Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Inoculation Effect of Methanotrophs on Rhizoremediation Performance and Methane Emission in Diesel-Contaminated Soil

  • Ji Ho Lee (Department of Environmental Science and Engineering, Ewha Womans University) ;
  • Hyoju Yang (Department of Environmental Science and Engineering, Ewha Womans University) ;
  • Kyung-Suk Cho (Department of Environmental Science and Engineering, Ewha Womans University)
  • Received : 2023.01.03
  • Accepted : 2023.03.30
  • Published : 2023.07.28
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Abstract

During the rhizoremediation of diesel-contaminated soil, methane (CH4), a representative greenhouse gas, is emitted as a result of anaerobic metabolism of diesel. The application of methantrophs is one of solutions for the mitigation CH4 emissions during the rhizoremediation of diesel-contaminated soil. In this study, CH4-oxidizing rhizobacteria, Methylocystis sp. JHTF4 and Methyloversatilis sp. JHM8, were isolated from rhizosphere soils of tall fescue and maize, respectively. The maximum CH4 oxidation rates for the strains JHTF4 and JHM8 were 65.8 and 33.8 mmol·g-DCW-1·h-1, respectively. The isolates JHTF4 and JHM8 couldn't degrade diesel. The inoculation of the isolate JHTF4 or JHM8 significantly enhanced diesel removal during rhizoremediation of diesel-contaminated soil planted with maize for 63 days. Diesel removal in the tall fescue-planting soil was enhanced by inoculating the isolates until 50 days, while there was no significant difference in removal efficiency regardless of inoculation at day 63. In both the maize and tall fescue planting soils, the CH4 oxidation potentials of the inoculated soils were significantly higher than the potentials of the non-inoculated soils. In addition, the gene copy numbers of pmoA, responsible for CH4 oxidation, in the inoculated soils were significantly higher than those in the non-inoculated soils. The gene copy numbers ratio of pmoA to 16S rDNA (the ratio of methanotrophs to total bacteria) in soil increased during rhizoremediation. These results indicate that the inoculation of Methylocystis sp. JHTF4 and Methyloversatilis sp. JHM8, is a promising strategy to minimize CH4 emissions during the rhizoremediation of diesel-contaminated soil using maize or tall fescue.

Keywords

Acknowledgement

This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government through the Ministry of Science and ICT (MSIT) (NRF-2019R1A2C2006701 & NRF- 2022R1A2C2006615).

References

  1. Saravanan A, Jeevanantham S, Narayanan VA, Kumar PS, Yaashikaa PR, Muthu CM. 2020. Rhizoremediation - A promising tool for the removal of soil contaminants: a review. J. Environ. Chem. Eng. 8: 103543. 
  2. Syranidou E, Christofilopoulos S, Kalogerakis N. 2017. Juncus spp.-The helophyte for all (phyto)remediation purposes? N. Biotechnol. 38: 43-55.  https://doi.org/10.1016/j.nbt.2016.12.005
  3. Gainer A, Bresee K, Hogan N, Siciliano SD. 2019. Advancing soil ecological risk assessments for petroleum hydrocarbon contaminated soils in Canada: persistence, organic carbon normalization and relevance of species assemblages. Sci. Total Environ. 668: 400-410.  https://doi.org/10.1016/j.scitotenv.2019.02.459
  4. Park IS, Park JW. 2011. Determination of a risk management primer at petroleum-contaminated sites: developing new human health risk assessment strategy. J. Hazard. Mater. 185: 1374-1380.  https://doi.org/10.1016/j.jhazmat.2010.10.058
  5. Baoune H, Aparicio JD, Acuna A, El Hadj-khelil AO, Sanchez L, Polti MA, et al. 2019. Effectiveness of the Zea mays-Streptomyces association for the phytoremediation of petroleum hydrocarbons impacted soils. Ecotoxicol. Environ. Saf. 184: 109591. 
  6. Lee YY, Lee SY, Lee SD, Cho KS. 2022. Seasonal dynamics of bacterial community structure in diesel oil-contaminated soil cultivated with tall fescue (Festuca arundinacea). Int. J. Environ. Res. Public Health 19.8: 4629. 
  7. Seo Y, Cho KS. 2021. Effects of plant and soil amendment on remediation performance and methane mitigation in petroleum-contaminated soil. J. Microbiol. Biotechnol. 31: 104-114.  https://doi.org/10.4014/jmb.2006.06023
  8. Shahzad A, Siddiqui S, Bano A, Sattar S, Hashmi MZ, Qin M, et al. 2020. Hydrocarbon degradation in oily sludge by bacterial consortium assisted with alfalfa (Medicago sativa L.) and maize (Zea mays L.). Arab. J. Geosci. 13: 879. 
  9. Correa-Garcia S, Pande P, Seguin A, St-Arnaud M, Yergeau E. 2018. Rhizoremediation of petroleum hydrocarbons: a model system for plant microbiome manipulation. Microb. Biotechnol. 11: 819-832.  https://doi.org/10.1111/1751-7915.13303
  10. Jason-Ogugbue VT, Mmom PC, Etela I, Orluchukwu JA. 2021. Uptake and bioaccumulation of diverse hydrocarbon compounds by selected food plants artificially exposed to bioremediated crude oil-contaminated soils. Acta Fytotechn Zootechn 24: 185-201. 
  11. Yang J, Li G, Qian Y, Zhang F. 2018. Increased soil methane emissions and methanogenesis in oil contaminated areas. L. Degrad. Dev. 29: 563-571.  https://doi.org/10.1002/ldr.2886
  12. IPCC. 2014. Climate Change 2014: Synthesis Report. 
  13. Ming A, Rowell I, Lewin S, Rouse R, Aubry T, Boland E. 2021. Key messages from the IPCC AR6 climate science report. Cambridge Open Engage. doi:10.33774/coe-2021-fj53b. 
  14. Semple KT, Reid BJ, Fermor TR. 2001. Impact of composting strategies on the treatment of soils contaminated with organic pollutants. Environ. Pollut. 112: 269-283.  https://doi.org/10.1016/S0269-7491(00)00099-3
  15. Davamani V, Parameswari E, Arulmani S. 2020. Mitigation of methane gas emissions in flooded paddy soil through the utilization of methanotrophs. Sci. Total Environ. 726: 138570. 
  16. Lee YY, Jung H, Ryu HW, Oh KC, Jeon JM, Cho KS. 2018. Seasonal characteristics of odor and methane mitigation and the bacterial community dynamics in an on-site biocover at a sanitary landfill. Waste Manag. 71: 277-286.  https://doi.org/10.1016/j.wasman.2017.10.037
  17. Reis PCJ, Ruiz-Gonzalez C, Crevecoeur S, Soued C, Prairie YT. 2020. Rapid shifts in methanotrophic bacterial communities mitigate methane emissions from a tropical hydropower reservoir and its downstream river. Sci. Total Environ. 748: 141374. 
  18. Ruiz-Ruiz P, Gomez-Borraz TL, Revah S, Morales M. 2020. Methanotroph-microalgae co-culture for greenhouse gas mitigation: effect of initial biomass ratio and methane concentration. Chemosphere 259: 127418. 
  19. Yang H, Jung H, Oh K, Jeon JM, Cho KS. 2021. Characterization of the bacterial community associated with methane and odor in a pilot-scale landfill biocover under moderately thermophilic conditions. J. Microbiol. Biotechnol. 31: 803-814.  https://doi.org/10.4014/jmb.2103.03005
  20. Lee YY, Seo Y, Ha M, Lee J, Yang H, Cho KS. 2021. Evaluation of rhizoremediation and methane emission in diesel-contaminated soil cultivated with tall fescue (Festuca arundinacea). Environ. Res. 194: 110606. 
  21. Herlemann DP, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ, Andersson AF. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 5: 1571-1579.  https://doi.org/10.1038/ismej.2011.41
  22. Kim TG, Lee EH, Cho KS. 2011. Microbial community analysis of a methane-oxidizing biofilm using ribosomal tag pyrosequencing. J. Microbiol. Biotechnol. 22: 360-370.  https://doi.org/10.4014/jmb.1109.09052
  23. Lee EH, Yi TW, Moon KE, Park HJ, Ryu HW, Cho KS. 2011. Characterization of methane oxidation by a methanotroph isolated from a landfill cover soil, South Korea. J. Microbiol. Biotechnol. 21: 753-756.  https://doi.org/10.4014/jmb.1102.01055
  24. Jackel U, Schnell S, Conrad R. 2004. Microbial ethylene production and inhibition of methanotrophic activity in a deciduous forest soil. Soil Biol. Biochem. 36: 835-840.  https://doi.org/10.1016/j.soilbio.2004.01.013
  25. Lee S, Kim S, Kim YJ, Lee Y, Cho KS. 2021. Characterization of CH4-oxidizing and N2O-reducing bacterial consortia enriched from the rhizospheres of maize and tall fescue. Microbiol. Biotechnol. Lett. 49: 225-238.  https://doi.org/10.48022/mbl.2102.02007
  26. Kolb S, Knief C, Stubner S, Conrad R. 2003. Quantitative detection of methanotrophs in soil by Novel. Society 69: 2423-2429.  https://doi.org/10.1128/AEM.69.5.2423-2429.2003
  27. Hanson RS, Hanson TE. 1996. Methanotrophic bacteria. Microbiol. Rev. 60: 439-471.  https://doi.org/10.1128/mr.60.2.439-471.1996
  28. Abazari M, Owlia P, Zarrini G, Aghdasinia H. 2021. Methane removal of isolated Methylocystis strains in the culture medium designed by evaluating strain capacity under adverse donditions. Biol. J. Microorg. 10: 23-36. 
  29. Dunfield PF, Yimga MT, Dedysh SN, Berger U, Liesack W, Heyer J. 2002. Isolation of a Methylocystis strain containing a novel pmoA-like gene. FEMS Microbiol. Ecol. 41: 17-26.  https://doi.org/10.1111/j.1574-6941.2002.tb00962.x
  30. Jung GY, Rhee SK, Han YS, Kim SJ. 2020. Genomic and physiological properties of a facultative methane-oxidizing bacterial strain of Methylocystis sp. from a wetland. Microorganisms 8: 1-20.  https://doi.org/10.3390/microorganisms8111719
  31. Rumah BL, Stead CE, Claxton Stevens BH, Minton NP, Grosse-Honebrink A, Zhang Y. 2021. Isolation and characterisation of Methylocystis spp. for poly-3-hydroxybutyrate production using waste methane feedstocks. AMB Express 11.1: 1-13.  https://doi.org/10.1186/s13568-020-01157-6
  32. Pardi-Comensoli L, Tonolla M, Colpo A, Palczewska Z, Revikrishnan S, Heeb M, et al. 2022. Microbial depolymerization of epoxy resins: a novel approach to a complex challenge. Appl. Sci. 12.1: 466. 
  33. Shrestha R, Cernousek T, Stoulil J, Kovarova H, Sihelska K, Spanek R, et al. 2021. Anaerobic microbial corrosion of carbon steel under conditions relevant for deep geological repository of nuclear waste. Sci. Total. Environ. 800: 149539. 
  34. Ossai IC, Ahmed A, Hassan A, Hamid F. S. 2020. Remediation of soil and water contaminated with petroleum hydrocarbon: a review. Environ. Technol. Innov. 17: 100526. 
  35. Seo Y, Cho K. 2020. Rhizoremdiation of petroleum hydrocarbon-contaminated soils and greenhouse gas emission characteristics: a Review. Microbiol. Biotechnol. Lett. 48: 99-112.  https://doi.org/10.4014/mbl.1911.11014
  36. de la Fuente Canto C, Simonin M, King E, Moulin L, Bennett MJ, Castrillo G, et al. 2020. An extended root phenotype: the rhizosphere, its formation and impacts on plant fitness. Plant J. 103: 951-964.  https://doi.org/10.1111/tpj.14781
  37. Koo SY, Cho KS. 2006. Interaction between plants and rhizobacteria in phytoremediation of heavy metal-contaminated soil. Kor. J. Microbiol. Biotechnol. 34: 83-93. 
  38. Vergani L, Mapelli F, Suman J, Cajthaml T, Uhlik O, Borin S. 2019. Novel PCB-degrading Rhodococcus strains able to promote plant growth for assisted rhizoremediation of historically polluted soils. PLoS One 14: e0221253. 
  39. Iannucci A, Canfora L, Nigro F, De Vita P, Beleggia R. 2021. Relationships between root morphology, root exudate compounds and rhizosphere microbial community in durum wheat. Appl. Soil Ecol. 158: 103781. 
  40. Hong SH, Ryu HW, Kim J, Cho KS. 2011. Rhizoremediation of diesel-contaminated soil using the plant growth-promoting rhizobacterium Gordonia sp. S2RP-17. Biodegradation 22: 593-601.  https://doi.org/10.1007/s10532-010-9432-2
  41. Lee YY, Seo Y, Ha M, Lee J, Yang H, Cho KS. 2021. Dynamics of bacterial functional genes and community structures during rhizoremediation of diesel-contaminated compost-amended soil. J. Environ. Sci. Heal. - Part A Toxic/Hazardous Subst. Environ. Eng. 56: 1107-1120.  https://doi.org/10.1080/10934529.2021.1965817
  42. Nie Y, Chi CQ, Fang H, Liang JL, Lu SL, Lai GL, et al. 2014. Diverse alkane hydroxylase genes in microorganisms and environments. Sci. Rep. 4: 4968. 
  43. Gutierrez T, Aitken MD. 2014. Role of methylotrophs in the degradation of hydrocarbons during the deepwater horizon oil spill. ISME J. 8: 2543-2545.  https://doi.org/10.1038/ismej.2014.88
  44. Chen P, Liu H, Xing Z, Wang Y, Zhang X, Zhao T, et al. 2022. Cometabolic degradation mechanism and microbial network response of methanotrophic consortia to chlorinated hydrocarbon solvents. Ecotoxicol. Environ. Saf. 230: 113110. 
  45. Semrau JD. 2011. Bioremediation via methanotrophy: overview of recent findings and suggestions for future research. Front. Microbiol. 2: 209. 
  46. Serrano-Silva N, Sarria-Guzman Y, Dendooven L, Luna-Guido M. 2014. Methanogenesis and methanotrophy in soil: a review. Pedosphere 24: 291-307.  https://doi.org/10.1016/S1002-0160(14)60016-3
  47. Cui J, Zhao J, Wang Z, Cao W, Zhang S, Liu J, et al. 2020. Diversity of active root-associated methanotrophs of three emergent plants in a eutrophic wetland in northern China. AMB Express 10: 48. 
  48. Degelmann DM, Borken W, Drake HL, Kolb S. 2010. Different atmospheric methane-oxidizing communities in european beech and norway spruce soils. Appl. Environ. Microbiol. 76: 3228-3235.  https://doi.org/10.1128/AEM.02730-09
  49. Alam MS, Jia Z. 2012. Inhibition of methane oxidation by nitrogenous fertilizers in a paddy soil. Front. Microbiol. 3: 246.