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Enrichment and response of iron-metabolizing microorganisms and metabolic genes in the contaminated area of stratified stacking coal gangue dumps, Northern China

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Abstract

In the Xishan coalfield of northern China, the stratified stacking of soil and gangue was applied to limit the acid pollution from high-sulfur coal gangue. In this study, we found that stratified stacking can effectively neutralize the acidity, with the pH value of gangue-leaching water being 6.02–8.13. In contrast to the acidic contaminated area, most of the microorganisms in the study area sediment were neutrophilic, with the main genera being Arthrobacter, Pseudorhodobacter, Pseudomonas, and Rhodoferax. A variety of iron- and sulfur-metabolizing bacteria was discovered in the gangue-leaching sediment, with the total relative abundance ranging from 4.20 to 23.75%, of which the iron-reducing bacteria (FeRB) accounted for the highest percentage. The distributions of these functional microorganisms in the samples were significantly influenced by Fe and S. The co-occurrence network analysis revealed a significant positive correlation between the iron- and sulfur-metabolizing bacteria in the sediment (93.75%), indicating a strong reciprocal symbiotic relationship between these bacteria. The iron and sulfur metabolism genes in the sediment were predicted and compared based on the Tax4Fun functional prediction method. Results showed that functional genes related to iron metabolism were highly expressed in the gangue-leaching sediment. This study enhances the understanding of iron and sulfur metabolism in gangue-leaching contaminated areas.

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References

  • Ahmed E, Holmström SJM (2015) Microbe–mineral interactions: the impact of surface attachment on mineral weathering and element selectivity by microorganisms. Chem Geol 403:13–23

    Article  CAS  Google Scholar 

  • Aisen P, Listowsky I (1980) Iron Transport and storage proteins. Annu Rev Biochem 49:357–393

    Article  CAS  Google Scholar 

  • Akcil A, Koldas S (2005) Acid mine drainage (AMD): causes, treatment and case studies. J Clean Prod 14:1139–1145

    Article  Google Scholar 

  • Anekwe IMS, Isa YM (2023) Bioremediation of acid mine drainage-Review. Alex Eng J 65:1047–1075

    Article  Google Scholar 

  • Apprill A, Mcnally S, Parsons R, Weber L (2015) Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Microb Ecol 75:129–137

    Article  Google Scholar 

  • Aßhauer KP, Bernd W, Rolf D, Peter M (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882–2884

    Article  Google Scholar 

  • Aurélie V, Odile B, Angélique D, Marina H, Corinne C, Noëlle B, Sophie D, Anne F, Fabien J, Olivier B, Robert D, Philippe NB, Françoise E, Béatrice L (2014) Diversity and spatiotemporal dynamics of bacterial communities: physicochemical and other drivers along an acid mine drainage. Fems Microbiol Ecol 90:247–263

    Article  Google Scholar 

  • Bao Y-P (2018) Diversity of iron- and sulfur-cycling microorganism and the role of microbial activity in Fe(III) hydroxysulfate mineral transformations in a river affected by acid mine drainage. South China University of Technology, Guang zhou (in Chinese)

    Google Scholar 

  • Banerjee S, Schlaeppi K, Van DHMG (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 9:567–576

    Article  Google Scholar 

  • Camargo F, Bento FM, Okeke BC, Frankenberger WT (2004) Hexavalent chromium reduction by an actinomycete, Arthrobacter crystallopoietes ES 32. Biol Trace Elem Res 97:183–194

    Article  CAS  Google Scholar 

  • Campbell BJ, Polson SW, Hanson TE, Mack MC, Schuur EAG (2010) The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ Microbiol 12:1842–1854

    Article  CAS  Google Scholar 

  • Chakraborty A, Picardal F (2012) Neutrophilic, nitrate-dependent, Fe(II) oxidation by a Dechloromonas species. World J Microbiol Biotechnol 29:617–623

    Article  Google Scholar 

  • Chakraborty R, O’Connor SM, Chan E, Coates JD (2005) Anaerobic degradation of benzene, toluene, ethylbenzene, and xylene compounds by Dechloromonas strain RCB. Appl Environ Microbiol 71:8649–8655

    Article  CAS  Google Scholar 

  • Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand Stat Theory Appl 11:265–270

    Google Scholar 

  • Chao TC, Becker A, Buhrmester J, Puhler A, Weidner S (2004) The Sinorhizobium meliloti fur gene regulates, with dependence on Mn(II), transcription of the sitABCD operon, encoding a metal-type transporter. J Bacteriol 186:3609

    Article  CAS  Google Scholar 

  • Chaudhary DK, Kim J (2016) Novosphingobium naphthae sp. nov., from oil-contaminated soil. Int J Syst Evol Microbiol 66:3170–3176

    Article  CAS  Google Scholar 

  • Chen D, Feng Q, Liang H (2021) Effects of long-term discharge of acid mine drainage from abandoned coal mines on soil microorganisms: microbial community structure, interaction patterns, and metabolic functions. Environ Sci Pollut Res Int 28:53936–53952

    Article  CAS  Google Scholar 

  • Chen QH, Han YL, Yao MA, Yan YL, Ping SZ, Wei LU (2013) Research progress on structure and evolution of biological nitrogen-fixation gene cluster. J Agric Sci Technol 15:129–138

    CAS  Google Scholar 

  • De Vet WW, Dinkla IJ, Rietveld LC, Van Loosdrecht MC (2011) Biological iron oxidation by Gallionella spp. in drinking water production under fully aerated conditions. Water Res 45:5389–5398

    Article  Google Scholar 

  • Ding J (2015) Isolation of an iron reducing bacterium Sphingomonas sp. DJ and characterization of its ability in degradation of refractory substances. Dissertation, Dalian University of Technology (in Chinese), China

    Google Scholar 

  • Downie HF, Standerwick JP, Burgess L, Natrajan LS, Lloyd JR (2018) Imaging redox activity and Fe(II) at the microbe-mineral interface during Fe(III) reduction. Res Microbiol 169:582–589

    Article  CAS  Google Scholar 

  • Dwa B, Hui L, Quan MA, Yb A, Jq A (2021) Manganese oxides in Phragmites rhizosphere accelerates ammonia oxidation in constructed wetlands. Water Res 205:117688

    Article  Google Scholar 

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  CAS  Google Scholar 

  • Erwin S, Sabine H (1998) ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains. Fems Microbiol Rev 22:1–20

    Article  Google Scholar 

  • Fang WW, Gu MF, Liang DQ, Chen GH, Wang SQ (2020) Generation of zero valent sulfur from dissimilatory sulfate reduction under methanogenic conditions. J Hazard Mater 383:121197

    Article  CAS  Google Scholar 

  • Finneran KT, Johnsen CV, Lovley DR (2003) Rhodoferax ferrireducens sp. nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III). Int J Syst Evol Microbiol 53:669–673

    Article  CAS  Google Scholar 

  • Flynn DFB, Mirotchnick N, Jain M, Palmer MI, Naeem S (2011) Functional and phylogenetic diversity as predictors of biodiversity ecosystem function relationships. Ecology 92:1573–1581

    Article  Google Scholar 

  • Gao P, Sun X, Xiao E, Xu Z, Li B, Sun W (2019) Characterization of iron-metabolizing communities in soils contaminated by acid mine drainage from an abandoned coal mine in Southwest China. Environ Sci Pollut Res Int 26:9585–9598

    Article  CAS  Google Scholar 

  • Glockner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig W, Gade D, Beck A, Borzym K, Heitmann K (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci 100:8298–8303

    Article  CAS  Google Scholar 

  • Goff J, Yee N (2017) Tellurate enters Escherichia coli K-12 cells via the SulT-type sulfate transporter CysPUWA. Fems Microbiol Lett 354:x241

    Google Scholar 

  • Goltsman DSA (2009) Community genomic and proteomic analyses of chemoautotrophic iron-oxidizing “Leptospirillum rubarum” (group II) and “Leptospirillum ferrodiazotrophum” (group III) bacteria in acid mine drainage biofilms. Appl Environ Microbiol 75:4599–4615

    Article  CAS  Google Scholar 

  • Hamza I, Qi Z, King ND, O'Brian MR (2000) Fur-independent regulation of iron metabolism by Irr in Bradyrhizobium japonicum. Microbiology (N Y) 146:669–676

    CAS  Google Scholar 

  • Hanson BT, Yagi JM, Che OJ, Madsen EM (2012) Role of nitrogen fixation in the autecology of Polaromonas naphthalenivorans in contaminated sediments. Environ Microbiol 14:1544–1557

    Article  CAS  Google Scholar 

  • Hersman L, Huang A, Maurice P, Forsythe J (2000) Siderophore production and iron reduction by Pseudomonas mendocina in response to iron deprivation. Geomicrobiol J 17:261–273

    Article  CAS  Google Scholar 

  • Islam FS, Boothman C, Gault AG, Polya DA, Lloyd JR (2005) Potential role of the Fe(III)-reducing bacteria Geobacter and Geothrix in controlling arsenic solubility in Bengal delta sediments. Mineral Mag 69:865–875

    Article  CAS  Google Scholar 

  • Jeong HI, Jin HM, Jeon CO (2016) Complete genome sequence of Sphingorhabdus sp. M41, a versatile hydrocarbon degrader, isolated from crude oil-contaminated costal sediment. J Biotechnol 227:41–42

    Article  CAS  Google Scholar 

  • Jiang Y, Ma J, Ruan X, Chen X (2020) Compound health risk assessment of cumulative heavy metal exposure: a case study of a village near a battery factory in Henan Province, China. Environ Sci: Process Impacts 22:1408–1422

    CAS  Google Scholar 

  • Johnson DB, Hallberg KB (2003) The microbiology of acidic mine waters. Res Microbiol 154:466–473

    Article  CAS  Google Scholar 

  • Johnson DB, Hallberg KB (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338:3–14

    Article  CAS  Google Scholar 

  • Kumar M, Zeyad MT, Choudhary P, Paul S, Chakdar H, Singh Rajawat MV (2020) Thiobacillus. In: Beneficial Microbes in Agro-Ecology. Amaresan N, Senthil Kumar M, Annapurna K, Kumar K, Sankaranarayanan A (eds). Academic Press. pp 545-557

  • Li H-J, Peng J-J (2012) Recent advances in studies on dissimilatory Fe(III)-reducing microorganisms. Acta Ecologica Sinica 32:1633–1642 (in Chinese)

    Article  CAS  Google Scholar 

  • Li JY, Wang JM (2019) Comprehensive utilization and environmental risks of coal gangue: a review. J Clean Prod 239

  • Liu J-C, Xu H-J, Li J-J, Cui X-K, Guo S-B (2011) Study on thickness of key water isolated stratum above ordovician system in Gujiao mining area. Coal Eng 5:83–85 (in Chinese )

    Google Scholar 

  • Liu Y, Gong L, Mu X, Zhang Z, Zhou T, Zhang S (2020) Characterization and co-occurrence of microbial community in epiphytic biofilms and surface sediments of wetlands with submersed macrophytes. Sci Total Environ 715:136950–136951

    Article  CAS  Google Scholar 

  • Lu G-L, Zhang B, Wang Y-B, Gong Y-S, Li G-Q, Gu J, Wang W-P (2020) Study on coal gangue comprehensive treatment mode of Tunlan Mine. Modern Mining 36:209–212 (in Chinese)

    Google Scholar 

  • Lu Z, Hu H, Yao H (2012) Study on quantitative analysis method for several heavy metals in soil sample by inductively coupled plasma-mass spectrometry. Rocks Miner Anal (Chinese) 31:241–246

    CAS  Google Scholar 

  • Ma D, Liu X, Zhang M, Wang J, Hu X, Yan X, Tang C, Zhong J (2021) Bioremediation of heavy metals pollution from acidic coal gangue with sulfate-reducing bacteria. IOP Conf Ser: Earth Environ 634:12024–12026

    Article  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  Google Scholar 

  • Pantke C, Obst M, Benzerara K, Morin G, Ona-Nguema G, Dippon U, Kappler A (2012) Green rust formation during Fe(II) oxidation by the nitrate-reducing Acidovorax sp. strain BoFeN1. Environ Sci Technol 46:1439–1446

    Article  CAS  Google Scholar 

  • Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 5:1403–1414

    Article  Google Scholar 

  • Peng T, Zhou D, Liu Y, Yu R, Qiu G, Zeng W (2019) Effects of pH value on the expression of key iron/sulfur oxidation genes during bioleaching of chalcopyrite on thermophilic condition. Ann Microbiol 69:627–635

    Article  CAS  Google Scholar 

  • Qureshi A, Maurice C, Öhlander B (2016) Potential of coal mine waste rock for generating acid mine drainage. J Geochem Explor 160:44–54

    Article  CAS  Google Scholar 

  • Schiff JA (1979) Pathways of assimilatory sulphate reduction in plants and microorganisms. Sulphur in Biology 72:49–69

    Google Scholar 

  • Segura A, Hernández-Sánchez V, Marqués S, Molina L (2017) Insights in the regulation of the degradation of PAHs in Novosphingobium sp. HR1a and utilization of this regulatory system as a tool for the detection of PAHs. Sci Total Environ 590-591:381–393

    Article  CAS  Google Scholar 

  • Shannon C, Weaver W (1950) The mathematical theory of communication. Phys Today 3:31

    Article  Google Scholar 

  • Shi L, Rosso KM, Clarke TA, Richardson DJ, Zachara JM, Fredrickson JK (2012) Molecular underpinnings of Fe(III) oxide reduction by Shewanella Oneidensis MR-1. Front Microbiol 3:50

    Article  Google Scholar 

  • Sun W, Xiao E, Krumins V, Dong Y, Xiao T, Ning Z, Chen H, Xiao Q (2016) Characterization of the microbial community composition and the distribution of Fe-metabolizing bacteria in a creek contaminated by acid mine drainage. Appl Microbiol Biotechnol 100:8523–8535

    Article  CAS  Google Scholar 

  • Sun W, Xiao E, Pu Z, Krumins V, Dong Y, Li B, Hu M (2018) Paddy soil microbial communities driven by environment and microbe-microbe interactions: a case study of elevation-resolved microbial communities in a rice terrace. Sci Total Environ 612:884–893

    Article  CAS  Google Scholar 

  • The State Environmental Protection Administration (2002) Water and wastewater monitoring and analysis method, 4th edn. China Environmental Science Press, Beijing (in Chinese)

    Google Scholar 

  • Viguier C, Páraic C, Clarke P, O'Connell M (2005) RirA is the iron response regulator of the rhizobactin 1021 biosynthesis and transport genes in Sinorhizobium meliloti 2011. Fems Microbiol Lett 246:235–242

    Article  CAS  Google Scholar 

  • Vile MA, Wieder RK (1993) Alkalinity generation by Fe(III) reduction versus sulfate reduction in wetlands constructed for acid mine drainage treatment. Water Air Soil Pollut 3–4:425–441

    Article  Google Scholar 

  • Wang H-D (2005) Occurrence feature of the sulfur in coal seam 8# in Gujiao coal mining district in Shanxi province. Coal 4:17–19 (in Chinese)

    CAS  Google Scholar 

  • Wang L, Huang J-C, Li J (2017) The experimental research on the comprehensive treatment of gangue and acidic pit water with loess as the neutralizer. Mine Eng (Chinese) 5:55–62

    Article  Google Scholar 

  • Warthmann R, Cypionka H (1996) Characteristics of assimilatory sulfate transport in Rhodobacter sulfidophilus. FEMS Microbiol Lett 142:243–246

    Article  CAS  Google Scholar 

  • Watanabe T, Fukui M, Kojima H (2016) Sulfuriferula thiophila sp. nov., a chemolithoautotrophic sulfur-oxidizing bacterium. Int J Syst Evol Microbiol 66:2041

    Article  CAS  Google Scholar 

  • Williams RJ, Howe A, Hofmockel KS (2014) Demonstrating microbial co-occurrence pattern analyses within and between ecosystems. Front Microbiol 5:358

    Article  Google Scholar 

  • Xu Z-S, Chen J-R, Wang S-B, Li X-D, Shu Y-F, Li J, Shu X-Q (2021) Study on the grading and quality-separating processing and utilization of coal gangue. China Coal 47:61–68 (in Chinese)

    Google Scholar 

  • Yan S, Wu G (2017) Reorganization of gene network for degradation of polycyclic aromatic hydrocarbons (PAHs) in Pseudomonas aeruginosa PAO1 under several conditions. J Appl Genet 58:545–563

    Article  CAS  Google Scholar 

  • Yan Z, Zhang Y, Wu H, Yang M, Zhang H, Hao Z, Jiang H (2017) Isolation and characterization of a bacterial strain Hydrogenophaga sp. PYR1 for anaerobic pyrene and benzo[a]pyrene biodegradation. Rsc Adv 7:46690–46698

    Article  CAS  Google Scholar 

  • Yu Z, Yu R, Liu A, Liu J, Zeng W, Liu X, Qiu G (2017) Effect of pH values on extracellular protein and polysaccharide secretions of Acidithiobacillus ferrooxidans during chalcopyrite bioleaching. Trans Nonferrous Met Soc China 27:406–412

    Article  CAS  Google Scholar 

  • Zhang H, Sun H, Yang R, Li S, Zhou M, Gao T, An L, Chen X, Dyson P (2016) Complete genome sequence of a psychotrophic Pseudarthrobacter sulfonivoransstrain Ar51 (CGMCC 4.7316), a novel crude oil and multi benzene compounds degradation strain. J Biotechnol 231:81–82

    Article  CAS  Google Scholar 

  • Zhang X, Szewzyk U, Fang M (2017) Characterization of Aquabacterium parvum sp. strain B6 during nitrate-dependent Fe(II) oxidation batch cultivation with various impact factors. Trans Tianjin Univ 23:315–324

    Article  CAS  Google Scholar 

  • Zhao J, Zhang R, Xue C, Xun W, Sun L, Xu Y, Shen Q (2014) Pyrosequencing reveals contrasting soil bacterial diversity and community structure of two main winter wheat cropping systems in China. Microb Ecol 67:443

    Article  Google Scholar 

  • Zhang Z-Y (2017) The environment capacity and environmental research of the treatment for acid mine drainage with loess. Dissertation, Taiyuan University of Technology, China (in Chinese)

    Google Scholar 

  • Zhong W-H, Zhu B-T, Zhao C-G, Zhang X-B, Xu H-F, Yang S-P (2019) Factors affecting nitrogen removal from aquaculture wastewater by Rhodobacter azotoformans YLK20. Microbiol China 46:2146–2156 (in Chinese)

    Google Scholar 

  • Zhou N, Yao Y-J, Song W-J, He Z-W, Meng G-H, Liu Y (2020) Present situation and prospect of coal gangue treatment technology. J Min Saf Eng 37:136–146 (in Chinese)

    Google Scholar 

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Acknowledgements

Thanks to Min Gong and Xin Zhang for their valuable help in the collection of samples.

Funding

This work was supported by the Key Technologies Research and Development Program of China (Grant No. 2020YFC1806501) and the National Natural Science Foundation of China (No. 41977159).

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Authors and Affiliations

  1. Engineering Research Center of Ministry of Education for Mine Ecological Restoration, China University of Mining and Technology, No.1 Daxue Street, Quanshan District, Xuzhou, 221116, People’s Republic of China

    Chen Di, Feng Qiyan & Zhang Yun

  2. School of Environment Science and Spatial Informatics, China University of Mining and Technology, No.1 Daxue Street, Quanshan District, Xuzhou, 221116, People’s Republic of China

    Chen Di, Feng Qiyan & Zhang Yun

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All authors contributed to the study’s conception and design. Di Chen: conceptualization, methodology, investigation, data curation, software, validation, writing—original draft preparation. Qiyan Feng: conceptualization, investigation, resources provision, supervision. Yun Zhang: investigation, writing—review & editing.

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Correspondence to Feng Qiyan.

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Chen, D., Feng, Q. & Zhang, Y. Enrichment and response of iron-metabolizing microorganisms and metabolic genes in the contaminated area of stratified stacking coal gangue dumps, Northern China. Environ Sci Pollut Res 30, 63603–63619 (2023). https://doi.org/10.1007/s11356-023-26775-y

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