Skip to main content
SpringerLink
Log in

The shifts of sediment microbial community phylogenetic and functional structures during chromium (VI) reduction

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The Lanzhou reach of the Yellow River, located at the upstream of Lanzhou, has been contaminated by heavy metals and polycyclic aromatic hydrocarbons over a long-time. We hypothesized that indigenous microbial communities would remediate those contaminants and some unique populations could play an important role in this process. In this study, we investigated the sediment microbial community structure and function from the Lanzhou reach. Sediment samples were collected from two nearby sites (site A and site B) in the Lanzhou reach along the Yellow River. Sediment geochemical property data showed that site A sediment samples contained significantly (p < 0.05) higher heavy metals than site B, such as chromium (Cr), manganese (Mn), and copper (Cu). Both site A and B samples were incubated with or without hexavalent chromium (Cr (VI)) for 30 days in the laboratory, and Cr (VI) reduction was only observed in site A sediment samples. After incubation, MiSeq sequencing of 16S rRNA gene amplicons revealed that the phylogenetic composition and structure of microbial communities changed in both samples, and especially Proteobacteria, as the most abundant phylum increased from 45.1 % to 68.2 % in site A, and 50.1 % to 71.3 % in site B, respectively. Some unique OTUs and populations affiliated with Geobacter, Clostridium, Desulfosporosinus and Desulfosporosinus might be involved in Cr (VI) reduction in site A. Furthermore, GeoChip 4.0 (a comprehensive functional gene array) data showed that genes involved in carbon and nitrogen cycling and metal resistance significantly (p < 0.05) increased in site A sediment samples. All the results indicated that indigenous sediment microbial communities might be able to remediate contaminants like Cr (VI), and this information provides possible strategies for future bioremediation of the Lanzhou reach.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alvarez AH, Moreno-Sanchez R and Cervantes C (1999) Chromate efflux by means of the ChrA chromate resistance protein from Pseudomonas aeruginosa. J Bacteriol: 7398–7400

  • Bjerregaard P and Hansen JC (2000) Organochlorines and heavy metals in pregnant women from the Disko Bay area in Greenland. Sci Total Environ: 195–202

  • Byrne C, Stokes HW and Ward KA (1988) Nucleotide sequence of the aceB gene encoding malate synthase A in Escherichia coli. Nucleic Acids Res 16(22):9342–9342

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L and Bauer M (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6(8): 1621–1624

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N and Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108(Supplement 1): 4516–4522

  • Cervantes C, Campos-Garcia J, Devars S, Gutierrez-Corona F, Loza-Tavera H, Torres-Guzman JC and Moreno-Sanchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25(3): 335–347

  • Chu PC, Chen Y, Lu S, Li Z and Lu Y (2008) Particulate air pollution in Lanzhou China. Environ Int: 698–713

  • Citak D and Tuzen M (2010) A novel preconcentration procedure using cloud point extraction for determination of lead, cobalt and copper in water and food samples using flame atomic absorption spectrometry. Food Chem Toxicol 48(5): 1399–1404

  • Degens BP, Schipper LA, Sparling GP and Duncan LC (2001) Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance? Soil Biol Biochem 33(9): 1143–1153

  • Faybishenko B, Hazen TC, Long PE, Brodie EL, Conrad ME, Hubbard SS, Christensen JN, Joyner D, Borglin SE and Chakraborty R (2008) In situ long-term reductive bioimmobilization of Cr (VI) in groundwater using hydrogen release compound. Environ Sci Technol 42(22): 8478–8485

  • Francis AJ, Dodge CJ, Lu F, Halada GP and Clayton CR (1994) XPS and XANES studies of uranium reduction by Clostridium sp. Environ Sci Technol 28(4): 636–639

  • Garavaglia L, Cerdeira SB and Vullo DL (2010) Chromium (VI) biotransformation by beta- and gamma-Proteobacteria from natural polluted environments: a combined biological and chemical treatment for industrial wastes. J Hazard Mater 175(1): 104–110. doi: 10.1016/j.jhazmat.2009.09.134

  • Gihring TM, Zhang G, Brandt CC, Brooks SC, Campbell JH, Carroll S, Criddle CS, Green SJ, Jardine P, Kostka JE, Lowe K, Mehlhorn TL, Overholt W, Watson DB, Yang Z, Wu WM and Schadt CW (2011) A limited microbial consortium is responsiblefor extended bioreduction of uranium in a contaminated aquifer. Appl Environ Microbiol  77(17): 5955–5965. doi: 10.1128/AEM.00220-11

  • Griffin AM, Morris VJ and Gasson MJ (1996) Genetic analysis of the acetan biosynthetic pathway in Acetobacter xylinum: nucleotide sequence analysis of the aceB, aceC, aceD and aceE genes. DNA Seq 6: 275–284

  • Hausmann B, Knorr K-H, Schreck K, Tringe SG, del Rio TG, Loy A and Pester M (2016) Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms. ISME J. doi: 10.1038/ismej.2016.42

  • He Z, Deng Y and Zhou J (2012) Development of functional gene microarrays for microbial community analysis. Curr Opin Biotechnol 23(1):49–55

  • He Z, Van Nostrand JD and Zhou J (2012) Applications of functional gene microarrays for profiling microbial communities. Curr Opin Biotechnol 23(3): 460–466

  • He Z, Xu M, Deng Y, Kang S, Kellogg L, Wu L, Van Nostrand JD, Hobbie SE, Reich PB and Zhou J (2010) Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. Ecol Lett 13(5): 564–575. doi: 10.1111/j.1461-0248.2010.01453.x

  • Hemme CL, Deng Y, Gentry TJ, Fields MW, Wu L, Barua S, Barry K, Tringe SG, Watson DB and He Z (2010) Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community. ISME J 4(5): 660–672

  • Hueso S, García C and Hernández T (2012) Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils. Soil Biol Biochem 50: 167–173

  • Jackson MLR and Barak P (2005) Soil chemical analysis: Advanced course. UW-Madison Libraries Parallel Press

  • Kandeler E, Deiglmayr K, Tscherko D, Bru D and Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72(9): 5957–5962. doi: 10.1128/AEM.00439-06

  • Kawaichi S, Ito N, Kamikawa R, Sugawara T, Yoshida T and Sako Y (2013) Ardenticatena maritima gen. nov., sp. nov., a ferric iron-and nitrate-reducing bacterium of the phylum ‘Chloroflexi’ isolated from an iron-rich coastal hydrothermal field, and description of Ardenticatenia classis nov. Int J Syst Evol Microbiol 63(8):2992–3002

  • Khan S, Hesham AE-L, Qiao M, Rehman S and He J-Z (2010) Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut R 17(2): 288–296

  • Liang Y, Van Nostrand JD, Deng Y, He Z, Wu L, Zhang X, Li G and Zhou J (2011) Functional gene diversity of soil microbial communities from five oil-contaminated fields in China. ISME J 5(3): 403–413

  • Liang Y, Van Nostrand JD, Lucie A, Peacock AD, Deng Y, Long PE, Resch CT, Wu L, He Z and Li G (2012) Microbial functional gene diversity with a shift of subsurface redox conditions during in situ uranium reduction. Appl Environ Microbiol 78(8): 2966–2972

  • Liu C, Xu J, Liu C, Zhang P and Dai M (2009) Heavy metals in the surface sediments in Lanzhou reach of yellow river, China. Bull Environ Contam Toxicol 82(1): 26–30

  • Liu L, Yuan Y, Li F-b and Feng C-h (2011) In-situ Cr (VI) reduction with electrogenerated hydrogen peroxide driven by iron-reducing bacteria. Bioresour Technol 102(3): 2468–2473

  • Liu Y, Fredrickson JK, Zachara JM and Shi L (2015) Direct involvement of ombB, omaB, and omcB genes in extracellular reduction of Fe (III) by Geobacter sulfurreducens PCA. Front Microbiol 6

  • Loman NJ, Constantinidou C, Chan JZ, Halachev M, Sergeant M, Penn CW, Robinson ER and Pallen MJ (2012) High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity. Nat Rev Microbiol 10(9): 599–606. doi: 10.1038/nrmicro2850

  • Lovley DR and Phillips EJP (1994) Reduction of Chromate by Desulfovibrio vulgaris and Its c3 Cytochrome. Appl Environ Microbiol 60(2): 726–728

  • Lu R (2000) Soil agricultural chemical analysis. China Agricultural Science and Technology Press, Beijing: 1–315

    Google Scholar 

  • McDonald IR and Murrell JC (2006) The particulate methane monooxygenase gene pmoA and its use as a functional gene probe for methanotrophs. FEMS Microbiol Lett 156(2): 205–210

  • Nagajyoti P, Lee K and Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3): 199–216

  • Nie M, Pendall E, Bell C, Gasch CK, Raut S, Tamang S and Wallenstein MD (2013) Positive climate feedbacks of soil microbial communities in a semi-arid grassland. Ecol Lett 16(2): 234–241

  • Nies A, Nies DH and Silver S (1990) Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant from Alcaligenes eutrophus. J Biol Chem 265(10): 5648–5653

  • Nies DH, Koch S, Wachi S, Peitzsch N and Saier MH, Jr. (1998) CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulfate antiporters. J Bacteriol 180(21): 5799–5802

  • Nowakowska J and Oliver JD (2013) Resistance to environmental stresses by Vibrio vulnificus in the viable but nonculturable state. FEMS Microbiol Ecol 84(1): 213–222. doi: 10.1111/1574-6941.12052

  • Olmedo P, Pla A, Hernández A, López-Guarnido O, Rodrigo L and Gil F (2010) Validation of a method to quantify chromium, cadmium, manganese, nickel and lead in human whole blood, urine, saliva and hair samples by electrothermal atomic absorption spectrometry. Anal Chim Acta 659(1): 60–67

  • Orellana R, Leavitt JJ, Comolli LR, Csencsits R, Janot N, Flanagan KA, Gray AS, Leang C, Izallalen M and Mester T (2013) U (VI) reduction by diverse outer surface c-type cytochromes of Geobacter sulfurreducens. Appl Environ Microbiol 79(20): 6369–6374

  • Otwell AE, Callister SJ, Zink EM, Smith RD and Richardson RE (2016) Comparative proteomic analysis of Desulfotomaculum reducens MI-1: insights into the metabolic versatility of a gram-positive sulfate-and metal-reducing bacterium. Front Microbiol 7: 191

  • Pepi M, Focardi S, Tarabelli A, Volterrani M and Focardi S (2013) Bacterial strains resistant to inorganic and organic forms of mercury isolated from polluted sediments of the Orbetello Lagoon, Italy, and their possible use in bioremediation processes. E3S Web of Conferences (Vol. 1). EDP Sciences, pp 31002

  • Pester M, Bittner N, Deevong P, Wagner M and Loy A (2010) A ‘rare biosphere’ microorganism contributes to sulfate reduction in a peatland. ISME J 4(12): 1591–1602

  • Piccirillo C, Pereira SI, Marques AP, Pullar RC, Tobaldi DM, Pintado ME and Castro PM (2013) Bacteria immobilisation on hydroxyapatite surface for heavy metals removal. J Environ Manage 121: 87–95. doi: 10.1016/j.jenvman.2013.02.036

  • Puskas LG, Inui M and Yukawa H (2000) Structure of the urease operon of Corynebacterium glutamicum. DNA Seq 11(5): 383–394, 467

  • Roberts GP, MacNeil T, MacNeil D and Brill WJ (1978) Regulation and characterization of protein products coded by the nif (nitrogen fixation) genes of Klebsiella pneumoniae. J Bacteriol 136(1): 267–279

  • Samanovic MI, Ding C, Thiele DJ and Darwin KH (2012) Copper in microbial pathogenesis: meddling with the metal. Cell Host Microbe 11(2): 106–115

  • Shelobolina ES, Coppi MV, Korenevsky AA, DiDonato LN, Sullivan SA, Konishi H, Xu H, Leang C, Butler JE and Kim B-C (2007) Importance of c-type cytochromes for U (VI) reduction by Geobacter sulfurreducens. BMC Microbiol 7(1): 1

  • Slobodkin A, Tourova T, Kostrikina N, Lysenko A, German K, Bonch-Osmolovskaya E and Birkeland N-K (2006) Tepidimicrobium ferriphilum gen. nov., sp. nov., a novel moderately thermophilic, Fe (III)-reducing bacterium of the order Clostridiales. Int J Syst Evol Microbiol 56(2): 369–372

  • Somenahally AC, Mosher JJ, Yuan T, Podar M, Phelps TJ, Brown SD, Yang ZK, Hazen TC, Arkin AP and Palumbo AV (2013) Hexavalent chromium reduction under fermentative conditions with lactate stimulated native microbial communities. PloS One 56(2): 369–372

  • Ta W, Wang T, Xiao H, Zhu X and Xiao Z (2004) Gaseous and particulate air pollution in the Lanzhou Valley, China. Sci Total Environ 320(2): 163–176

  • Team RDC (2010). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, 2007. ISBN 3-900051-07-0

    Google Scholar 

  • Tebo BM and Obraztsova AY (1998) Sulfate-reducing bacterium grows with Cr (VI), U (VI), Mn (IV), and Fe (III) as electron acceptors. FEMS Microbiol Lett 162(1): 193–199

  • Tien C-J, Lin M-C, Chiu W-H and Chen CS (2013) Biodegradation of carbamate pesticides by natural river biofilms in different seasons and their effects on biofilm community structure. Environ Pollut 179: 95–104

  • Tu Q, Yu H, He Z, Deng Y, Wu L, Nostrand JD, Zhou A, Voordeckers J, Lee YJ and Qin Y (2014) GeoChip 4: a functional gene array based high‐throughput environmental technology for microbial community analysis. Mol Ecol Resour 14(5): 914–928

  • Velma V and Tchounwou PB (2013) Oxidative stress and DNA Damage Induced by chromium in Liver and Kidney of Goldfish, Carassius auratus. Biomark Insights 8: 43

  • Wang Q, Garrity GM, Tiedje JM and Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16): 5261–5267

  • Wang Y, Chen P, Cui R, Si W, Zhang Y and Ji W (2010) Heavy metal concentrations in water, sediment, and tissues of two fishspecies (Triplohysa pappenheimi, Gobio hwanghensis) from the Lanzhou section of the Yellow River, China. Environ Monit Assess 165(1–4): 97–102

  • Westergaard K, Müller A, Christensen S, Bloem J and Sørensen S (2001) Effects of tylosin as a disturbance on the soil microbial community. Soil Biol Biochem 33(15): 2061–2071

  • Xiaoyan T, Jinlong L and Zhenxing D (1989) Photochemical pollution in Lanzhou, China-a case study. J Environ Sci (China) 1: 31–38

  • Xu M, Wu WM, Wu L, He Z, Van Nostrand JD, Deng Y, Luo J, Carley J, Ginder-Vogel M, Gentry TJ, Gu B, Watson D, Jardine PM, Marsh TL, Tiedje JM, Hazen T, Criddle CS and Zhou J (2010) Responses of microbial community functional structures to pilot-scale uranium in situ bioremediation. ISME J 4(8): 1060–1070. doi: 10.1038/ismej.2010.31

  • Yan Z and Desheng L (2007) An analysis of water pollution along Lanzhou reaches of yellow river and its prevention [J]. Environ Sci Manage: 054

  • Zeng J, Yang S, Xu W, Wang S and Nan Z (2007) Analysis of the top soil pollution of Cu, Zn, Pb in the different city zones of Lanzhou. J Lanzhou Univ Nat Sci 43(1): 24

  • Zhang X-H, Zhang X, Wang X-C, Jin L-F, Yang Z-P, Jiang C-X, Chen Q, Ren X-B, Cao J-Z and Wang Q (2011) Chronic occupational exposure to hexavalent chromium causes DNA damage in electroplating workers. BMC Public Health 11(1): 1

  • Zhang X, Wu W, Virgo N, Zou L, Liu P and Li X (2014) Global transcriptome analysis of hexavalent chromium stress responses in Staphylococcus aureus LZ-01. Ecotoxicology 23(8): 1534-1545. doi: 10.1007/s10646-014-1294-7

  • Zhao C-c, Nan Z-r, Wang S-l, Zeng J-j, Liu J and Jin W-q (2010) Spatial distribution and pollution assessment of heavy metals in soil of main districts of Lanzhou City. Urban Environ Urban Ecol 3: 002

Download references

Acknowledgments

This work was supported by National Natural Science Foundation grant 31200085 to X. Li and 31100888 to P. Liu.

Author information

Author notes

    Authors and Affiliations

    1. Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou, Gansu, 730000, China

      Zhengsheng Yu, Xuanyu Tao, Xiaowei Zhang, Zhe Zheng, Pu Liu, Yong Chen, Virgo Nolan & Xiangkai Li

    2. Department of Microbiology and Plant Biology and Institute for Environmental Genomics, University of Oklahoma, Norman, OK, 73019, USA

      Zhili He, Jizhong Zhou & Tong Yuan

    3. State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China

      Yunfeng Yang & Mengxin Zhao

    Authors
    1. Zhengsheng Yu
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Zhili He
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Xuanyu Tao
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Jizhong Zhou
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Yunfeng Yang
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Mengxin Zhao
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Xiaowei Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Zhe Zheng
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Tong Yuan
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. Pu Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    11. Yong Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    12. Virgo Nolan
      View author publications

      You can also search for this author in PubMed Google Scholar

    13. Xiangkai Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Xiangkai Li.

    Ethics declarations

    Conflict of interest

    The authors declare that they have no conflict interest.

    Additional information

    Zhengsheng Yu and Zhili He contributed equally to this work.

    Electronic supplementary material

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Yu, Z., He, Z., Tao, X. et al. The shifts of sediment microbial community phylogenetic and functional structures during chromium (VI) reduction. Ecotoxicology 25, 1759–1770 (2016). https://doi.org/10.1007/s10646-016-1719-6

    Download citation

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10646-016-1719-6

    Keywords

    Search

    Navigation