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The Effect of Changes in Soil Microbial Communities on Geochemical Behavior of Arsenic

토양 미생물 군집의 변화가 비소의 지구화학적 거동에 미치는 영향

  • Eui-Jeong Hwang (Department of Energy and Resources Engineering, Chonnam National University) ;
  • Yejin Choi (Department of Energy and Resources Engineering, Chonnam National University) ;
  • Hyeop-Jo Han (Geo-Environment Research Center, Mineral Resources Division, Korea Institute of Geoscience and Mineral Resources) ;
  • Daeung Yoon (Department of Energy and Resources Engineering, Chonnam National University) ;
  • Jong-Un Lee (Department of Energy and Resources Engineering, Chonnam National University)
  • 황의정 (전남대학교 에너지자원공학과) ;
  • 최예진 (전남대학교 에너지자원공학과) ;
  • 한협조 (한국지질자원연구원 자원환경연구센터) ;
  • 윤대웅 (전남대학교 에너지자원공학과) ;
  • 이종운 (전남대학교 에너지자원공학과)
  • Received : 2024.05.04
  • Accepted : 2024.06.20
  • Published : 2024.06.28

Abstract

To investigate the effect of changes in microbial communities on arsenic release in soil, experiments were conducted on arsenic-contaminated soils (F1, G7, and G10). The experiments involved three groups of the experimental sets; ① BAC: sterilized soil + Bacillus fungorum, ② IND: indigenous bacteria, and ③ MIX: indigenous bacteria + B. fungorum, and incubated them for seven weeks using lactate as a carbon source under anaerobic conditions. The experimental results showed that higher concentrations of arsenic were released from the IND and MIX soils, where indigenous bacterial communities existed, compared to BAC. Significantly higher levels of arsenic were released from the G10 soil, which showed higher pH, compared to the F1 and G7 soils. In the G10 soil, unlike other soils, the proportion of As(III) among the released arsenic was also low. These results may be attributed to differences in microbial community composition that vary depending on the soil. By the seventh week, the diversity of microbial species in the IND and MIX soils had significantly decreased, with dominant orders such as Eubacteriales and Bacillales thriving. Bacteroidales in the seventh week of the MIX in the F1 soil, Rummeliibacillus in the seventh week of the IND and MIX of the G7 soil, and Enterobacterales in the IND and MIX of the G10 soil were dominant. At present, it is not known which mechanisms of microbial community changes affect the geochemical behavior of arsenic; however, these results indicate that microbiome in the soil may function as one of the factors regulating arsenic release.

토양 내 미생물 군집의 변화가 비소 용출에 미치는 영향을 파악하기 위해 비소 오염 토양(F1, G7, G10)을 대상으로 실험을 수행하였다. 실험은 혐기적 조건에서 비소 오염 토양을 ① BAC: 멸균토양 + Bacillus fungorum, ② IND: 토착균 토양, ③ MIX: 토착균 토양 + B. fungorum으로 나누어 혐기적 조건에서 유산염을 탄소원으로 하여 7주간 배양하였다. 실험 결과, 토착균 군집이 존재하는 IND와 MIX에서 BAC에 비하여 높은 함량의 비소가 용출되었으며, pH가 높은 G10 토양에서 F1과 G7 토양에 비해 비소 용출량이 월등히 높았다. G10 토양의 경우, 다른 토양과 달리 용출된 비소 중 As(III) 함량의 비율이 낮았다. 이러한 결과는 토양에 따라 상이하게 나타나는 미생물 군집의 차이에 기인할 수도 있다. IND와 MIX는 7주차에 이르러 미생물의 다양성이 크게 감소하였으며 실험 조건에 적응한 Eubacteriales 및 Bacillales 등의 우점목이 번성하였다. F1 토양의 7주차 MIX에서는 Bacteroidales, G7 토양의 7주차 IND와 MIX에서는 Rummelibaciilus가 번성하였다. G10 토양의 IND와 MIX에서는 Enterobacterales가 우점목 중 하나를 차지하였다. 현재로서는 미생물 군집의 변화가 비소의 지구화학적 거동에 어떠한 메커니즘으로 영향을 미치는지에 관한 정보가 부족하나, 이러한 결과는 토양 내 마이크로바이옴이 비소의 용출을 조절하는 요인 중 하나로 기능할 수 있음을 나타낸다.

Keywords

Acknowledgement

이 논문은 한국연구재단 지역대학우수과학자지원사업(과제번호 2020R1I1A307435913) 지원을 받아 수행하였습니다.

References

  1. Ahmann, D., Roberts, A.L., Krumholz, L.R., and Morel, F.M.M. (1994) Microbe grows by reducing arsenic. Nature, v.371, p.750. doi: 10.1038/371750a0
  2. Blum, J.S., Bindi, A.B., Buzelli, J., Stolz, J.F., and Oremland, R.S. (1998) Bacillus arsenicoselenatis, sp. nov.. and Bacillus selenitireducens sp. nov.: two haloalkaliphiles from Mono Lake, California that respire oxyanions of selenium and arsenic. Archives of Microbiology, v.171, p.19-30. doi: 10.1007/s002030050673
  3. Boyle, J. (2004) A comparison of two methods for estimating the organic matter content of sediments. Journal of Paleolimnology, v.31, p.125-127. doi: 10.1023/B:JOPL.0000013354.67645.df
  4. Busenberg, E. and Clemency, C.V. (1973) Determination of the cation exchange capacity of clays and soils using an ammonia electrode. Clays and Clay Minerals, v.21, p.213-217. doi: 10.1346/CCMN.1973.0210403
  5. Coates, J.D., Ellis, D., Gaw, C., and Lovely, D. (1999) Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. International Journal of Systematic and Evolutionary Microbiology, v.49(4), p. 1615-1622. doi:10.1099/00207713-49-4-1615
  6. Ghosh, S., Mohapatra, B., Satyanarayana, T., and Sar, P. (2020) Molecular and taxonomic characterization of arsenic (As) transforming Bacillus sp. strain IIIJ3-1 isolated from As-contaminated groundwater of Brahmaputra river basin, India. BMC Microbiology, v.20, 256. doi: 10.1186/s12866-020-01893-6
  7. Hernandez-Eugenio, G., Fardeau, M.L., Cayol, J.L., Patel, B.K., Thomas, P., Macarie, H., Garcia, J.L., and Ollivier, B. (2002) Clostridium thiosulfatireducens sp. nov., a proteolytic, thiosulfate-and sulfur-reducing bacterium isolated from an upflow anaerobic sludge blanket (UASB) reactor. International Journal of Systematic and Evolutionary Microbiology, v.52, p.1461-1468. doi:10.1099/ijs.0.01946-0
  8. Huber, R., Sacher, M., Vollmann, A., Huber, H., and Rose, D. (2000) Respiration of arsenate and selenate by hyperthermophilic Archaea. Systematic and Applied Microbiology, v.23, p.305-314. doi: 10.1016/S0723-2020(00)80058-2
  9. Jain, S., Saluja, B., Gupta, A., Marla, S.S., and Goel, R. (2011) Validation of arsenic resistance in Bacillus cereus strain AG27 by comparative protein modeling of arsC gene product. The Protein Journal, v.30, p.91-101. doi: 10.1007/s10930-011-9305-5
  10. Jang, H.-Y., Chon, H.-T. and Lee, J.-U. (2009) In-situ precipitation of arsenic and copper in soil by microbiological sulfate reduction. Economic and Environmental Geology, v.42, p.445-455.
  11. Jiao, S., Chen, W. and Wei, G. (2019) Resilience and assemblage of soil microbiome in response to chemical contamination combined with plant growth. Applied and Environmental Microbiology, v.85, e02523-18. doi: 10.1128/AEM.02523-18
  12. Kim, S.-H., Lee, J.-U., Ko, M.-S., Yun, Y.-H., Lee, J.-S. and Hong, S.-J. (2011) The effects of carbon sources supply to contaminated soil in the vicinity of Pungjeong mine on geomicrobiological behavior of heavy metals and arsenic. Journal of the Korean Society for Geosystem Engineering, v.48, p.584-597.
  13. Ko, M.S., Lee, J.-U., Park, H.S., Shin, J.S., Bang, K.M., Chon, H.T., Lee, J.S. and Kim, J.Y. (2009) Geomicrobiological behavior of heavy metals in paddy soil near abandoned Au-Ag mine supplied with carbon sources. Economic and Environmental Geology, v.42, p.413-426.
  14. Laverman, A.M., Blum, J.S., Schaefer, J.K., Philips, E.J.P., Lovley, D.R., and Oremland, R.S. (1995) Growth of strain SES-3 with arsenate and other diverse electron acceptors. Applied and Environmental Microbiology, v.61, p.3556-3561. doi: 10.1128/aem.61.10.3556-3561.1995
  15. Lee, J.-U. and Beveridge, T.J. (2001) Interaction between iron and Pseudomonas aeruginosa biofilms attached to Sepharose surfaces. Chemical Geology, 180, p.67-80. doi: 10.1016/S0009-2541(01)00306-0
  16. Lee, S.K., Chiang, M.S., Hseu, Z.Y., Kuo, C,H. and Liu, C.T. (2022) A photosynthetic bacterial inoculant exerts beneficial effects on the yield and quality of tomato and affects bacterial community structure in an organic field. Frontiers in Microbiology, v.13, p.1-17. doi: 10.3389/fmicb.2022.959080
  17. Lentini, C.J., Wankel, S.D., and Hansel, C.M. (2012) Enriched iron(III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Frontiers in Microbiology, December v.3, 404. doi: 10.3389/fmicb.2012.00404
  18. Liu, X., Wang, L., Han, M., Xue, Q.-H., Zhang, G.-S., Gao, J. and Sun, X. (2020) Bacillus fungorum sp. nov., a bacterium isolated from spent mushroom substrate. International Journal of Systematic and Evolutionary Microbiology, v.70, p.1457-1462. doi: 10.1099/ijsem.0.003673
  19. Lutz, S., Bodenhausen, N., Hess, J., Valzano-Held, A., Waelchli, J., Deslandes-Herold, G., Schlaeppi, K. and van der Heijden, M.G.A. (2023) Soil microbiome indicators can predict crop growth response to large-scale inoculation with arbuscular mycorrhizal fungi. Nature Microbiology, v.8, p.2277-2289. doi: 10.1038/s41564-023-01520-w
  20. Macaskie, L.E., Bonthrone, K.M., Yong, P., and Goddard, D.T. (2000) Enzymically mediated bioprecipitation of uranium by a Citrobacter sp.: a concerted role for exocellular lipopolysaccharide and associated phosphatase in biomineral formation. Microbiology, v.146(8), p.1855-1867. doi:10.1099/00221287-146-8-1855
  21. Macy, J.M., Nunan, K., Hagen, K.D., Dixon, D.R., Harbour, P.J., Cahill, M., and Sly, U. (1996) Chrysiogenes arsenatis gen. nov., sp. nov .. a new arsenic-respiring bacterium isolated from gold mine wastewater. International Journal of Systematic Bacteriology, v.46, p.1153-1157. doi: 10.1099/00207713-46-4-1153
  22. Maste, D.T., Huang, C.-H., Huang, Y.-M. and Yen, M.-Y. (2020) Nitrogen uptake and growth of white clover inoculated with indigenous and exotic Rhizobium strains. Journal of Plant Nutrition, v.43, p.2013-2027. doi: 10.1080/01904167.2020.1758134
  23. Mawarda, P.C., Le Roux, X., Van Elsas, J.D. and Salles, J.F. (2020) Deliberate introduction of invisible invaders: A critical appraisal of the impact of microbial inoculants on soil microbial communities. Soil Biology and Biochemistry, v.148, 107874. doi: 10.1016/j.soilbio.2020.107874
  24. Miyatake, M. and Hayashi, S. (2011) Characteristics of arsenic removal by Bacillus cereus strain W2. Resources Processing, v.58, p.101-107. doi: 10.4144/rpsj.58.101
  25. Moreina-Grez, B., Munoz-Rojas, M., Kariman, K., Storer, P., O'Donnell, A.G., Kumaresan, D. and Whiteley, A.S. (2019) Reconditioning degraded mine site soils with exogenous soil microbes: Plant fitness and soil microbiome outcomes. Frontiers in Microbiology, v.10, 1617. doi: 10.3389/fmicb.2019.01617
  26. Newman, D.K., Beveridge, T.J., and Morel, F. (1997) Precipitation of arsenic trisulfide by Desulfotomaculum auripigmentum. Applied and Environmental Microbiology, v.63(5), p.2022-2028. doi:10.1128/aem.63.5.2022-2028.1997
  27. Newman, D.K., Kennedy, E.K., Coates, J.D., Ahmann, D., Ellis, D.J., Lovely, D.R., and Morel, F.M.M. (1997) Dissimilatory arsenate and sulfate reduction in Desulfotomaculum auripigmentum sp. nov. Archives of Microbiology, v.168, p.380-388. doi:10.1007/s002030050512
  28. Osborne, T.H., McArthur, J.M., Sikdar, P.K., and Santini, J.M. (2015) Isolation of an arsenate-respiring bacterium from a redox front in an arsenic-polluted aquifer in West Bengal, Bengal Basin. Environmental Science and Technology, v.49(7), p.4193-4199. doi: 10.1021/es504707x
  29. Perdomo-Gonzalez, A., Perez-Reveron, R., Goberna, M., Leon-Barrios, M., Fernandez-Lopez, M., Villadas, P.J., ReyesBetancort, J.A. and Diaz-Pena, F.J. (2023) How harmful are exotic plantations for soils and its microbiome? A case study in an arid island. Science of the Total Environment, v.879, 163030. https://doi.org/10.1016/j.scitotenv.2023.163030
  30. Rizvi, A., Ahmed, B., Khan, M.S., Rajput, V.D., Umar, S., Minkina, T. and Lee, J. (2022) Maize associated bacterial microbiome linked mitigation of heavy metal stress: a multidimensional detoxification approach. Environmental and Experimental Botany, v.200, 104911. doi: 10.1016/j.envexpbot.2022.104911
  31. Smith, M.E., Facelli, J.M. and Cavagnaro, T.R. (2018) Interactions between soil properties, soil microbes and plants in remnant-grassland and old-field areas: a reciprocal transplant approach. Plant and Soil, v.433, p.127-145. doi: 10.1007/s11104-018-3823-2
  32. Song, D.S., Lee, J.-U., Ko, I.W. and Kim, K.W. (2007) Study on geochemical behavior of heavy metals by indigenous bacteria in contaminated soil and sediment. Economic and Environmental Geology, v,40, p.575-585.
  33. Tan, H.Y., Chen, S.-W., and Hu, S.-Y. (2019) Improvements in the growth performance, immunity, disease resistance, and gut microbiota by the probiotic Rummeliibacillus stabekisii in Nile tilapia (Oreochromis niloticus). Fish and Shellfish Immunology, v.92, p.265-275. doi:10.1016/j.fsi.2019.06.027
  34. Torsvik, V., Ovreas, L. and Thingstad, T. F. (2002) Prokaryotic diversity-magnitude, dynamics, and controlling factors. Science, v.296, p.1064-1066. doi: 10.1126/science.1071698
  35. Xue, X.-M., Xiong, C., Yoshinaga, M., Rosen, B., and Zhu, Y.-G. (2022) The enigma of environmental organoarsenicals: Insights and implications. Critical Reviews in Environmental Science and Technology, 52(21), p.3835-3862. doi:10.1080/10643389.2021.1947678