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Drivers for Efficient Bioaugmentation and Clean-Up of Contaminated Soil

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The Handbook of Environmental Chemistry

Abstract

Bioaugmentation constitutes a viable approach for the bioremediation of soils polluted by organic chemicals, but limitations may arise due to the poor in situ performance of the inoculated microorganisms. This chapter examines these – poorly understood – drawbacks in the light of the latest advances in microbial ecology and bioremediation strategies. We discuss how biotic and abiotic factors may compromise the establishment and activity of microbial inoculants in soil, as well as how to design efficient inoculants that exhibit increased robustness and dispersal. Innovative approaches could include taking advantage of microbial networks through bacterial consortia with complementary catabolic capabilities, and fungal- and plant-bacterial associations that provide an enhanced bacterial dispersion in water-unsaturated soil conditions. We also provide recommendations on the most convenient strategies for inoculant production and application, considering their mass production, the optimal dosing ratios and the optimised use of platforms for microbial action in soil, such as solid carriers (e.g. biochar) and plants.

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References

  1. Singh P, Jain R, Srivastava N, Borthakur A, Pal DB, Singh R, Madhav S, Srivastava P, Tiwary D, Pradeep, Mishra K, Mishra PK (2017) Current and emerging trends in bioremediation of petrochemical waste: a review. Crit Rev Environ Sci Technol 47:155–201. https://doi.org/10.1080/10643389.2017.1318616

    Article  Google Scholar 

  2. Alkorta I, Garbisu C (2021) Reflections and insights on the evolution of the biological remediation of contaminated soils. Front Environ Sci:9. https://doi.org/10.3389/fenvs.2021.734628

  3. Cycoń M, Mrozik A, Piotrowska-Seget Z (2017) Bioaugmentation as a strategy for the remediation of pesticide-polluted soil: a review. Chemosphere 172:52–71. https://doi.org/10.1016/J.CHEMOSPHERE.2016.12.129

    Article  Google Scholar 

  4. Garbisu C, Garaiyurrebaso O, Epelde L, Grohmann E, Alkorta I (2017) Plasmid-mediated bioaugmentation for the bioremediation of contaminated soils. Front Microbiol 8:1966. https://doi.org/10.3389/FMICB.2017.01966/BIBTEX

    Article  Google Scholar 

  5. Tripathi V, Edrisi SA, Chen B, Gupta VK, Vilu R, Gathergood N, Abhilash PC (2017) Biotechnological advances for restoring degraded land for sustainable development. Trends Biotechnol 35:847–859. https://doi.org/10.1016/J.TIBTECH.2017.05.001

    Article  Google Scholar 

  6. Wang B, Teng Y, Li R, Meng K, Xu Y, Liu S, Luo Y (2023) Exploring the PAHs dissipation and indigenous bacteria response in soil amended with two different microbial inoculants. Sci Total Environ 859:160186. https://doi.org/10.1016/J.SCITOTENV.2022.160186

    Article  Google Scholar 

  7. Guarino C, Spada V, Sciarrillo R (2017) Assessment of three approaches of bioremediation (natural attenuation, landfarming and bioagumentation – assistited landfarming) for a petroleum hydrocarbons contaminated soil. Chemosphere 170:10–16. https://doi.org/10.1016/J.CHEMOSPHERE.2016.11.165

    Article  Google Scholar 

  8. Salam JA, Hatha MAA, Das N (2017) Microbial-enhanced lindane removal by sugarcane (Saccharum officinarum) in doped soil-applications in phytoremediation and bioaugmentation. J Environ Manage 193:394–399., ISSN 0301-4797. https://doi.org/10.1016/j.jenvman.2017.02.006

    Article  Google Scholar 

  9. Chuang S, Yang H, Wang X, Xue C, Jiang J, Hong Q (2021) Potential effects of Rhodococcus qingshengii strain djl-6 on the bioremediation of carbendazim-contaminated soil and the assembly of its microbiome. J Hazard Mater 414:125496., ISSN 0304-3894. https://doi.org/10.1016/j.jhazmat.2021.125496

    Article  Google Scholar 

  10. Jia W, Li N, Yang T, Dai W, Jiang J, Chen K, Xu X (2021) Bioaugmentation of atrazine-contaminated soil with Paenarthrobacter sp. strain AT-5 and its effect on the soil microbiome. Front Microbiol 12. https://doi.org/10.3389/fmicb.2021.771463

  11. Wojtowicz K, Steliga T (2020) Study on bioremediation of soil contaminated with polychlorinated biphenyls (PCBs). Nafta-Gaz 8:507–516. https://doi.org/10.18668/ng.2020.08.03

    Article  Google Scholar 

  12. Simmer R, Mathieu J, da Silva MLB, Lashmit P, Gopishetty S, Alvarez PJJ, Schnoor JL (2020) Bioaugmenting the poplar rhizosphere to enhance treatment of 1,4-dioxane. Sci Total Environ 744:140823. https://doi.org/10.1016/j.scitotenv.2020.140823

    Article  Google Scholar 

  13. Bai N, Li S, Zhang J, Zhang H, Zhang H, Zheng X, Lv W (2020) Efficient biodegradation of DEHP by CM9 consortium and shifts in the bacterial community structure during bioremediation of contaminated soil. Environ Pollut 266:115112. https://doi.org/10.1016/j.envpol.2020.115112

    Article  Google Scholar 

  14. Papadopoulou ES, Genitsaris S, Omirou M, Perruchon C, Stamatopoulou A, Ioannides J, Karpouzas DG (2018) Bioaugmentation of thiabendazole-contaminated soils from a wastewater disposal site: factors driving the efficacy of this strategy and the diversity of the indigenous soil bacterial community. Environ Pollut 233:16–25. https://doi.org/10.1016/j.envpol.2017.10.021

    Article  Google Scholar 

  15. Zhou N, Guo H, Liu Q, Zhang Z, Sun J, Wang H (2022) Bioaugmentation of polycyclic aromatic hydrocarbon (PAH)-contaminated soil with the nitrate-reducing bacterium PheN7 under anaerobic condition. J Hazard Mater 439:129643. https://doi.org/10.1016/j.jhazmat.2022.129643

    Article  Google Scholar 

  16. Imam A, Kumar Suman S, Kanaujia PK, Ray A (2022) Biological machinery for polycyclic aromatic hydrocarbons degradation: a review. Bioresour Technol 343:126121. https://doi.org/10.1016/J.BIORTECH.2021.126121

    Article  Google Scholar 

  17. Vila J, Tauler M, Grifoll M (2015) Bacterial PAH degradation in marine and terrestrial habitats. Curr Opin Biotechnol 2015(33):95–102. https://doi.org/10.1016/j.copbio.2015.01.006

    Article  Google Scholar 

  18. Kaminsky LM, Trexler RV, Malik RJ, Hockett KL, Bell TH (2019) The inherent conflicts in developing soil microbial inoculants. Trends Biotechnol 37:140–151. https://doi.org/10.1016/J.TIBTECH.2018.11.011

    Article  Google Scholar 

  19. Vanbroekhoven K, Ryngaert A, Bastiaens L, Wattiau P, Vancanneyt M, Swings J, De Mot R, Springael D (2004) Streptomycin as a selective agent to facilitate recovery and isolation of introduced and indigenous Sphingomonas from environmental samples. Environ Microbiol 6(11):1123–1136. https://doi.org/10.1111/j.1462-2920.2004.00654.x

    Article  Google Scholar 

  20. Stevenson BS, Eichorst SA, Wertz JT, Schmidt TM, Breznak JA (2004) New strategies for cultivation and detection of previously uncultured microbes. Appl Environ Microbiol 70:4748–4755. https://doi.org/10.1128/AEM.70.8.4748-4755.2004

    Article  Google Scholar 

  21. Jiménez-Volkerink SN, Vila J, Jordán M, Minguillón C, Smidt H, Grifoll M (2023) Multi-omic profiling of a newly isolated oxy-PAH degrading specialist from PAH-contaminated soil reveals bacterial mechanisms to mitigate the risk posed by polar transformation products. Environ Sci Technol 57(1):139–149. https://doi.org/10.1021/acs.est.2c05485

    Article  Google Scholar 

  22. Espinosa-Ortiz EJ, Rene ER, Gerlach R (2022) Potential use of fungal-bacterial co-cultures for the removal of organic pollutants. Crit Rev Biotechnol 42(3):361–383. https://doi.org/10.1080/07388551.2021.1940831

    Article  Google Scholar 

  23. Furuno S, Remer R, Chatzinotas A, Harms H, Wick LY (2012) Use of mycelia as paths for the isolation of contaminant-degrading bacteria from soil. J Microbial Biotechnol 5(1):142–148

    Google Scholar 

  24. Junier P, Cailleau G, Palmieri I, Vallotton C et al (2021) Democratization of fungal highway columns as a tool to investigate bacteria associated with soil fungi. FEMS Microbiol Ecol 97:fiab003

    Google Scholar 

  25. Huys GR, Raes J (2018) Go with the flow or solitary confinement: a look inside the single-cell toolbox for isolation of rare and uncultured microbes. Curr Opin Microbiol 44:1–8. https://doi.org/10.1016/J.MIB.2018.05.002

    Article  Google Scholar 

  26. Shan Y, Guo Y, Jiao W, Zeng P (2023) Single-cell techniques in environmental microbiology. Processes 11:1109. https://doi.org/10.3390/pr11041109

    Article  Google Scholar 

  27. Berdy B, Spoering AL, Ling LL, Epstein SS (2017) In situ cultivation of previously uncultivable microorganisms using the ichip. Nat Protoc 12:2232–2242. https://doi.org/10.1038/nprot.2017.074

    Article  Google Scholar 

  28. O’Callaghan M, Ballard RA, Wright D (2022) Soil microbial inoculants for sustainable agriculture: limitations and opportunities. Soil Use Manage 38:1340–1369. https://doi.org/10.1111/SUM.12811

    Article  Google Scholar 

  29. Ghosh S, Sharma I, Nath S, Webster TJ (2021) Bioremediation – the natural solution. Microb Ecol Wastewater Treatment Plants:11–40. https://doi.org/10.1016/B978-0-12-822503-5.00018-7

  30. Gao D, Zhao H, Wang L, Li Y, Tang T, Bai Y, Liang H (2022) Current and emerging trends in bioaugmentation of organic contaminated soils: a review. J Environ Manage 320:115799. https://doi.org/10.1016/J.JENVMAN.2022.115799

    Article  Google Scholar 

  31. Saravanan A, Senthil Kumar P, Vo D-VN, Jeevanantham S, Karishma S, Yaashikaa PR (2021) A review on catalytic-enzyme degradation of toxic environmental pollutants: microbial enzymes. J Hazard Mater 419:126451., ISSN 0304-3894. https://doi.org/10.1016/j.jhazmat.2021.126451

    Article  Google Scholar 

  32. Zhong H, Liu G, Jiang Y, Yang J, Yang L, Yang X, Liu Z, Zeng G (2017) Transport of bacteria in porous media and its enhancement by surfactants for bioaugmentation: a review. Biotechnol Adv 35(4):490–504., ISSN 0734-9750. https://doi.org/10.1016/j.biotechadv.2017.03.009

    Article  Google Scholar 

  33. Wu M, Jialuo W, Zhang X, Ye X (2019) Effect of bioaugmentation and biostimulation on hydrocarbon degradation and microbial community composition in petroleum-contaminated loessial soil. Chemosphere 237:124456., ISSN 0045-6535. https://doi.org/10.1016/j.chemosphere.2019.124456

    Article  Google Scholar 

  34. Albright MBN, Louca S, Winkler DE et al (2022) Solutions in microbiome engineering: prioritizing barriers to organism establishment. ISME J 16:331–338. https://doi.org/10.1038/s41396-021-01088-5

    Article  Google Scholar 

  35. Delgado-Baquerizo M, Maestre F, Reich P et al (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541

    Article  Google Scholar 

  36. Vogel TM (1996) Bioaugmentation as a soil bioremediation approach. Curr Opin Biotechnol 7:311–316. https://doi.org/10.1016/S0958-1669(96)80036-X

    Article  Google Scholar 

  37. Sprocati AR, Alisi C, Tasso F, Marconi P, Sciullo A, Pinto V, Chiavarini S, Ubaldi C, Cremisini C (2012) Effectiveness of a microbial formula, as a bioaugmentation agent, tailored for bioremediation of diesel oil and heavy metal co-contaminated soil. Process Biochem 47:1649–1655. https://doi.org/10.1016/J.PROCBIO.2011.10.001

    Article  Google Scholar 

  38. Horemans B, Breugelmans P, Saeys W, Springael D (2017) Soil-bacterium compatibility model as a decision-making tool for soil bioremediation. Environ Sci Technol 51:1605–1615. https://doi.org/10.1021/ACS.EST.6B04956/ASSET/IMAGES/LARGE/ES-2016-049569_0003.JPEG

    Article  Google Scholar 

  39. Wick LY (2020) Bioavailability as a microbial system property: lessons learned from biodegradation in the mycosphere. In: Ortega-Calvo J-J, Parsons JR (eds) Bioavailability of organic chemicals in soil and sediment. Handbook of environmental chemistry series, vol 100. Springer, Berlin, pp 267–289

    Google Scholar 

  40. Niqui-Arroyo JL, Bueno-Montes M, Ortega-Calvo JJ (2011) Biodegradation of anthropogenic organic compounds in natural environments. Biophysico-chemical processes of anthropogenic organic compounds in environmental systems. In: Xing B, Senesi N, Huang PM (eds) IUPAC series on biophysico-chemical processes in environmental systems, vol 3. Wiley, Chichester. ISBN: 978-0-470-53963-7, pp 483–501. https://doi.org/10.1002/9780470944479.ch19

    Chapter  Google Scholar 

  41. Alexander M (2000) Aging, bioavailability, and overestimation of risk from enviromental pollutants. Environ Sci Technol 34:4259–4265. https://doi.org/10.1021/es001069+

    Article  Google Scholar 

  42. Tiwari M, Tripathy DB (2023) Soil contaminants and their removal through surfactant-enhanced soil remediation: a comprehensive review. Sustainability 15:13161. https://doi.org/10.3390/su151713161

    Article  Google Scholar 

  43. Bueno-Montes M, Springael D, Ortega-Calvo JJ (2011) Effect of a non-ionic surfactant on biodegradation of slowly desorbing PAHs in contaminated soils. Environ Sci Technol 45:3019–3026. https://doi.org/10.1021/es1035706

    Article  Google Scholar 

  44. Zhu H, Aitken MD (2010) Surfactant-enhanced desorption and biodegradation of polycyclic aromatic hydrocarbons in contaminated soil. Environ Sci Technol 44:7260–7265. https://doi.org/10.1021/es100112a

    Article  Google Scholar 

  45. Congiu E, Ortega-Calvo J-J (2014) Role of desorption kinetics in the rhamnolipid enhanced biodegradation of polycyclic aromatic hydrocarbons. Environ Sci Technol 48:10869–10877. https://doi.org/10.1021/es5011253

  46. Posada-Baquero R, Grifoll M, Ortega-Calvo J-J (2019) Rhamnolipid-enhanced solubilization and biodegradation of PAHs in soils after conventional bioremediation. Sci Total Environ 668:790–796. https://doi.org/10.1016/j.scitotenv.2019.03.056

  47. Posada-Baquero R, Lopez-Martin M, Ortega-Calvo J-J (2019) Implementing standardized desorption extraction into bioavailability-oriented bioremediation of PAH polluted soils. Sci Total Environ 696:134011. https://doi.org/10.1016/j.scitotenv.2019.134011

  48. Posada-Baquero R, Jiménez-Volkerink SN, García JL, Vila J, Cantos M, Grifoll M, Ortega-Calvo JJ (2020) Rhizosphere-enhanced biosurfactanct action on slowly desorbing PAHs in contaminated soil. Sci Total Environ 720:137608. https://doi.org/10.1016/j.scitotenv.2020.137608

    Article  Google Scholar 

  49. Ortega-Calvo JJ, Stibany F, Semple KT, Schaeffer A, Parsons JR, Smith KCE (2020) Why biodegradable chemicals persist in the environment? A look at bioavailability. In: Ortega-Calvo J-J, Parsons JR (eds) Bioavailability of organic chemicals in soil and sediment. Handbook of environmental chemistry series, vol 100. Springer, Berlin, pp 243–266. https://doi.org/10.1007/698_2020_586

    Chapter  Google Scholar 

  50. Passatore L, Rossetti S, Juwarkar AA, Massacci A (2014) Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): state of knowledge and research perspectives. J Hazard Mater 278:189–202. https://doi.org/10.1016/J.JHAZMAT.2014.05.051

    Article  Google Scholar 

  51. Subramanian S, Schnoor JL, Van Aken B (2017) Effects of polychlorinated biphenyls (PCBs) and their hydroxylated metabolites (OH-PCBs) on Arabidopsis thaliana. Environ Sci Technol 51:7263–7270. https://doi.org/10.1021/acs.est.7b01538

    Article  Google Scholar 

  52. Thavamani P, Megharaj M, Krishnamurti GSR, McFarland R, Naidu R (2011) Finger printing of mixed contaminants from former manufactured gas plant (MGP) site soils: Implications to bioremediation. Environ Int 37:184–189. https://doi.org/10.1016/j.envint.2010.08.017

    Article  Google Scholar 

  53. Zhang H, Yuan X, Xiong T, Wang H, Jiang L (2020) Bioremediation of co-contaminated soil with heavy metals and pesticides: influence factors, mechanisms and evaluation methods. Chem Eng J 398:125657. https://doi.org/10.1016/j.cej.2020.125657

    Article  Google Scholar 

  54. Ye S, Zeng G, Wu H, Zhang C, Liang J, Dai J, Liu Z, Xiong W, Wan J, Xu P, Cheng M (2017) Co-occurrence and interactions of pollutants, and their impacts on soil remediation – a review. Crit Rev Environ Sci Technol 47:1528–1553. https://doi.org/10.1080/10643389.2017.1386951

    Article  Google Scholar 

  55. Alkorta I, Epelde L, Garbisu C (2017) Environmental parameters altered by climate change affect the activity of soil microorganisms involved in bioremediation. FEMS Microbiol Lett 364:1–9. https://doi.org/10.1093/femsle/fnx200

    Article  Google Scholar 

  56. Leys NM, Bastiaens L, Verstraete W et al (2005) Influence of the carbon/nitrogen/phosphorus ratio on polycyclic aromatic hydrocarbon degradation by Mycobacterium and Sphingomonas in soil. Appl Microbiol Biotechnol 66:726–736. https://doi.org/10.1007/s00253-004-1766-4

    Article  Google Scholar 

  57. Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.01369

  58. Coulon F, Brassington KJ, Bazin R, Linnet PE, Thomas KA, Mitchell TR, Lethbridge G, Smith JWN, Pollard JT (2012) Effect of fertilizer formulation and bioaugmentation on biodegradation and leaching of crude oils and refined products in soils. Environ Technol 33(16):1879–1893. https://doi.org/10.1080/09593330.2011.650221

    Article  Google Scholar 

  59. Thompson P, Van Der Gast CJ, Ciric L, Singer AC (2005) Bioaugmentation for bioremediation: the challenge of strain selection. Environ Microbiol 7:909–915

    Google Scholar 

  60. Laothamteep N, Naloka K, Pinyakong O (2022) Bioaugmentation with zeolite-immobilized bacterial consortium OPK results in a bacterial community shift and enhances the bioremediation of crude oil-polluted marine sandy soil microcosms. Environ Pollut 292:118309. https://doi.org/10.1016/j.envpol.2021.118309

    Article  Google Scholar 

  61. Zhai Q, Chen X, Zhang M, Zhang C, Zhang Z, Pan H, Zhang H, Sun F (2023) Immobilisation of Klebsiella jilinsis strain 2N3 by corn straw biochar enhanced the degradation of nicosulfuron and restores the soil microbiome function and composition. Appl Soil Ecol 189:104917. https://doi.org/10.1016/j.apsoil.2023.104917

    Article  Google Scholar 

  62. Uhlik O, Leewis M-C, Strejcek M, Musilova L, Mackova M, Leigh MB, Macek T (2013) Stable isotope probing in the metagenomics era: a bridge towards improved bioremediation. Biotechnol Adv 31(2):154–165., ISSN 0734-9750. https://doi.org/10.1016/j.biotechadv.2012.09.003

    Article  Google Scholar 

  63. Lerner H, Öztürk B, Dohrmann AB, Thomas J, Marchal K, De Mot R, Dehaen W, Tebbe CC, Springael D (2020) Culture-independent analysis of linuron-mineralizing microbiota and functions in on-farm biopurification systems via DNA-stable isotope probing: comparison with enrichment culture. Environ Sci Technol 54(15):9387–9397. https://doi.org/10.1021/acs.est.0c02124

    Article  Google Scholar 

  64. Liu S, Moon CD, Zheng N et al (2022) Opportunities and challenges of using metagenomic data to bring uncultured microbes into cultivation. Microbiome 10:76. https://doi.org/10.1186/s40168-022-01272-5

    Article  Google Scholar 

  65. Luo C, Zhao X, Zhang D, Dai Y, Li Q, Wang S, Lin H, Zhang G, Li J (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 EST Water 1:1390–1400. https://doi.org/10.1021/acsestwater.0c00257

    Article  Google Scholar 

  66. Vogel LE, Makowski D, Garnier P, Vieublé-Gonod L, Coquet Y, Raynaud X, Nunan N, Chenu C, Falconer R, Pot V (2015) Modeling the effect of soil meso- and macropores topology on the biodegradation of a soluble carbon substrate. Adv Water Resour 83:123–136. https://doi.org/10.1016/J.ADVWATRES.2015.05.020

    Article  Google Scholar 

  67. Baveye PC, Otten W, Kravchenko A, Balseiro-Romero M, Beckers É, Chalhoub M, Darnault C, Eickhorst T, Garnier P, Hapca S, Kiranyaz S, Monga O, Mueller CW, Nunan N, Pot V, Schlüter S, Schmidt H, Vogel H-J (2018) Emergent properties of microbial activity in heterogeneous soil microenvironments: different research approaches are slowly converging, yet major challenges remain. Front Microbiol 9:1929. https://doi.org/10.3389/fmicb.2018.01929

    Article  Google Scholar 

  68. Hölscher T, Kovács ÁT (2017) Sliding on the surface: bacterial spreading without an active motor. Environ Microbiol 19:2537–2545. https://doi.org/10.1111/1462-2920.13741

    Article  Google Scholar 

  69. Tchoufag J, Ghosh P, Pogue CB, Nan B, Mandadapu KK (2019) Mechanisms for bacterial gliding motility on soft substrates. Proc Natl Acad Sci 116:25087–25096. https://doi.org/10.1073/pnas.1914678116

    Article  Google Scholar 

  70. Krell T, Lacal J, Reyes-Darias JA, Jimenez-Sanchez C, Sungthong R, Ortega-Calvo JJ (2013) Bioavailability of pollutants and chemotaxis. Curr Opin Biotechnol 24:451–456. https://doi.org/10.1016/j.copbio.2012.08.011

    Article  Google Scholar 

  71. Ren X, Zeng G, Tang L, Wang J, Wan J, Liu Y, Yu J, Yi H, Ye S, Deng R (2018) Sorption, transport and biodegradation – an insight into bioavailability of persistent organic pollutants in soil. Sci Total Environ 610–611:1154–1163. https://doi.org/10.1016/j.scitotenv.2017.08.089

    Article  Google Scholar 

  72. Ford RM, Harvey RW (2007) Role of chemotaxis in the transport of bacteria through saturated porous media. Adv Water Resour 30:1608–1617. https://doi.org/10.1016/j.advwatres.2006.05.019

    Article  Google Scholar 

  73. Jiménez-Sánchez C, Wick LY, Ortega-Calvo JJ (2012) Chemical effectors cause different motile behavior and deposition of bacteria in porous media. Environ Sci Technol 46:6790–6797. https://doi.org/10.1021/es300642n

    Article  Google Scholar 

  74. Castilla-Alcantara J-C, Posada-Baquero R, Ortega-Calvo J-J (2023) Taxis-mediated bacterial transport and its implication for the cometabolism of pyrene in a model aquifer. Water Res 248:120850. https://doi.org/10.1016/j.watres.2023.120850

    Article  Google Scholar 

  75. Jimenez-Sanchez C, Wick LY, Ortega-Calvo JJ (2018) Impact of chemoeffectors on bacterial motility, transport, and contaminant degradation in sand-filled percolation columns. Environ Sci Technol 52:10673–10679. https://doi.org/10.1021/acs.est.8b02370

    Article  Google Scholar 

  76. Rolando L, Vila J, Posada-Baquero R, Castilla-Alcantara JC, Barra-Caracciolo A, Ortega-Calvo JJ (2020) Impact of bacterial motility on biosorption and cometabolism of pyrene in a porous medium. Sci Total Environ 717:137210

    Google Scholar 

  77. Hagai E, Dvora R, Havkin-Blank T, Zelinger E, Porat Z, Schulz S, Helman Y (2014) Surface-motility induction, attraction and hitchhiking between bacterial species promote dispersal on solid surfaces. ISME J 8:1147–1151. https://doi.org/10.1038/ismej.2013.218

    Article  Google Scholar 

  78. Muok AR, Briegel A (2021) Intermicrobial hitchhiking: how nonmotile microbes leverage communal motility. Trends Microbiol 29:542–550. https://doi.org/10.1016/j.tim.2020.10.005

    Article  Google Scholar 

  79. Balseiro-Romero M, Prieto-Fernández Á, Shor LM, Ghoshal S, Baveye PC, Ortega-Calvo JJ (2022) Chemotactic bacteria facilitate the dispersion of nonmotile bacteria through micrometer-sized pores in engineered porous media. Environ Sci Technol 56:13975–13984. https://doi.org/10.1021/acs.est.2c03149

    Article  Google Scholar 

  80. Fester T, Giebler J, Wick LY, Schlosser D, Kästner M (2014) Plant–microbe interactions as drivers of ecosystem functions relevant for the biodegradation of organic contaminants. Curr Opin Biotechnol 27:168–175. https://doi.org/10.1016/J.COPBIO.2014.01.017

    Article  Google Scholar 

  81. Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9(3):177–192

    Google Scholar 

  82. Kohlmeier S, Smits THM, Ford RM, Keel C, Harms H, Wick LY (2005) Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci Technol 39:4640–4646. https://doi.org/10.1021/es047979z

    Article  Google Scholar 

  83. Banitz T, Wick LY, Fetzer I, Frank K, Harms H, Johst K (2011) Dispersal networks for enhancing bacterial degradation in heterogeneous environments. Environ Pollut 159:2781–2788. https://doi.org/10.1016/J.ENVPOL.2011.05.008

    Article  Google Scholar 

  84. Furuno S, Foss S, Wild E, Jones KC, Semple KT, Harms H, Wick LY (2012) Mycelia promote active transport and spatial dispersion of polycyclic aromatic hydrocarbons. Environ Sci Technol 46:5463–5470. https://doi.org/10.1021/es300810b

    Article  Google Scholar 

  85. Schamfuß S, Neu TR, van der Meer JR, Tecon R, Harms H, Wick LY (2013) Impact of Mycelia on the accessibility of fluorene to PAH-degrading bacteria. Environ Sci Technol 47:6908–6915. https://doi.org/10.1021/es304378d

    Article  Google Scholar 

  86. Sungthong R, Tauler M, Grifoll M, Ortega-Calvo JJ (2017) Mycelium-enhanced bacterial degradation of organic pollutants under bioavailability restrictions. Environ Sci Technol 51:11935–11942. https://doi.org/10.1021/acs.est.7b03183

    Article  Google Scholar 

  87. Khan N, Muge E, Mulaa FJ, Wamalwa B, von Bergen M, Jehmlich N, Wick LY (2023) Mycelial nutrient transfer promotes bacterial co-metabolic organochlorine pesticide degradation in nutrient-deprived environments. ISME J 17:570–578

    Google Scholar 

  88. Bezza FA, Nkhalambayausi Chirwa EM (2016) Biosurfactant-enhanced bioremediation of aged polycyclic aromatic hydrocarbons (PAHs) in creosote contaminated soil. Chemosphere 144:635–644. https://doi.org/10.1016/j.chemosphere.2015.08.027

    Article  Google Scholar 

  89. Lamichhane S, Bal Krishna KC, Sarukkalige R (2017) Surfactant-enhanced remediation of polycyclic aromatic hydrocarbons: a review. J Environ Manage 199:46–61. https://doi.org/10.1016/j.jenvman.2017.05.037

    Article  Google Scholar 

  90. Pacwa-Płociniczak M, Płaza G, Piotrowska-Seget Z, Cameotra SS (2011) Environmental applications of biosurfactants: recent advances. Int J Mol Sci 12:633–654. https://doi.org/10.3390/ijms12010633

    Article  Google Scholar 

  91. Zhang Y, Wang F, Zhu X, Zeng J, Zhao Q, Jiang X (2015) Extracellular polymeric substances govern the development of biofilm and mass transfer of polycyclic aromatic hydrocarbons for improved biodegradation. Bioresour Technol 193:274–280. https://doi.org/10.1016/J.BIORTECH.2015.06.110

    Article  Google Scholar 

  92. Ortega-Calvo JJ, Tejeda-Agredano MC, Jimenez-Sanchez C, Congiu E, Sungthong R, Niqui-Arroyo JL, Cantos M (2013) Is it possible to increase bioavailability but not environmental risk of PAHs in bioremediation? J Hazard Mater 261:733–745. https://doi.org/10.1016/j.jhazmat.2013.03.042

    Article  Google Scholar 

  93. Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234. https://doi.org/10.1016/J.SOILBIO.2012.11.009

    Article  Google Scholar 

  94. Van Hamme JD (2004) Singh A, Ward OP (eds) Bioavailability and biodegradation of organic pollutants – a microbial perspective BT – biodegradation and bioremediation. Springer, Berlin, pp 37–56. https://doi.org/10.1007/978-3-662-06066-7_3

    Chapter  Google Scholar 

  95. Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2011) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In: Shukla G, Varma A (eds) Soil enzymology. Springer, Berlin, pp 229–243. https://doi.org/10.1007/978-3-642-14225-3_12

    Chapter  Google Scholar 

  96. Xu Y, Zhou NY (2016) Microbial remediation of aromatics-contaminated soil. Front Environ Sci Eng 11:1–9. https://doi.org/10.1007/S11783-017-0894-X

    Article  Google Scholar 

  97. Tauler M, Vila J, Nieto JM, Grifoll M (2016) Key high molecular weight PAH-degrading bacteria in a soil consortium enriched using a sand-in-liquid microcosm system. Appl Microbiol Biotechnol 100(7):3321–3336. https://doi.org/10.1007/s00253-015-7195-8

    Article  Google Scholar 

  98. Vila J, Nieto JM, Mertens J, Springael D, Grifoll M (2010) Microbial community structure of a heavy fuel oil-degrading marine consortium: linking microbial dynamics with polycyclic aromatic hydrocarbon utilization. FEMS Microbiol Ecol 73:349–362. https://doi.org/10.1111/j.1574-6941.2010.00902.x

    Article  Google Scholar 

  99. Louca S, Polz MF, Mazel F et al (2018) Function and functional redundancy in microbial systems. Nat Ecol Evol 2:936–943. https://doi-org.sire.ub.edu/10.1038/s41559-018-0519-1

    Google Scholar 

  100. Guazzaroni ME, Herbst FA, Lores I et al (2013) Metaproteogenomic insights beyond bacterial response to naphthalene exposure and bio-stimulation. ISME J 7:122–136. https://doi.org/10.1038/ismej.2012.82

    Article  Google Scholar 

  101. Chibwe L, Geier MC, Nakamura J, Tanguay RL, Aitken MD, Simonich SLM (2015) Aerobic bioremediation of PAH contaminated soil results in increased genotoxicity and developmental toxicity. Environ Sci Technol 49:13889–13898. https://doi.org/10.1021/acs.est.5b00499

    Article  Google Scholar 

  102. Tian Z, Gold A, Nakamura J, Zhang Z, Vila J, Singleton DR, Collins LB, Aitken MD (2017) Nontarget analysis reveals a bacterial metabolite of pyrene implicated in the genotoxicity of contaminated soil after bioremediation. Environ Sci Technol 51:7091–7100. https://doi.org/10.1021/acs.est.7b01172

    Article  Google Scholar 

  103. Neuwoehner J, Schofer A, Erlenkaemper B, Steinbach K, Hund-Rinke K, Eisentraeger A (2009) Toxicological characterization of 2,4,6-trinitrotoluene, its transformation products, and two nitramine explosives. Environ Toxicol Chem 26:1090–1099. https://doi.org/10.1897/06-471R.1

    Article  Google Scholar 

  104. Du H, Wang M, Dai H, Hong W, Wang M, Wang J, Weng N, Nie Y, Xu A (2015) Endosulfan isomers and sulfate metabolite induced reproductive toxicity in Caenorhabditis elegans involves genotoxic response genes. Environ Sci Technol 49:2460–2468. https://doi.org/10.1021/es504837z

    Article  Google Scholar 

  105. Enhui Z, Na C, MengYun L, Jia L, Dan L, Yongsheng Y, Ying Z, DeFu H (2014) Isomers and their metabolites of endosulfan induced cytotoxicity and oxidative damage in SH-SY5Y cells. Environ Toxicol 31:496–504. https://doi.org/10.1002/tox.22066

    Article  Google Scholar 

  106. Giacomazzi S, Cochet N (2004) Environmental impact of diuron transformation: a review. Chemosphere 56:1021–1032. https://doi.org/10.1016/j.chemosphere.2004.04.061

    Article  Google Scholar 

  107. Zengler K, Zaramela LS (2018) The social network of microorganisms – how auxotrophies shape complex communities. Nat Rev Microbiol 16:383–390. https://doi.org/10.1038/s41579-018-0004-5

    Article  Google Scholar 

  108. Lu X, Heal KR, Ingalls AE et al (2020) Metagenomic and chemical characterization of soil cobalamin production. ISME J 14:53–66. https://doi.org/10.1038/s41396-019-0502-0

    Article  Google Scholar 

  109. Perruchon C, Vasileiadis S, Papadopoulou ES, Karpouzas DG (2020) Genome-based metabolic reconstruction unravels the key role of B12 in methionine auxotrophy of an ortho-phenylphenol-degrading Sphingomonas haloaromaticamans. Front Microbiol 10:3009. https://doi.org/10.3389/FMICB.2019.03009

    Article  Google Scholar 

  110. Jiménez-Volkerink SN, Jordán M, Smidt H, Minguillón C, Vila J, Grifoll M (2024) Metagenomic insights into the microbial cooperative networks of a benz(a)anthracene-7,12-dione degrading community from a creosote-contaminated soil. Sci Total Environ 907:167832. https://doi.org/10.1016/j.scitotenv.2023.167832

  111. Álvarez A, Rodríguez-Garrido B, Cerdeira-Pérez A, Tomé-Pérez A, Kidd P, Prieto-Fernandez A (2022) Enhanced biodegradation of hexachlorocyclohexane (HCH) isomers by Sphingobium sp. strain D4 in the presence of root exudates or in co-culture with HCH-mobilizing strains. J Hazard Mater 433:128764. https://doi.org/10.1016/j.jhazmat.2022.128764

    Article  Google Scholar 

  112. Simon A, Bindschedler S, Job D, Wick LY, Filippidou S, Kooli WM, Verrecchia EP, Junier P (2015) Exploiting the fungal highway: development of a novel tool for the in situ isolation of bacteria migrating along fungal mycelium. FEMS Microbiol Ecol 91:fiv116. https://doi.org/10.1093/femsec/fiv116

    Article  Google Scholar 

  113. Warmink JA, Nazir R, Corten B, van Elsas JD (2011) Hitchhikers on the fungal highway: the helper effect for bacterial migration via fungal hyphae. Soil Biol Biochem 43:760–765. https://doi.org/10.1016/j.soilbio.2010.12.009

    Article  Google Scholar 

  114. Magan N, Gouma S, Fragoeiro S, Shuaib ME, Bastos AC (2022) Bacterial and fungal bioremediation strategies. Microbial Biodegradation Bioremed:193–212. https://doi.org/10.1016/B978-0-323-85455-9.00028-X

  115. Liu B, Liu J, Ju M, Li X, Wang P (2017) Bacteria-white-rot fungi joint remediation of petroleum-contaminated soil based on sustained-release of laccase. RSC Adv. https://doi.org/10.1039/c7ra06962f

  116. Jiang J, Liu H, Li Q, Gao N, Yao Y, Xu H (2015) Combined remediation of Cd–phenanthrene co-contaminated soil by Pleurotus cornucopiae and Bacillus thuringiensis FQ1 and the antioxidant responses in Pleurotus cornucopiae. Ecotoxicol Environ Saf 120:386–393. https://doi.org/10.1016/J.ECOENV.2015.06.028

    Article  Google Scholar 

  117. Takors R (2012) Scale-up of microbial processes: Impacts, tools and open questions. J Biotechnol 160(1–2):3–9. https://doi.org/10.1016/j.jbiotec.2011.12.010

    Article  Google Scholar 

  118. Gupta PK, Mustapha HI, Singh B, Sharma YC (2022) Bioremediation of petroleum contaminated soil-water resources using neat biodiesel: a review. Sustain Energy Technol Assess 53:102703. https://doi.org/10.1016/j.seta.2022.102703

    Article  Google Scholar 

  119. Schoebitz M, López MD, Roldán A (2013) Bioencapsulation of microbial inoculants for better soil-plant fertilization. A review. Agron Sustain Dev 33:751–765. https://doi.org/10.1007/S13593-013-0142-0/FIGURES/7

    Article  Google Scholar 

  120. Deng F, Dou R, Sun J, Li J, Dang Z (2021) Phenanthrene degradation in soil using biochar hybrid modified bio-microcapsules: determining the mechanism of action via comparative metagenomic analysis. Sci Total Environ 775:145798

    Google Scholar 

  121. Chen W, Zhang H, Zhang M, Shen X, Zhang X, Wu F, Hu J, Wang B, Wang X (2021) Removal of PAHs at high concentrations in a soil washing solution containing TX-100 via simultaneous sorption and biodegradation processes by immobilized degrading bacteria in PVA-SA hydrogel beads. J Hazard Mater 410:124533

    Google Scholar 

  122. Dou R, Sun J, Lu J, Deng F, Yang C, Lu G, Dang Z (2021) Bacterial communities and functional genes stimulated during phenanthrene degradation in soil by bio-microcapsules. Ecotoxicol Environ Saf 212:111970

    Google Scholar 

  123. Ren W, Liu H, Mao T, Teng Y, Zhao R, Luo Y (2022) Enhanced remediation of PAHs-contaminated site soil by bioaugmentation with graphene oxide immobilized bacterial pellets. J Hazard Mater 433:128793

    Google Scholar 

  124. Innemanová P, Filipová A, Michalíková K, Wimmerová L, Cajthaml T (2018) Bioaugmentation of PAH-contaminated soils: a novel procedure for introduction of bacterial degraders into contaminated soil. Ecol Eng 118:93–96. https://doi.org/10.1016/J.ECOLENG.2018.04.014

    Article  Google Scholar 

  125. Wang Z, Xu Y, Zhao J, Li F, Gao D, Xing B (2011) Remediation of petroleum contaminated soils through composting and rhizosphere degradation. J Hazard Mater 190:677–685. https://doi.org/10.1016/j.jhazmat.2011.03.103

    Article  Google Scholar 

  126. Jha P, Panwar J, Jha PN (2015) Secondary plant metabolites and root exudates: guiding tools for polychlorinated biphenyl biodegradation. Int J Environ Sci Technol 12:789–802. https://doi.org/10.1007/S13762-014-0515-1/TABLES/2

    Article  Google Scholar 

  127. Wojtera-Kwiczor J, Żukowska W, Graj W, Małecka A, Piechalak A, Ciszewska L, Chrzanowski Ł, Lisiecki P, Komorowicz I, Barałkiewicz D, Voss I, Scheibe R, Tomaszewska B (2014) Rhizoremediation of diesel-contaminated soil with two rapeseed varieties and petroleum degraders reveals different responses of the plant defense mechanisms. Int J Phytoremediation 16:770–789. https://doi.org/10.1080/15226514.2013.856848

    Article  Google Scholar 

  128. Álvarez A, Yañez ML, Benimeli CS, Amoroso MJ (2012) Maize plants (Zea mays) root exudates enhance lindane removal by native Streptomyces strains. Int Biodeter Biodegr 66:14–18. https://doi.org/10.1016/j.ibiod.2011.10.001

    Article  Google Scholar 

  129. Balseiro-Romero M, Kidd PS, Monterroso C (2014) Influence of plant root exudates on the mobility of fuel volatile compounds in contaminated soils. Int J Phytoremediation 16:824–839. https://doi.org/10.1080/15226514.2013.856851

    Article  Google Scholar 

  130. Gao Y, Hu X, Zhou Z, Zhang W, Wang Y, Sun B (2017) Phytoavailability and mechanism of bound PAH residues in filed contaminated soils. Environ Pollut 222:465–476. https://doi.org/10.1016/j.envpol.2016.11.076

    Article  Google Scholar 

  131. Martin BC, George SJ, Price CA, Ryan MH, Tibbett M (2014) The role of root exuded low molecular weight organic anions in facilitating petroleum hydrocarbon degradation: current knowledge and future directions. Sci Total Environ 472:642–653. https://doi.org/10.1016/j.scitotenv.2013.11.050

    Article  Google Scholar 

  132. Mitton FM, Gonzalez M, Peña A, Miglioranza KSB (2012) Effects of amendments on soil availability and phytoremediation potential of aged p,p′-DDT, p,p′-DDE and p,p′-DDD residues by willow plants (Salix sp.). J Hazard Mater 203–204:62–68. https://doi.org/10.1016/j.jhazmat.2011.11.080

    Article  Google Scholar 

  133. LeFevre GH, Hozalski RM, Novak PJ (2013) Root exudate enhanced contaminant desorption: an abiotic contribution to the rhizosphere effect. Environ Sci Technol 47:11545–11553. https://doi.org/10.1021/es402446v

    Article  Google Scholar 

  134. Fernández-López C, Posada-Baquero R, García JL, Castilla-Alcantara JC, Cantos M, Ortega-Calvo JJ (2021) Root-mediated bacterial accessibility and cometabolism of pyrene in soil. Sci Total Environ 760:143408

    Google Scholar 

  135. Castilla-Alcantara JC, Posada-Baquero R, Balseiro-Romero M, Fernández-López C, García JL, Fernandez-Vazquez A, Parsons JR, Cantos M, Ortega-Calvo JJ (2023) Risk reductions during pyrene biotransformation and mobilization in a model plant-bacteria-biochar system. Sci Total Environ 868:161600. https://doi.org/10.1016/j.scitotenv.2023.161600

    Article  Google Scholar 

  136. Castilla-Alcantara J-C, Akbari A, Ghoshal S, Ortega-Calvo J-J (2022) Role of tactic response on the mobilization of motile bacteria through micrometer-sized pores. Sci Total Environ 832:154938. https://doi.org/10.1016/j.scitotenv.2022.154938

    Article  Google Scholar 

  137. Ahmad M, Pataczek L, Hilger TH, Zahir ZA, Hussain A, Rasche F, Schafleitner R, Solberg S (2018) Perspectives of microbial inoculation for sustainable development and environmental management. Front Microbiol 9:2992. https://doi.org/10.3389/FMICB.2018.02992/BIBTEX

    Article  Google Scholar 

  138. Saeed Q, Xiukang W, Haider FU, Kučerik J, Zahid Mumtaz M, Holatko J, Naseem M, Kintl A, Ejaz M, Naveed M, Brtnicky M, Mustafa A (2021) Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: a comprehensive review of effects and mechanisms. Int J Mol Sci 22:10529. https://doi.org/10.3390/ijms221910529

    Article  Google Scholar 

  139. Xiang L, Harindintwali JD, Wang F, Redmile-Gordon M, Chang SX, Fu Y, He C, Muhoza B, Brahushi F, Bolan N, Jiang X, Ok YS, Rinklebe J, Schaeffer A, Zhu Y, Tiedje JM, Xing B (2022) Integrating biochar, bacteria, and plants for sustainable remediation of soils contaminated with organic pollutants. Environ Sci Technol 56(23):16546–16566. https://doi.org/10.1021/acs.est.2c02976

    Article  Google Scholar 

  140. Hussain F, Hussain I, Khan AHA, Muhammad YS, Iqbal M, Soja G, Reichenauer TG, Zeshan, Yousaf S (2018) Combined application of biochar, compost, and bacterial consortia with italian ryegrass enhanced phytoremediation of petroleum hydrocarbon contaminated soil. Environ Exp Bot 153:80. https://doi.org/10.1016/j.envexpbot.2018.05.012

    Article  Google Scholar 

  141. Sarma H, Sonowal S, Prasad MNV (2019) Plant-microbiome assisted and biochar-amended remediation of heavy metals and polyaromatic compounds – a microcosmic study. Ecotoxicol Environ Saf 176:288. https://doi.org/10.1016/j.ecoenv.2019.03.081

    Article  Google Scholar 

  142. Liu X, Xu X, Zhang H, Li C, Shao X, Ye Q, Li Z (2015) Bioavailability and release of nonextractable (bound) residues of chiral cycloxaprid using geophagous earthworm Metaphire guillelmi in rice paddy soil. Sci Total Environ 526:243–250. https://doi.org/10.1016/J.SCITOTENV.2015.03.105

    Article  Google Scholar 

  143. Zhao L, Zhu L, Zhao S, Ma X (2016) Sequestration and bioavailability of perfluoroalkyl acids (PFAAs) in soils: implications for their underestimated risk. Sci Total Environ 572:169–176. https://doi.org/10.1016/j.scitotenv.2016.07.196

    Article  Google Scholar 

  144. Dubrovskaya E, Pozdnyakova N, Golubev S, Muratova A, Grinev V, Bondarenkova A, Turkovskaya O (2017) Peroxidases from root exudates of Medicago sativa and Sorghum bicolor: catalytic properties and involvement in PAH degradation. Chemosphere 169:224–232. https://doi.org/10.1016/J.CHEMOSPHERE.2016.11.027

    Article  Google Scholar 

  145. Košnář Z, Částková T, Wiesnerová L, Praus L, Jablonský I, Koudela M, Tlustoš P (2019) Comparing the removal of polycyclic aromatic hydrocarbons in soil after different bioremediation approaches in relation to the extracellular enzyme activities. J Environ Sci 76:249–258. https://doi.org/10.1016/J.JES.2018.05.007

    Article  Google Scholar 

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Acknowledgements

We would like to thank the European Union’s Horizon 2020 research and innovation program (Marie Sklodowska-Curie grant agreement no. 895340, BIOTAC) and the Spanish Ministry of Science and Innovation (PID2019-109700RB-C21, PID 2019-109700RB-C22, PID2022-139732OB-C21 and PID2022-139732OB-C22) for supporting this work. JV is a Serra Húnter Professor (Generalitat de Catalunya). MG and JV are members of the Water Research Institute from the University of Barcelona (IdRA-UB), and the recognised research group on Sustainable Biotechnology and Bioremediation (2021-SGR00852, Generalitat de Catalunya).

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Balseiro-Romero, M., Wick, L.Y., Vila, J., Grifoll, M., Ortega-Calvo, J.J. (2024). Drivers for Efficient Bioaugmentation and Clean-Up of Contaminated Soil. In: The Handbook of Environmental Chemistry. Springer, Berlin, Heidelberg. https://doi.org/10.1007/698_2023_1064

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