scholar 

  • Huang SH, Peng B, Yang ZH, Chai LY, Zhou LC (2009) Chromium accumulation, microorganism population and enzyme activities in soils around chromium-containing slag heap of steel alloy factory. Trans Nonferr Metal Soc 19:241–248. doi:10.1016/s1003-6326(08)60259-9

    Article  CAS  Google Scholar 

  • Hugenholtz P (2002) Exploring prokaryotic diversity in the genomic era. Genome Biol 3:1-0003

    Article  Google Scholar 

  • Kamaludeen SPB, Megharaj M, Juhasz AL, Sethunathan N, Naidu R (2003) Chromium-microorganism interactions in soils: Remediation implications. In: Ware GW (ed) Reviews of Environmental Contamination and Toxicology, vol 178. Reviews of Environmental Contamination and Toxicology. pp 93–164. doi:10.1007/0-387-21728-2_4

  • Katsaveli K, Vayenas D, Tsiamis G, Bourtzis K (2012) Bacterial diversity in Cr(VI) and Cr(III)-contaminated industrial wastewaters. Extremophiles 16:285–296. doi:10.1007/s00792-012-0429-0

    Article  CAS  Google Scholar 

  • Khattar J, Parveen S, Singh Y, Singh D, Gulati A (2014) Intracellular uptake and reduction of hexavalent chromium by the cyanobacterium Synechocystis sp. PUPCCC 62. J Appl Phycol 27(2):1–11

    Google Scholar 

  • Martins M, Faleiro ML, Chaves S, Tenreiro R, Santos E, Costa MC (2010) Anaerobic bio-removal of uranium (VI) and chromium (VI): comparison of microbial community structure. J Hazard Mater 176:1065–1072. doi:10.1016/j.jhazmat.2009.11.149

    Article  CAS  Google Scholar 

  • McLean JS, Beveridge TJ, Phipps D (2000) Isolation and characterization of a chromium-reducing bacterium from a chromated copper arsenate-contaminated site. Environ Microbiol 2:611–619. doi:10.1046/j.1462-2920.2000.00143.x

    Article  CAS  Google Scholar 

  • Megharaj M, Avudainayagam S, Naidu R (2003) Toxicity of hexavalent chromium and its reduction by bacteria isolated from soil contaminated with tannery waste. Curr Microbiol 47:0051–0054

    Article  CAS  Google Scholar 

  • Miao Y et al (2015) Metagenomic insights into Cr (VI) effect on microbial communities and functional genes of an expanded granular sludge bed reactor treating high-nitrate wastewater. Water Res 76:43–52

    Article  CAS  Google Scholar 

  • Murugavelh S, Mohanty K (2012) Bioreduction of hexavalent chromium by free cells and cell free extracts of Halomonas sp. Chem Eng J 203:415–422. doi:10.1016/j.cej.2012.07.069

    Article  CAS  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670. doi:10.1046/j.1351-0754.2003.0556.x

    Article  Google Scholar 

  • Odum EP (1985) Trends expected in stressed ecosystems. Bioscience 35:419–422

    Article  Google Scholar 

  • Ozturk S, Kaya T, Aslim B, Tan S (2012) Removal and reduction of chromium by Pseudomonas spp. and their correlation to rhamnolipid production. J Hazard Mater 231:64–69

    Article  Google Scholar 

  • Page AL (1982) Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy, Soil Science Society of America.

  • Pal A, Paul A (2004) Aerobic chromate reduction by chromium-resistant bacteria isolated from serpentine soil. Microbiol Res 159:347–354

    Article  CAS  Google Scholar 

  • Poornima M, Kumar RS, Thomas PD (2014) Isolation and molecular characterization of bacterial Strains from tannery effluent and reduction of chromium. Int J Curr Microbiol App Sci 3:530–538

    Google Scholar 

  • Rehman A, Zahoor A, Muneer B, Hasnain S (2008) Chromium tolerance and reduction potential of a Bacillus sp.ev3 isolated from metal contaminated wastewater. Bull Environ Contam Tox 81:25–29. doi:10.1007/s00128-008-9442-5

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Sheik CS et al (2012) Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PloS one 7:e40059. doi:10.1371/journal.pone.0040059

    Article  CAS  Google Scholar 

  • Soni SK, Singh R, Awasthi A, Kalra A (2014) A Cr (VI)-reducing Microbacterium sp. strain SUCR140 enhances growth and yield of Zea mays in Cr (VI) amended soil through reduced chromium toxicity and improves colonization of arbuscular mycorrhizal fungi. Environ Sci Pollut R 21:1971–1979

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  Google Scholar 

  • VanEngelen MR, Peyton BM, Mormile MR, Pinkart HC (2008) Fe(III), Cr(VI), and Fe(III) mediated Cr(VI) reduction in alkaline media using a Halomonas isolate from Soap Lake. Washington Biodegradation 19:841–850. doi:10.1007/s10532-008-9187-1

    Article  CAS  Google Scholar 

  • Viti C, Pace A, Giovannetti L (2003) Characterization of Cr(VI)-resistant bacteria isolated from chromium-contaminated soil by tannery activity. Curr Microbiol 46:1–5. doi:10.1007/s00284-002-3800-z

    Article  CAS  Google Scholar 

  • Viti C, Mini A, Ranalli G, Lustrato G, Giovannetti L (2006) Response of microbial communities to different doses of chromate in soil microcosms. Appl Soil Ecol 34:125–139. doi:10.1016/j.apsoil.2006.03.003

    Article  Google Scholar 

  • Viti C, Marchi E, Decorosi F, Giovannetti L (2014) Molecular mechanisms of Cr (VI) resistance in bacteria and fungi. FEMS Microbiol Rev 38:633–659

    Article  CAS  Google Scholar 

  • Wani R, Kodam K, Gawai K, Dhakephalkar P (2007) Chromate reduction by Burkholderia cepacia MCMB-821, isolated from the pristine habitat of alkaline crater lake. Appl Microbiol Biot 75:627–632

    Article  CAS  Google Scholar 

  • Xie X, Xiao S, He Z, Liu J, Qiu G (2007) Microbial populations in acid mineral bioleaching systems of Tong Shankou Copper Mine, China. J Appl Microbiol 103:1227–1238

    Article  CAS  Google Scholar 

  • Xu L et al (2012) In vitro reduction of hexavalent chromium by cytoplasmic fractions of Pannonibacter phragmitetus LSSE-09 under aerobic and anaerobic conditions. Appl Biochem Biotechol 166:933–941

    Article  CAS  Google Scholar 

  • Zhou B-J, Chen T-H (2014) Biodegradation of phenol with chromium (VI) reduction by the Pseudomonas sp. strain JF122. Desalination Water Treat:1–8

  • Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microb 62:316–322

    CAS  Google Scholar 

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Acknowledgments

The authors would like to thank prof. Peter Dunfield at University of Calgary and prof. Zhili He at University of Oklahoma for their help in revising the paper. This work was financially supported by the National Natural Science Foundation of China (No. 31370053 and No. 31500091), Co-Innovation Center for Clean & efficient Utilization of Strategic Metal Mineral Resources, and Innovation Driven Plan of Central South University (No. 2016CX016).

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Authors and Affiliations

  1. School of Minerals Processing and Bioengineering, Central South University, Changsha, 410083, People’s Republic of China

    Zhiguo He, Yuting Hu, Zhen Yin & Yuehua Hu

  2. Key Laboratory of Biohydrometallurgy of Ministry of Education, Central South University, Changsha, Hunan, 410083, People’s Republic of China

    Zhiguo He, Yuting Hu, Zhen Yin & Yuehua Hu

  3. School of Life Science, Central South University, Changsha, Hunan, 410012, People’s Republic of China

    Hui Zhong

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  1. Zhiguo He
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Correspondence to Zhiguo He.

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He, Z., Hu, Y., Yin, Z. et al. Microbial Diversity of Chromium-Contaminated Soils and Characterization of Six Chromium-Removing Bacteria. Environmental Management 57, 1319–1328 (2016). https://doi.org/10.1007/s00267-016-0675-5

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