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http://dx.doi.org/10.7857/JSGE.2020.25.1.025

Effect of Repetitive Redox Transitions to Soil Bacterial Community and its Potential Impact on the Cycles of Iron and Arsenic  

Park, Sujin (Department of Civil and Environmental Engineering, Seoul National University)
Kim, Sanghyun (Department of Civil and Environmental Engineering, Seoul National University)
Chung, Hyeonyong (Department of Civil and Environmental Engineering, Seoul National University)
Chang, Sun Woo (Korea Institute of Civil Engineering and Building Technology)
Moon, Heesun (Korea Institute of Geoscience and Mineral Resources)
Nam, Kyoungphile (Department of Civil and Environmental Engineering, Seoul National University)
Publication Information
Journal of Soil and Groundwater Environment / v.25, no.1, 2020 , pp. 25-36 More about this Journal
Abstract
In a redox transition zone, geochemical reactions are facilitated by active bacteria that mediate reactions involving electrons, and arsenic (As) and iron (Fe) cycles are the major electron transfer reactions occurring at such a site. In this study, the effect of repetitive redox changes on soil bacterial community in As-contaminated soil was investigated. The results revealed that bacterial community changed actively in response to redox changes, and bacterial diversity gradually decreased as the cycle repeated. Proportion of strict aerobes and anaerobes decreased, while microaerophilic species such as Azospirillum oryzae group became the predominant species, accounting for 72.7% of the total counts after four weeks of incubation. Bacterial species capable of reducing Fe or As (e.g., Clostridium, Desulfitobacterium) belonging to diverse phylogenetic groups were detected. Indices representing richness (i.e., Chao 1) and phylogenetic diversity decreased from 1,868 and 1,926 to 848 and 1,121, respectively. Principle component analysis suggests that repetitive redox fluctuation, rather than oxic or anoxic status itself, is an important factor in determining the change of soil bacterial community, which in turn affects the cycling of As and Fe in redox transition zones.
Keywords
Redox transition zone; Bacterial community; Phylogenetic diversity; As contaminated soil;
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1 Clague, J.C., Stenger, R., and Morgenstern, U., 2019, The influence of unsaturated zone drainage status on denitrification and the redox succession in shallow groundwater. Sci. Total Environ., 660, 1232-1244.   DOI
2 Couture, R.-M., Charlet, L., Markelova, E., Made, B.t., and Parsons, C.T., 2015, On-off mobilization of contaminants in soils during redox oscillations. Environ. Sci. Technol., 49(5), 3015-3023.   DOI
3 D'Hondt, S., Jorgensen, B.B., Miller, D.J., Batzke, A., Blake, R., Cragg, B.A., Cypionka, H., Dickens, G.R., Ferdelman, T., and Hinrichs, K.-U., 2004, Distributions of microbial activities in deep subseafloor sediments. Science, 306(5705), 2216-2221.   DOI
4 de Zamaroczy, M., Delorme, F., and Elmerich, C., 1989, Regulation of transcription and promoter mapping of the structural genes for nitrogenase (nifHDK) of Azospirillum brasilense Sp7. Mol. Gen. Genet., 220(1), 33-42.   DOI
5 DeAngelis, K.M., Silver, W.L., Thompson, A.W., and Firestone, M.K., 2010, Microbial communities acclimate to recurring changes in soil redox potential status. Environ. Microbiol., 12(12), 3137-3149.   DOI
6 Dobbin, P.S., Carter, J.P., Garcia-Salamanca San Juan, C., von Hobe, M., Powell, A.K., and Richardson, D.J., 1999, Dissimilatory Fe (III) reduction by Clostridium beijerinckii isolated from freshwater sediment using Fe (III) maltol enrichment. FEMS Microbiol. Lett., 176(1), 131-138.   DOI
7 Duan, Y., Schaefer, M.V., Wang, Y., Gan, Y., Yu, K., Deng, Y., and Fendorf, S., 2019, Experimental constraints on redox-induced arsenic release and retention from aquifer sediments in the central Yangtze River Basin. Sci. Total Environ., 649, 629-639.   DOI
8 Hong, H., Kim, S.-J., Min, U.-G., Lee, Y.-J., Kim, S.-G., Jung, M.-Y., Seo, Y.-S., and Rhee, S.-K., 2015, Geosporobacter ferrireducens sp. nov., an anaerobic iron-reducing bacterium isolated from an oil-contaminated site. Antonie Van Leeuwenhoek, 107(4), 971-977.   DOI
9 Falkowski, P.G., Fenchel, T., and Delong, E.F., 2008, The microbial engines that drive Earth's biogeochemical cycles. Science, 320(5879), 1034-1039.   DOI
10 Harvey, C.F., Swartz, C.H., Badruzzaman, A., Keon-Blute, N., Yu, W., Ali, M.A., Jay, J., Beckie, R., Niedan, V., and Brabander, D., 2002, Arsenic mobility and groundwater extraction in Bangladesh. Science, 298(5598), 1602-1606.   DOI
11 Islam, F.S., Gault, A.G., Boothman, C., Polya, D.A., Charnock, J.M., Chatterjee, D., and Lloyd, J.R., 2004, Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature, 430(6995), 68-71.   DOI
12 Jackson, C.R., Dugas, S.L., and Harrison, K.G., 2005, Enumeration and characterization of arsenate-resistant bacteria in arsenic free soils. Soil Biol. Biochem., 37(12), 2319-2322.   DOI
13 Loreau, M., 2001, Microbial diversity, producer-decomposer interactions and ecosystem processes: a theoretical model. Proc. R. Soc. London, Ser. B, 268(1464), 303-309.   DOI
14 Jiang, S., Lee, J.-H., Kim, D., Kanaly, R.A., Kim, M.-G., and Hur, H.-G., 2013, Differential arsenic mobilization from Asbearing ferrihydrite by iron-respiring Shewanella strains with different arsenic-reducing activities. Environ. Sci. Technol., 47(15), 8616-8623.   DOI
15 Jung, H.B., Zheng, Y., Rahman, M.W., Rahman, M.M., and Ahmed, K.M., 2015, Redox zonation and oscillation in the hyporheic zone of the Ganges-Brahmaputra-Meghna Delta: implications for the fate of groundwater arsenic during discharge. Appl. Geochem., 63, 647-660.   DOI
16 Lara, J., Gonzalez, L.E., Ferrero, M., Diaz, G.C., Pedros-Alio, C., and Demergasso, C., 2012, Enrichment of arsenic transforming and resistant heterotrophic bacteria from sediments of two salt lakes in Northern Chile. Extremophiles, 16(3), 523-538.   DOI
17 Lee, J.H., Fredrickson, J.K., Plymale, A.E., Dohnalkova, A.C., Resch, C.T., McKinley, J.P., and Shi, L., 2015, An autotrophic H 2-oxidizing, nitrate-respiring, T c (VII)-reducing A cidovorax sp. isolated from a subsurface oxic-anoxic transition zone. Environ. Microbiol. Rep., 7(3), 395-403.   DOI
18 Lin, Z., Wang, X., Wu, X., Liu, D., Yin, Y., Zhang, Y., Xiao, S., and Xing, B., 2018, Nitrate reduced arsenic redox transformation and transfer in flooded paddy soil-rice system. Environ. Pollut., 243, 1015-1025.   DOI
19 Lovley, D., 2006, Dissimilatory Fe (III)-and Mn (IV)-reducing prokaryotes. The Prokaryotes: Volume 2: Ecophysiology and Biochemistry, 635-658.
20 Mandal, B.K. and Suzuki, K.T., 2002, Arsenic round the world: a review. Talanta, 58(1), 201-235.   DOI
21 Oliveira, A., Pampulha, M., Neto, M., and Almeida, A., 2009, Enumeration and characterization of arsenic-tolerant diazotrophic bacteria in a long-term heavy-metal-contaminated soil. Water, Air, Soil Pollut., 200(1-4), 237-243.   DOI
22 Meng, X., Dupont, R.R., Sorensen, D.L., Jacobson, A.R., and McLean, J.E., 2017, Mineralogy and geochemistry affecting arsenic solubility in sediment profiles from the shallow basin-fill aquifer of Cache Valley Basin, Utah. Appl. Geochem., 77, 126-141.   DOI
23 Moller, L., Laas, P., Rogge, A., Goetz, F., Bahlo, R., Leipe, T., and Labrenz, M., 2019, Sulfurimonas subgroup GD17 cells accumulate polyphosphate under fluctuating redox conditions in the Baltic Sea: possible implications for their ecology. The ISME journal, 13(2), 482-493.   DOI
24 Muntau, M., Schulz, M., Jewell, K.S., Hermes, N., Hubner, U., Ternes, T., and Drewes, J.E., 2017, Evaluation of the short-term fate and transport of chemicals of emerging concern during soilaquifer treatment using select transformation products as intrinsic redox-sensitive tracers. Sci. Total Environ., 583, 10-18.   DOI
25 Newman, D.K. and Banfield, J.F., 2002, Geomicrobiology: how molecular-scale interactions underpin biogeochemical systems. Science, 296(5570), 1071-1077.   DOI
26 Noel, V., Boye, K., Kukkadapu, R.K., Li, Q., and Bargar, J.R., 2019, Uranium storage mechanisms in wet-dry redox cycled sediments. Water Res., 152, 251-263.   DOI
27 Oremland, R.S. and Stolz, J.F., 2005, Arsenic, microbes and contaminated aquifers. Trends Microbiol., 13(2), 45-49.   DOI
28 Mejia, J., Roden, E.E., and Ginder-Vogel, M., 2016, Influence of oxygen and nitrate on Fe (hydr) oxide mineral transformation and soil microbial communities during redox cycling. Environ. Sci. Technol., 50(7), 3580-3588.   DOI
29 Paul, S., Majumdar, S., and Giri, A.K., 2015, Genetic susceptibility to arsenic-induced skin lesions and health effects: a review. Gene. Environ., 37(1), 23.   DOI
30 Parsons, C.T., Couture, R.-M., Omoregie, E.O., Bardelli, F., Greneche, J.-M., Roman-Ross, G., and Charlet, L., 2013, The impact of oscillating redox conditions: arsenic immobilisation in contaminated calcareous floodplain soils. Environ. Pollut., 178, 254-263.   DOI
31 Ray, A.E., Connon, S.A., Neal, A.L., Fujita, Y., Cummings, D.E., Ingram, J.C., and Magnuson, T.S., 2018, Metal transformation by a novel pelosinus isolate from a subsurface environment. Front. Microbiol., 9.
32 Rodriguez-Mora, M.J., Scranton, M.I., Taylor, G.T., and Chistoserdov, A.Y., 2015, The dynamics of the bacterial diversity in the redox transition and anoxic zones of the Cariaco Basin assessed by parallel tag sequencing. FEMS Microbiol. Ecol., 91(9), fiv088.   DOI
33 Shade, A. and Handelsman, J., 2012, Beyond the Venn diagram: the hunt for a core microbiome. Environ. Microbiol., 14(1), 4-12.   DOI
34 Smedley, P.L. and Kinniburgh, D.G., 2002, A review of the source, behaviour and distribution of arsenic in natural waters. Appl. Geochem., 17(5), 517-568.   DOI
35 Stookey, L. L., 1970, Ferrozine---a new spectrophotometric reagent for iron. Anal. Chem., 42(7), 779-781.   DOI
36 Sultana, M., Vogler, S., Zargar, K., Schmidt, A.-C., Saltikov, C., Seifert, J., and Schlomann, M., 2012, New clusters of arsenite oxidase and unusual bacterial groups in enrichments from arsenic-contaminated soil. Arch. Microbiol., 194(7), 623-635.   DOI
37 Teh, Y.A., Silver, W.L., and Conrad, M.E., 2005, Oxygen effects on methane production and oxidation in humid tropical forest soils. Global Change Biol., 11(8), 1283-1297.   DOI
38 Wang, N., Xue, X.-M., Juhasz, A.L., Chang, Z.-Z., and Li, H.-B., 2017, Biochar increases arsenic release from an anaerobic paddy soil due to enhanced microbial reduction of iron and arsenic. Environ. Pollut., 220, 514-522.   DOI
39 Torsvik, V. and Ovreas, L., 2002, Microbial diversity and function in soil: from genes to ecosystems. Curr. Opin. Microbiol., 5(3), 240-245.   DOI
40 Waldrop, M.P. and Firestone, M.K., 2006, Seasonal dynamics of microbial community composition and function in oak canopy and open grassland soils. Microb. Ecol., 52(3), 470-479.   DOI
41 Wang, X.-J., Yang, J., Chen, X.-P., Sun, G.-X., and Zhu, Y.-G., 2009, Phylogenetic diversity of dissimilatory ferric iron reducers in paddy soil of Hunan, South China. J. Soils Sed., 9(6), 568-577.   DOI
42 Wang, Y., Liu, X.-h., Si, Y.-b., and Wang, R.-f., 2016, Release and transformation of arsenic from As-bearing iron minerals by Fe-reducing bacteria. Chem. Eng. J., 295, 29-38.   DOI
43 Wenzel, W.W., Kirchbaumer, N., Prohaska, T., Stingeder, G., Lombi, E., and Adriano, D.C., 2001, Arsenic fractionation in soils using an improved sequential extraction procedure. Anal. Chim. Acta, 436(2), 309-323.   DOI
44 Winkel, L., Berg, M., Amini, M., Hug, S.J., and Johnson, C.A., 2008, Predicting groundwater arsenic contamination in Southeast Asia from surface parameters. Nature Geoscience, 1(8), 536-542.   DOI
45 Benz, M., Schink, B., and Brune, A., 1998, Humic acid reduction by Propionibacterium freudenreichii and other fermenting bacteria. Appl. Environ. Microbiol., 64(11), 4507-4512.   DOI
46 Xie, Z., Wang, J., Wei, X., Li, F., Chen, M., Wang, J., and Gao, B., 2018, Interactions between arsenic adsorption/desorption and indigenous bacterial activity in shallow high arsenic aquifer sediments from the Jianghan Plain, Central China. Sci. Total Environ., 644, 382-388.   DOI
47 Yang, Y.-P., Zhang, H.-M., Yuan, H.-Y., Duan, G.-L., Jin, D.-C., Zhao, F.-J., and Zhu, Y.-G., 2018, Microbe mediated arsenic release from iron minerals and arsenic methylation in rhizosphere controls arsenic fate in soil-rice system after straw incorporation. Environ. Pollut., 236, 598-608.   DOI
48 Zhao, R., Hannisdal, B., Mogollon, J.M., and Jorgensen, S.L., 2019, Nitrifier abundance and diversity peak at deep redox transition zones. Scientific Reports, 9(1), 8633.   DOI
49 Ahmed, B., Cao, B., McLean, J.S., Ica, T., Dohnalkova, A., Istanbullu, O., Paksoy, A., Fredrickson J.K., and Beyenal, H., 2012, Fe (III) reduction and U (VI) immobilization by Paenibacillus sp. strain 300A, isolated from Hanford 300A subsurface sediments. Appl. Environ. Microbiol., 78(22), 8001-8009.   DOI
50 Bachate, S.P., Cavalca, L., and Andreoni, V., 2009, Arsenicresistant bacteria isolated from agricultural soils of Bangladesh and characterization of arsenate-reducing strains. J. Appl. Microbiol., 107(1), 145-156.   DOI
51 Bishop, M.E., Dong, H., Glasser, P., Briggs, B.R., Pentrak, M., Stucki, J.W., Boyanov, M.I., Kemner, K.M., and Kovarik, L., 2019, Reactivity of redox cycled Fe-bearing subsurface sediments towards hexavalent chromium reduction. Geochim. Cosmochim. Acta, 252, 88-106.   DOI
52 Boucher, D., Jardillier, L., and Debroas, D., 2006, Succession of bacterial community composition over two consecutive years in two aquatic systems: a natural lake and a lake-reservoir. FEMS Microbiol. Ecol., 55(1), 79-97.   DOI
53 Burnol, A., Garrido, F., Baranger, P., Joulian, C., Dictor, M.-C., Bodenan, F., Morin, G., and Charlet, L., 2007, Decoupling of arsenic and iron release from ferrihydrite suspension under reducing conditions: a biogeochemical model. Geochem. Trans., 8(1), 12.   DOI
54 Calatayud, M., Gimeno-Alcaniz, J.V., Velez, D., and Devesa, V., 2014, Trivalent arsenic species induce changes in expression and levels of proinflammatory cytokines in intestinal epithelial cells. Toxicol. Lett., 224(1), 40-46.   DOI