Redox-driven shifts in soil microbial community structure in the drawdown zone after construction of the Three Gorges Dam

Abstract

Soil redox is a critical environmental factor shaping the microbial community structure and ultimately alters the nutrient cycling. However, the response of soil microbial community structure to prolonged or repeated redox fluctuations is not yet clear. To study the dynamic effects of prolonged redox disturbances to the soil microbial community structure, soil samples experiencing 8, 5 and 0 alternating oxic-anoxic cycles within approximately 6 months each year were collected and the microbial community structure were evaluated using phospholipid fatty acid analysis (PLFA) profiles. Prolonged redox disturbances had significant effects on soil physiochemical properties and soil microbial community structure. The relative abundance of straight chain saturated PLFAs, cyclopropyl, and terminal- and mid-branched chain saturated PLFAs increased due to prolonged redox disturbances, but there was a consistent decrease in linear monounsaturated PLFAs and polyunsaturated PLFAs in the fluctuating zone. Prolonged redox disturbances had a negative impact on the total PLFA content (a proxy for biomass), which decreased in the order of 0 cycles>5 cycles>8 cycles. Both the fluctuating zone (8-cycle and 5-cycle plots) and the never flooded zone (0-cycle plots) were dominated by Gram-positive bacteria and a low content of fungi, actinomycetes and protozoa. The fungi and protozoa abundance decreased significantly with an increase in the occurrence of flooding-dry down events, suggesting that the prolonged redox disturbance leads to high stress on the fungi and protozoa populations. Moreover, total organic matter (TOC) and C:N ratio, environmental factors that can be influenced by recurring redox fluctuations, also influenced the microbial community structure.

Keywords

Water fluctuation zone / Redox disturbance / Microbial community structure / Phospholipid fatty acids (PLFA) / Three Gorges Reservoir

References

[1] Bååth, E., Anderson, T.H., 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biology & Biochemistry 35, 955–963

[2] Bai, Q., Gattinger, A., Zelles, L., 2000. Characterization of microbial consortia in paddy rice soil by phospholipid analysis. Microbial Ecology 39, 273–281

[3] Balasooriya, W.K., Huygens, D., Denef, K., Roobroeck, D., Verhoest, N.E.C., Boeckx, P., 2013. Temporal variation of rhizodeposit-C assimilating microbial communities in a natural wetland. Biology and Fertility of Soils 49, 333–341

[4] Bardgett, R.D., Jones, A.C., Jones, D.L., Kemmitt, S.J., Cook, R., Hobbs, P.J., 2001. Soil microbial community patterns related to the history and intensity of grazing in sub-montane ecosystems. Soil Biology & Biochemistry 33, 1653–1664

[5] Binnerup, S.J., Jensen, K., Revsbech, N.P., Jensen, M.H., Sørensen, J., 1992. Denitrification, dissimilatory reduction of nitrate to ammonium, and nitrification in a bioturbated estuarine sediment as measured with N and microsensor techniques. Applied and Environmental Microbiology 58, 303–313

[6] Bossio, D.A., Fleck, J.A., Scow, K.M., Fujii, R., 2006. Alteration of soil microbial communities and water quality in restored wetlands. Soil Biology & Biochemistry 38, 1223–1233

[7] Bossio, D.A., Scow, K.M., 1998. Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology 35, 265–278

[8] Bossio, D.A., Scow, K.M., Gunapala, N., Graham, K.J., 1998. Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microbial Ecology 36, 1–12

[9] Bremner, J., 1996. Nitrogen-total. Methods of soil analysis. Part 3, 1085–1121.

[10] Cao, Y., Fu, S., Zou, X., Cao, H., Shao, Y., Zhou, L., 2010. Soil microbial community composition under Eucalyptus plantations of different age in subtropical China. European Journal of Soil Biology 46, 128–135

[11] Chang, C., Xie, Z.Q., Xiong, G.M., 2011. The effects of three gorges reservoir water storage on the physical and chemical properties of soil. Ziran Ziyuan Xuebao 26, 1236–1244.

[12] Clegg, C.D., Lovell, R.D., Hobbs, P.J., 2003. The impact of grassland management regime on the community structure of selected bacterial groups in soils. FEMS Microbiology Ecology 43, 263–270

[13] Drenovsky, R.E., Vo, D., Graham, K.J., Scow, K.M., 2004. Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microbial Ecology 48, 424–430

[14] England, L.S., Lee, H., Trevors, J.T., 1993. Bacterial survival in soil: effect of clays and protozoa. Soil Biology & Biochemistry 25, 525–531

[15] Fernandes, M.F., Saxena, J., Dick, R.P., 2013. Comparison of whole-cell fatty acid (MIDI) or phospholipid fatty acid (PLFA) extractants as biomarkers to profile soil microbial communities. Microbial Ecology 66, 145–157

[16] Fenchel, T and Finlay, B.J, 1995. Ecology and Evolution in Anoxic Worlds. Oxford University Press, Oxford, UK.

[17] Imlay J A, 2002. How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Advances in Microbial Physiology 46(1):111–153.

[18] Fierer, N., Schimel, J.P., 2002. Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biology & Biochemistry 34, 777–787

[19] Findlay, R.H., Dobbs, F.C., 1993. Quantitative description of microbial communities using lipid analysis. Handbook of methods in aquatic microbial ecology 32, 271–284.

[20] Findlay, R.H., Trexler, M.B., Guckert, J., White, D.C., 1990. Laboratory study of disturbance in marine sediments: response of a microbial community. Marine Ecology Progress Series 62, 121–133

[21] Frindte, K., Allgaier, M., Grossart, H.P., Eckert, W., 2016. Redox stability regulates community structure of active microbes at the sediment-water interface. Environmental Microbiology Reports 8, 798–804

[22] Guckert, J.B., Antworth, C.P., Nichols, P.D., White, D.C., 1985. Phospholipid, ester linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiology Ecology 31, 147–158

[23] Guenet, B., Lenhart, K., Leloup, J., Giusti-Miller, S., Pouteau, V., Mora, P., Nunan, N., Abbadie, L., 2012. The impact of long-term CO2 enrichment and moisture levels on soil microbial community structure and enzyme activities. Geoderma 170, 331–336

[24] Haberer, C.M., Rolle, M., Cirpka, O.A., Grathwohl, P., 2012. Oxygen transfer in a fluctuating capillary fringe. Vadose Zone Journal 11, 811–822

[25] Heintze, S.G., 1934. The use of the glass electrode in soil reaction and oxidation-reduction potential measurements. Journal of Agricultural Science 24, 28–41

[26] Ibekwe, A.M., Kennedy, A.C., 1998. Phospholipid fatty acid profiles and carbon utilization patterns for analysis of microbial community structure under field and green house conditions. FEMS Microbiology Ecology 26, 151–163

[27] Langer, U., Rinklebe, J., 2009. Lipid biomarkers for assessment of microbial communities in floodplain soils of the Elbe River (Germany). Wetlands 29, 353–362

[28] Li, N., Yao, S.H., Qiao, Y.F., Zou, W.X., You, M.Y., Han, X.Z., Zhang, B., 2015. Separation of soil microbial community structure by aggregate size to a large extent under agricultural practices during early pedogenesis of a Mollisol. Applied Soil Ecology 88, 9–20

[29] Lüdemann, H., Arth, I., Liesack, W., 2000. Spatial changes in the bacterial community structure along a vertical oxygen gradient in flooded paddy soil cores. Applied and Environmental Microbiology 66, 754–762

[30] Mentzer, J.L., Goodman, R.M., Balser, T.C., 2006. Microbial response over time to hydrologic and fertilization treatments in a simulated wet prairie. Plant and Soil 284, 85–100

[31] Moche, M., Gutknecht, J., Schulz, E., Langer, U., Rinklebe, J., 2015. Monthly dynamics of microbial community structure and their controlling factors in three floodplain soils. Soil Biology & Biochemistry 90, 169–178

[32] Navarrete, A., Peacock, A., Macnaughton, S.J., Urmeneta, J., Mas-Castellà J., White, D.C., Guerrero, R., 2000. Physiological status and community composition of microbial mats of the Ebro Delta, Spain, by signature lipid biomarkers. Microbial Ecology 39, 92–99

[33] Nelson, D., Sommers, L., 1996. Total carbon, organic carbon and organic matter. In ‘Methods of soil analysis. Part 3. Chemical methods. Soil Science Society of America: Madison, WI, (Ed. D.L. Sparks) pp. 961–1010.

[34] Nikolausza, M., Székely, A., Rusznyák, A., , 2008. 2008, Diurnal redox fluctuation and microbial activity in the rhizosphere of wetland plants. European Journal of Soil Biology 44, 324–333

[35] Or, D., Smets, B.F., Wraith, J.M ., Dechesne, A., Friedman, S.P., 2007. Physical constraints affecting bacterial habitats and activity in unsaturated porous media – a review. Advances in Water Resources 30(6):1505–1527.

[36] Orwin, K.H., Wardle, D.A., Greenfield, L.G., 2006. Context-dependent changes in the resistance and resilience of soil microbes to an experimental disturbance for three primary plant chronosequences. Oikos 112(1):196–208.

[37] Pett-Ridge, J., Firestone, M.K., 2005. Redox fluctuation structures microbial communities in a wet tropical soil. Applied and Environmental Microbiology 71, 6998–7007

[38] Picek, T., Šimek, M., Šantrůčková H., 2000. Microbial responses to fluctuation of soil aeration status and redox conditions. Biology and Fertility of Soils 31, 315–322

[39] Rinklebe, J., Langer, U., 2006. Microbial diversity in three floodplain soils at the Elbe River (Germany). Soil Biology & Biochemistry, 38), 2144–2151.

[40] Satpathy, S.N., Rath, A.K., Ramakrishnan, B., Rao, V.R., Adhya, T.K., Sethunathan, N., 1997. Diurnal variation in methane efflux at different growth stages of tropical rice. Plant and Soil 195, 267–271

[41] Shamsi, I.H., 2012. Effects of irrigation patterns and nitrogen fertilization on rice yield and microbial community structure in paddy soil. Pedosphere 22, 661–672

[42] Shen, Z., Chen, L., Hong, Q., Qiu, J., Xie, H., Liu, R., 2013. Assessment of nitrogen and phosphorus loads and causal factors from different land use and soil types in the Three Gorges Reservoir Area. Science of the Total Environment 454-455, 383–392

[43] Silver, W.L., Lugo, A.E., Keller, M., 1999. Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44, 301–328

[44] Sinclair, J.L., Ghiorse, W.C., 1989. Distribution of aerobic bacteria, protozoa, algae, and fungi in deep subsurface sediments. Geomicrobiology Journal 7, 15–31

[45] Song, Y., Deng, S.P., Acosta-Martinez, V., Katsalirou, E., 2008. Characterization of redox-related soil microbial communities along a river floodplain continuum by fatty acid methyl ester (FAME) and 16S rRNA genes. Applied Soil Ecology 40, 499–509

[46] Sundh, I., Börjesson, G., Tunlid, A., 2000. Methane oxidation and phospholipid fatty acid composition in a podzolic soil profile. Soil Biology & Biochemistry 32, 1025–1028

[47] Teichert, A., Böttcher, J., Duijnisveld, W.H.M., 2000. Redox measurements as a qualitative indicator of spatial and temporal variability of redox state in a sandy forest soil. Redox. Springer Berlin Heidelberg, 95–110.

[48] van Aarle, I.M., Olsson, P.A., 2003. Fungal lipid accumulation and development of mycelial structures by two arbuscular mycorrhizal fungi. Applied and Environmental Microbiology 69, 6762–6767

[49] Vestal, J.R., White, D.C., 1989. Lipid analysis in microbial ecology: quantitative approaches to the study of microbial communities. Bioscience 39, 535–541

[50] Wilms, R., Sass, H., Köpke, B., Köster, J., Cypionka, H., Engelen, B., 2006. Specific bacterial, archaeal, and eukaryotic communities in tidal-flat sediments along a vertical profile of several meters. Applied and Environmental Microbiology 72, 2756–2764

[51] 吴 金水，何 电源. 土壤有机质及其周转动力学[J]. 中国南方土壤肥力与栽培植物施肥. 北京：科学出版社， 1994， 62：1994.28–62.

[52] Ye, C., Li, S., Zhang, Y., Zhang, Q., 2011. Assessing soil heavy metal pollution in the water-level-fluctuation zone of the Three Gorges Reservoir, China. Journal of Hazardous Materials 191, 366–372

[53] Zhou, Y.J., Qiu, J.X., Wang, J., 2010. Evaluation of ecological environmental vulnerability in the xiaolan area of the three gorges reservoir area. Journal of Ecology 30, 672–673.

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