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Differences among active toluene-degrading microbial communities in farmland soils with different levels of heavy metal pollution

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Abstract

Heavy metals can severely influence the mineralisation of organic pollutants in a compound-polluted environment. However, to date, no study has focused on the effects of heavy metals on the active organic pollutant-degrading microbial communities to understand the bioremediation mechanism. In this study, toluene was used as the model organic pollutant to explore the effects of soils with different levels of heavy metal pollution on organic contaminant degradation in the same area via stable isotope probing (SIP) and 16 S rRNA high-throughput sequencing. Heavy metals can seriously affect toluene biodegradation and regulate the abundance and diversity of microbial communities. SIP revealed a drastic difference in the community structure of active toluene degraders between the unpolluted and heavy metal-polluted soils. All SIP-identified degraders were assigned to nine bacterial classes, among which Alphaproteobacteria, Gammaproteobacteria, and Bacilli were shared by both treatments. Among all active degraders, Nitrospira, Nocardioides, Conexibacteraceae, and Singulisphaera were linked to toluene biodegradation for the first time. Notably, the type of active degrader and microbial diversity were strongly related to biodegradation efficiency, indicating their key role in toluene biodegradation. Overall, heavy metals can affect the microbial diversity and alter the functional microbial communities in soil, thereby influencing the removal efficiency of organic contaminants. Our findings provide novel insights into the biodegradation mechanism of organic pollutants in heavy metal-polluted soils and highlight the biodiversity of microbes involved in toluene biodegradation in compound-polluted environments.

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References

  • Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Appolinario LR, Tschoeke D, Paixao RVS, Venas T, Calegario G, Leomil L et al (2019) Metagenomics sheds light on the metabolic repertoire of oil-biodegrading microbes of the South Atlantic Ocean. Environ Pollut 249:295–304

    Article  CAS  PubMed  Google Scholar 

  • Arsic M, Nikolic D, Mihajlovic I, Zivkovic Z (2014) Monitoring of the surface ozone concentrations in the western Banat Region (Serbia). Appl Ecol Environ Res 12:975–989

    Article  Google Scholar 

  • Azarbad H, Niklinska M, Nikiel K, van Straalen NM, Roling WFM (2015) Functional and compositional responses in soil microbial communities along two metal pollution gradients: does the level of historical pollution affect resistance against secondary stress? Biol Fertil Soils 51:879–890

    Article  CAS  Google Scholar 

  • Azubuike CC, Chikere CB, Okpokwasili GC (2016) Bioremediation techniques-classification based on site of application: principles, advantages, limitations and prospects. World J Microbiol Biotechnol 32:180

    Article  PubMed  PubMed Central  Google Scholar 

  • Bai XT, Wang JC, Dong HL, Chen JM, Ge Y (2021) Relative importance of soil properties and heavy metals/metalloids to modulate microbial community and activity at a smelting site. J Soils Sedim 21:1–12

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao WL, Hsu SF (2004) Response of the soil bacterial community to the addition of toluene and toluene-degrading bacteria. Soil Biol Biochem 36:479–487

    Article  CAS  Google Scholar 

  • Chen JH, He F, Zhang XH, Sun X, Zheng JF, Zheng JW (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  PubMed  Google Scholar 

  • Cheng ZY, Shi JC, He Y, Wu LS, Xu JM (2022) Assembly of root-associated bacterial community in cadmium contaminated soil following five-year consecutive application of soil amendments: evidences for improved soil health. J Haz Mater 426:128095

    Article  CAS  Google Scholar 

  • Datta R, Holatko J, Latal O, Hammerschmiedt T, Elbl J, Pecina V et al (2020) Bentonite-based organic amendment enriches microbial activity in agricultural soils. Land 9:258–258

    Article  Google Scholar 

  • Dobaradaran S, Schmidt TC, Kaziur-Cegla W, Jochmann MA (2021) BTEX compounds leachates from cigarette butts into water environment: a primary study. Environ Pollut 269:116185

    Article  CAS  PubMed  Google Scholar 

  • Dumont MG, Murrell JC (2005) Stable isotope probing—linking microbial identity to function. Nat Rev Microbiol 3:499–504

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez T (2011) Identifying polycyclic aromatic hydrocarbon-degrading bacteria in oil-contaminated surface waters at deepwater horizon by cultivation, stable isotope probing and pyrosequencing. Rev Environ Sci Bio Technol 10:301–305

    Article  CAS  Google Scholar 

  • Gutierrez T, Singleton DR, Berry D, Yang T, Aitken MD, Teske A (2013) Hydrocarbon-degrading bacteria enriched by the deepwater horizon oil spill identified by cultivation and DNA-SIP. ISME J 7:2091–2104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon CO, Park W, Padmanabhan P, DeRito C, Snape JR, Madsen EL (2003) Discovery of a bacterium, with distinctive dioxygenase, that is responsible for in situ biodegradation in contaminated sediment. Proc Natl Acad Sci USA 100:13591–13596

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang LF, Song MK, Yang L, Zhang DY, Sun YT, Shen ZG et al (2016) Exploring the influence of environmental factors on bacterial communities within the rhizosphere of the Cu-tolerant plant, Elsholtzia splendens. Sci Rep 6:36302

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang L, Luo C, Zhang D, Song M, Mei W, Sun Y et al (2021) Shifts in a phenanthrene-degrading microbial community are driven by carbohydrate metabolism selection in a ryegrass rhizosphere. Environ Sci Technol 55:962–973

    Article  ADS  CAS  PubMed  Google Scholar 

  • Kong J, Guo QJ, Wei RF, Strauss H, Zhu GX, Li SL et al (2018) Contamination of heavy metals and isotopic tracing of Pb in surface and profile soils in a polluted farmland from a typical karst area in southern China. Sci Total Environ 637:1035–1045

    Article  ADS  PubMed  Google Scholar 

  • Kutralam-Muniasamy G, Perez-Guevara F, Martinez IE, Shruti VC (2021) Overview of microplastics pollution with heavy metals: analytical methods, occurrence, transfer risks and call for standardization. J Haz Mater 415:125755

    Article  CAS  Google Scholar 

  • Lee J, Kim JR, Jeong S, Cho J, Kim JY (2017) Long-term performance of anaerobic digestion for crop residues containing heavy metals and response of microbial communities. Waste Manag 59:498–507

    Article  CAS  PubMed  Google Scholar 

  • Lewis WH, Tahon G, Geesink P, Sousa DZ, Ettema TJG (2021) Innovations to culturing the uncultured microbial majority. Nat Rev Microbiol 19:225–240

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Hu QJ, Zhang CL, Muller WEG, Schroder HC, Li ZY et al (2015) The effect of toxicity of heavy metals contained in tailing sands on the organic carbon metabolic activity of soil microorganisms from different land use types in the karst region. Environ Earth Sci 74:6747–6756

    Article  ADS  CAS  Google Scholar 

  • Li J, Luo C, Song M, Dai Q, Jiang L, Zhang D et al (2017) Biodegradation of phenanthrene in polycyclic aromatic hydrocarbon-contaminated wastewater revealed by coupling cultivation-dependent and -independent approaches. Environ Sci Technol 51:3391–3401

    Article  ADS  CAS  PubMed  Google Scholar 

  • Li J, Zhang D, Song M, Jiang L, Wang Y, Luo C et al (2017) Novel bacteria capable of degrading phenanthrene in activated sludge revealed by stable-isotope probing coupled with high-throughput sequencing. Biodegradation 28:423–436

    Article  PubMed  Google Scholar 

  • Li J, Luo C, Zhang D, Song M, Cai X, Jiang L et al (2018) Autochthonous bioaugmentation modified bacterial diversity of phenanthrene degraders in PAH-contaminated wastewater as revealed by DNA-stable isotope probing. Environ Sci Technol 52:2934–2944

    Article  ADS  CAS  PubMed  Google Scholar 

  • Li J, Luo C, Zhang G, Zhang D (2018) Coupling magnetic-nanoparticle mediated isolation (MMI) and stable isotope probing (SIP) for identifying and isolating the active microbes involved in phenanthrene degradation in wastewater with higher resolution and accuracy. Water Res 144:226–234

    Article  CAS  PubMed  Google Scholar 

  • Li J, Luo C, Zhang D, Cai X, Jiang L, Zhang G (2019) Stable-isotope probing enabled cultivation of the indigenous strain Ralstonia sp. M1 capable of degrading phenanthrene and biphenyl in industrial wastewater. Appl Environ Microbiol 85(14):e00511–e00519

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Li ZH, Wang W, Zhu LZ (2019) Effects of mixed surfactants on the bioaccumulation of polycyclic aromatic hydrocarbons (PAHs) in crops and the bioremediation of contaminated farmlands. Sci Total Environ 646:1211–1218

    Article  ADS  CAS  PubMed  Google Scholar 

  • Li BL, Wei ZS, Huang ZS, Xiao XL, Ming S, Jiao HY et al (2020) Removal of toluene from synthetic waste gas through aerobic denitrification in biotrickling reactor. Environ Eng Sci 37:769–781

    Article  CAS  Google Scholar 

  • Li J, Peng K, Zhang D, Luo C, Cai X, Wang Y et al (2020) Autochthonous bioaugmentation with non-direct degraders: a new strategy to enhance wastewater bioremediation performance. Environ Int 136:105473

    Article  CAS  PubMed  Google Scholar 

  • Li J, Luo C, Zhang D, Zhao X, Dai Y, Cai X et al (2021) The catabolic pathways of in situ rhizosphere PAH degraders and the main factors driving PAH rhizoremediation in oil-contaminated soil. Environ Microbiol 23:7042–7055

    Article  CAS  PubMed  Google Scholar 

  • Li J, Zhang D, Li B, Luo C, Zhang G (2022) Identifying the active phenanthrene degraders and characterizing their metabolic activities at the single-cell level by the combination of magnetic-nanoparticle-mediated isolation, stable-isotope probing, and raman-activated cell sorting (MMI–SIP–RACS). Environ Sci Technol 56:2289–2299

    Article  ADS  CAS  PubMed  Google Scholar 

  • Liang JD, Gao S, Wu ZJ, Rijnaarts HHM, Grotenhuis T (2021) DNA-SIP identification of phenanthrene-degrading bacteria undergoing bioaugmentation and natural attenuation in petroleum-contaminated soil. Chemosphere 266:128984

    Article  CAS  PubMed  Google Scholar 

  • Lin YB, Ye YM, Hu YM, Shi HK (2019) The variation in microbial community structure under different heavy metal contamination levels in paddy soils. Ecotoxicol Environ Saf 180:557–564

    Article  CAS  PubMed  Google Scholar 

  • Liu SH, Zeng GM, Niu QY, Liu Y, Zhou L, Jiang LH et al (2017) Bioremediation mechanisms of combined pollution of PAHs and heavy metals by bacteria and fungi: a mini review. Bioresour Technol 224:25–33

    Article  CAS  PubMed  Google Scholar 

  • Luo C, Xie S, Sun W, Li X, Cupples AM (2009) Identification of a novel toluene-degrading bacterium from the candidate phylum TM7, as determined by DNA stable isotope probing. Appl Environ Microbiol 75:4644–4647

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo C, Zhao X, Zhang D, Dai Y, Li Q, Wang S et al (2021) Toward a more comprehensive understanding of autochthonous bioaugmentation (ABA): cases of ABA for phenanthrene and biphenyl by Ralstonia sp. M1 in industrial wastewater. ACS ES&T Water 1:1390–1400

    Article  CAS  Google Scholar 

  • Maixner F, Wagner M, Lucker S, Pelletier E, Schmitz-Esser S, Hace K et al (2008) Environmental genomics reveals a functional chlorite dismutase in the nitrite-oxidizing bacterium ‘Candidatus nitrospira defluvii.’ Environ Microbiol 10:3043–3056

    Article  CAS  PubMed  Google Scholar 

  • Mierzwa-Hersztek M, Gondek K, Klimkowicz-Pawlas A, Baran A, Bajda T (2018) Sewage sludge biochars management-ecotoxicity, mobility of heavy metals, and soil microbial biomass. Environ Toxicol Chem 37:1197–1207

    Article  CAS  PubMed  Google Scholar 

  • Mikkonen A, Li T, Vesala M, Saarenheimo J, Ahonen V, Karenlampi S et al (2018) Biofiltration of airborne VOCs with green wall systems microbial and chemical dynamics. Indoor Air 28:697–707

    Article  CAS  Google Scholar 

  • Muller S, Vogt C, Laube M, Harms H, Kleinsteuber S (2009) Community dynamics within a bacterial consortium during growth on toluene under sulfate-reducing conditions. FEMS Microbiol Ecol 70:586–596

    Article  PubMed  Google Scholar 

  • Nguyen OT, Ha DD (2019) Degradation of chlorotoluenes and chlorobenzenes by the dual-species biofilm of comamonas testosteroni strain KT5 and Bacillus subtilis strain DKT. Ann Microbiol 69:267–277

    Article  CAS  Google Scholar 

  • Qin X, Wu T, Zhu Y, Shan X, Liu C, Tao N (2020) A paper based milli-cantilever sensor for detecting hydrocarbon gases via smartphone camera. Anal Chem 92:8480–8486

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro H, da Silva JG, Jesus J, Magalhaes C, Dias JM, Danko AS (2019) Biodegradation of biodiesel and toluene under nitrate-reducing conditions and the impact on bacterial community structure. J Soils Sedim 19:439–450

    Article  CAS  Google Scholar 

  • Sayqal A, Ahmed OB (2021) Advances in heavy metal bioremediation: an overview. Appl Bionics Biomech 2021:1609149

    Article  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Song MK, Wang YJ, Jiang LF, Peng K, Wei ZK, Zhang DY et al (2019) The complex interactions between novel DEHP-metabolising bacteria and the microbes in agricultural soils. Sci Total Environ 660:733–740

    Article  ADS  CAS  PubMed  Google Scholar 

  • Sun Y, Yin M, Zheng D, Wang T, Zhao X, Luo C et al (2021) Different acetonitrile degraders and degrading genes between anaerobic ammonium oxidation and sequencing batch reactor as revealed by stable isotope probing and magnetic-nanoparticle mediated isolation. Sci Total Environ 758:143588

    Article  ADS  CAS  PubMed  Google Scholar 

  • Thomas F, Corre E, Cebron A (2019) Stable isotope probing and metagenomics highlight the effect of plants on uncultured phenanthrene-degrading bacterial consortium in polluted soil. ISME J 13:1814–1830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu HP, Lai C, Zeng GM, Liang J, Chen J, Xu JJ et al (2017) The interactions of composting and biochar and their implications for soil amendment and pollution remediation: a review. Crit Rev Biotechnol 37:754–764

    Article  CAS  PubMed  Google Scholar 

  • Xie SG, Sun WM, Luo CL, Cupples AM (2010) Stable isotope probing identifies novel m-xylene degraders in soil microcosms from contaminated and uncontaminated sites. Water Air Soil Pollut 212:113–122

    Article  ADS  CAS  Google Scholar 

  • Yang MY, Zhang H, Ni JZ, Chen WF, Yang LM, Wei R (2020) Effect of cadmium on pyrene biodegradation in solution and soil using free and immobilized Escherichia sp. on biochar. Appl Soil Ecol 150:103472

    Article  Google Scholar 

  • Yi ML, Zhang LL, Qin CL, Lu PL, Bai HC, Han XK et al (2022) Temporal changes of microbial community structure and nitrogen cycling processes during the aerobic degradation of phenanthrene. Chemosphere 286:131709

    Article  CAS  PubMed  Google Scholar 

  • Yoshikawa M, Zhang M, Toyota K (2016) Enhancement and biological characteristics related to aerobic biodegradation of toluene with co-existence of benzene. Water Air Soil Pollut 227:1–11

    Article  CAS  Google Scholar 

  • Zhao X, Li J, Zhang D, Huang Z, Luo C, Jiang L et al (2022) Mechanism of salicylic acid in promoting the rhizosphere benzo[a]pyrene biodegradation as revealed by DNA-stable isotope probing. Sci Total Environ 810:152202

    Article  ADS  CAS  PubMed  Google Scholar 

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Acknowledgements

Financial support was provided by the Natural Science Foundation of Guangdong Province, China (2019A1515011862 & 2019A1515011033), National Key Technology R&D Program of China (2022YFD1700804), Guangdong Province Key Field R&D Project (2023B0202010027) and Guangzhou Science and Technology Plan Project (2023B03J1286).

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Authors and Affiliations

  1. National-Regional Joint Engineering Research Center for Soil Pollution Control and Remediation in South China, Guangdong Key Laboratory of Integrated Agroenvironmental Pollution Control and Management, Institute of Eco-environmental and Soil Sciences, Guangdong Academy of Sciences, Guangzhou, 510650, China

    Fei Dou, Yundang Wu & Chuanping Liu

  2. State Key Laboratory of Organic Geochemistry and Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China

    Jibing Li

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  1. Fei Dou
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Contributions

FD and CL designed the experiments; FD performed the experiments; FD, YW and JL collected and analysed the data; FD wrote the first draft of the manuscript; FD, JL, YW and CL revised the manuscript.

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Correspondence to Chuanping Liu.

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10532_2023_10057_MOESM1_ESM.doc

(Table S1) Experimental design of the study; (Table S2) Taxonomy of functional microbes; (Fig. S1) Residual toluene percentage in unpolluted (UP) and heavy metal-polluted (HP) microcosms; (Fig. S2) Relative abundance of 16 S rRNA-defined bacterial genera in UP and HP treatments after three days of incubation. The selected genera had a minimal relative abundance of > 1%. UP0 and HP0 represent the initial microbial communities in the UP and HP soil samples; (Fig. S3) Venn plot for the diversity of active toluene degraders in UP and HP treatments. Figures in different compartments indicate the number of degraders specific for or common to UP and HP treatments; (Fig. S4) Relative abundance of stable isotope probing (SIP)-identified operational taxonomic units (OTUs) in UP (a) and HP (b) treatments; (Fig. S5) (a) Relative abundance of all active toluene degraders across treatments. (b) 16 S rRNA gene copies in UP and HP microcosms after three days of incubation. (c) Copy numbers of 16 S rRNA genes of active toluene degraders in the heavy-DNA fractions of 13C_UP and 13C_HP microcosms after three days of incubation. Supplementary material 1 (DOC 672 kb)

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Dou, F., Wu, Y., Li, J. et al. Differences among active toluene-degrading microbial communities in farmland soils with different levels of heavy metal pollution. Biodegradation 35, 329–340 (2024). https://doi.org/10.1007/s10532-023-10057-y

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