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Redox potential and microbial functional gene diversity in wetland sediments under simulated warming conditions: implications for phosphorus mobilization

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Abstract

Microbial-driven biogeochemical cycles in wetlands impacted by global warming pose a potential downstream eutrophication risk. However, the consequences of ongoing warming on the functional and metabolic potential of sediment microbial communities are largely unknown. We incubated sediment samples under both ambient temperature conditions (control) and simulated warming conditions of 5°C above ambient temperature (warmed) using a novel field microcosm system. In warmed samples, we observed in situ a decreased thickness of the oxidized sediment layer and associated lower sediment redox potential. GeoChip 4.0, a comprehensive functional gene microarray, demonstrated that many functional genes that are involved in oxidation–reduction reactions and in phosphorus (P) degradation were preferentially enriched under warming conditions. The enriched genes included those genes encoding carbon monoxide dehydrogenase, acetyl-CoA carboxylase biotin carboxylase (ppc), and ribulose-1,5-bisphosphate carboxylase (Rubisco) for carbon fixation; nitrate reductases (narG) and nitrous oxide reductases (nosZ) for denitrification; cytochrome c for metal reduction; and exopolyphosphatase (ppx) for polyphosphate degradation. The redox potential was one of the most significant parameters linked to microbial functional gene structure. These results demonstrate that the enhanced hypoxia and anaerobic metabolic pathways accelerated sediment P mobilization in freshwater wetland subject to warming, raising the potential of water eutrophication.

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References

  • Achtnich, C., F. Bak & R. Conrad, 1995. Competition for electron-donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biology and Fertility of Soils 19(1): 65–72.

    Article  CAS  Google Scholar 

  • Allison, S. D. & K. K. Treseder, 2008. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biology 14(12): 2898–2909.

    Article  Google Scholar 

  • Angel, R., P. Claus & R. Conrad, 2012. Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME Journal 6(4): 847–862.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bond-Lamberty, B. & A. Thomson, 2010. Temperature-associated increases in the global soil respiration record. Nature 464(7288): U132–U579.

    Article  Google Scholar 

  • Borcard, D., P. Legendre & P. Drapeau, 1992. Partialling out the spatial component of ecological variation. Ecology 73(3): 1045–1055.

    Article  Google Scholar 

  • Bradford, M. A., C. A. Davies, S. D. Frey, T. R. Maddox, J. M. Melillo, J. E. Mohan, J. F. Reynolds, K. K. Treseder & M. D. Wallenstein, 2008. Thermal adaptation of soil microbial respiration to elevated temperature. Ecology Letters 11(12): 1316–1327.

    Article  PubMed  Google Scholar 

  • Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage & G. B. West, 2004. Toward a metabolic theory of ecology. Ecology 85(7): 1771–1789.

    Article  Google Scholar 

  • Brune, A., P. Frenzel & H. Cypionka, 2000. Life at the oxic-anoxic interface: microbial activities and adaptations. FEMS Microbiology Reviews 24(5): 691–710.

    CAS  PubMed  Google Scholar 

  • Cheng, W. G., H. Sakai, M. Matsushima, K. Yagi & T. Hasegawa, 2010. Response of the floating aquatic fern Azolla filiculoides to elevated CO2, temperature, and phosphorus levels. Hydrobiologia 656(1): 5–14.

    Article  CAS  Google Scholar 

  • Conley, D. J., S. Bjorck, E. Bonsdorff, J. Carstensen, G. Destouni, B. G. Gustafsson, S. Hietanen, M. Kortekaas, H. Kuosa, H. E. M. Meier, B. Muller-Karulis, K. Nordberg, A. Norkko, G. Nurnberg, H. Pitkanen, N. N. Rabalais, R. Rosenberg, O. P. Savchuk, C. P. Slomp, M. Voss, F. Wulff & L. Zillen, 2009. Hypoxia-related processes in the Baltic Sea. Environmental Science and Technology 43(10): 3412–3420.

    Article  CAS  PubMed  Google Scholar 

  • Cypionka, H., 1994. Novel metabolic capacities of sulfate-reducing bacteria, and their activities in microbial mats. In Stal, L. J. & P. Caumette (eds), Microbial Mats. Springer Verlag, Berlin: 367–376.

    Chapter  Google Scholar 

  • Diaz, R. J. & R. Rosenberg, 2008. Spreading dead zones and consequences for marine ecosystems. Science 321(5891): 926–929.

    Article  CAS  PubMed  Google Scholar 

  • Feuchtmayr, H., R. Moran, K. Hatton, L. Connor, T. Heyes, B. Moss, I. Harvey & D. Atkinson, 2009. Global warming and eutrophication: effects on water chemistry and autotrophic communities in experimental hypertrophic shallow lake mesocosms. Journal of Applied Ecology 46(3): 713–723.

    Article  Google Scholar 

  • Fierer, N., J. W. Leff, B. J. Adams, U. N. Nielsen, S. T. Bates, C. L. Lauber, S. Owens, J. A. Gilbert, D. H. Wall & J. G. Caporaso, 2012. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proceedings of the National Academy of Sciences of the United States of America 109(52): 21390–21395.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fierer, N., J. Ladau, J. C. Clemente, J. W. Leff, S. M. Owens, K. S. Pollard, R. Knight, J. A. Gilbert & R. L. McCulley, 2013. Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 342(6158): 621–624.

    Article  CAS  PubMed  Google Scholar 

  • Frostegard, A., A. Tunlid & E. Baath, 2011. Use and misuse of PLFA measurements in soils. Soil Biology and Biochemistry 43(8): 1621–1625.

    Article  CAS  Google Scholar 

  • Gilbert, J. A., D. Field, Y. Huang, R. Edwards, W. Z. Li, P. Gilna & I. Joint, 2008. Detection of large numbers of novel sequences in the metatranscriptomes of complex marine microbial communities. PLoS One 3(8). Doi:10.1371/Journal.Pone.0003042.

  • Goericke, R., 2002. Bacteriochlorophyll a in the ocean: is anoxygenic bacterial photosynthesis important? Limnology and Oceanography 47(1): 290–295.

    Article  CAS  Google Scholar 

  • Gudasz, C., D. Bastviken, K. Steger, K. Premke, S. Sobek & L. J. Tranvik, 2010. Temperature-controlled organic carbon mineralization in lake sediments. Nature 466(7305): U3–U478.

    Article  Google Scholar 

  • Hazen, T. C., E. A. Dubinsky, T. Z. DeSantis, G. L. Andersen, Y. M. Piceno, N. Singh, J. K. Jansson, A. Probst, S. E. Borglin, J. L. Fortney, W. T. Stringfellow, M. Bill, M. E. Conrad, L. M. Tom, K. L. Chavarria, T. R. Alusi, R. Lamendella, D. C. Joyner, C. Spier, J. Baelum, M. Auer, M. L. Zemla, R. Chakraborty, E. L. Sonnenthal, P. D’haeseleer, H. Y. N. Holman, S. Osman, Z. M. Lu, J. D. Van Nostrand, Y. Deng, J. Z. Zhou & O. U. Mason, 2010. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330(6001): 204–208.

    Article  CAS  PubMed  Google Scholar 

  • He, Z. L., Y. Deng, J. D. Van Nostrand, Q. C. Tu, M. Y. Xu, C. L. Hemme, X. Y. Li, L. Y. Wu, T. J. Gentry, Y. F. Yin, J. Liebich, T. C. Hazen & J. Z. Zhou, 2010. GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity. ISME Journal 4(9): 1167–1179.

    Article  CAS  PubMed  Google Scholar 

  • Henderson, R., N. Kabengi, N. Mantripragada, M. Cabrera, S. Hassan & A. Thompson, 2012. Anoxia-induced release of colloid- and nanoparticle-bound phosphorus in grassland soils. Environmental Science and Technology 46(21): 11727–11734.

    Article  CAS  PubMed  Google Scholar 

  • Himmelheber, D. W., S. H. Thomas, F. E. Loffler, M. Taillefert & J. B. Hughes, 2009. Microbial colonization of an in situ sediment cap and correlation to stratified redox zones. Environmental Science and Technology 43(1): 66–74.

    Article  CAS  PubMed  Google Scholar 

  • Hui, D. F., M. A. Mayes & G. S. Wang, 2013. Kinetic parameters of phosphatase: a quantitative synthesis. Soil Biology and Biochemistry 65: 105–113.

    Article  CAS  Google Scholar 

  • Hupfer, M. & J. Lewandowski, 2008. Oxygen controls the phosphorus release from lake sediments: a long-lasting paradigm in limnology. International Review of Hydrobiology 93(4–5): 415–432.

    Article  CAS  Google Scholar 

  • Hupfer, M., S. Gloess & H. P. Grossart, 2007. Polyphosphate-accumulating microorganisms in aquatic sediments. Aquatic Microbial Ecology 47(3): 299–311.

    Article  CAS  Google Scholar 

  • Jensen, H. S. & F. O. Andersen, 1992. Importance of temperature, nitrate, and pH for phosphate release from aerobic sediments of four shallow, eutrophic lakes. Limnology and Oceanography 37(3): 577–589.

    Article  Google Scholar 

  • Jerman, V., M. Metje, I. Mandic-Mulec & P. Frenzel, 2009. Wetland restoration and methanogenesis: the activity of microbial populations and competition for substrates at different temperatures. Biogeosciences 6(6): 1127–1138.

    Article  CAS  Google Scholar 

  • Kleeberg, A., C. Herzog & M. Hupfer, 2013. Redox sensitivity of iron in phosphorus binding does not impede lake restoration. Water Research 47(3): 1491–1502.

    Article  CAS  PubMed  Google Scholar 

  • Korosi, J. B., B. K. Ginn, B. F. Cumming & J. P. Smol, 2013. Establishing past environmental conditions and tracking long-term environmental change in the Canadian Maritime provinces using lake sediments. Environmental Reviews 21(1): 15–27.

    Article  Google Scholar 

  • Lepš, J. & P. Šmilauer, 2003. Multivariate Analysis of Ecological Data Using CANOCO. Cambridge University Press, Cambridge.

    Google Scholar 

  • Liang, Y. T., J. D. Van Nostrand, L. A. N’Guessan, A. D. Peacock, Y. Deng, P. E. Long, C. T. Resch, L. Y. Wu, Z. L. He, G. H. Li, T. C. Hazen, D. R. Lovley & J. Z. Zhou, 2012. Microbial functional gene diversity with a shift of subsurface redox conditions during in situ uranium reduction. Applied and Environmental Microbiology 78(8): 2966–2972.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu, M., Z. J. Zhang, Q. He, H. Wang, X. Li & J. Schoer, 2014. Exogenous phosphorus inputs alter complexity of soil-dissolved organic carbon in agricultural riparian wetlands. Chemosphere 95: 572–580.

    Article  CAS  PubMed  Google Scholar 

  • Lovley, D. R., S. J. Giovannoni, D. C. White, J. E. Champine, E. J. P. Phillips, Y. A. Gorby & S. Goodwin, 1993. Geobacter-metallireducens gen-nov sp-nov, a microorganism capable of coupling the complete oxidation of organic-compounds to the reduction of iron and other metals. Archives of Microbiology 159(4): 336–344.

    Article  CAS  PubMed  Google Scholar 

  • Lu, Z. M., Y. Deng, J. D. Van Nostrand, Z. L. He, J. Voordeckers, A. F. Zhou, Y. J. Lee, O. U. Mason, E. A. Dubinsky, K. L. Chavarria, L. M. Tom, J. L. Fortney, R. Lamendella, J. K. Jansson, P. D’haeseleer, T. C. Hazen & J. Z. Zhou, 2012. Microbial gene functions enriched in the deepwater horizon deep-sea oil plume. ISME Journal 6(2): 451–460.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martins, G., A. Terada, D. C. Ribeiro, A. M. Corral, A. G. Brito, B. F. Smets & R. Nogueira, 2011. Structure and activity of lacustrine sediment bacteria involved in nutrient and iron cycles. FEMS Microbiology Ecology 77(3): 666–679.

    Article  CAS  PubMed  Google Scholar 

  • Murphy, J. & J. P. Riley, 1962. A modified single solution method for determination of phosphate in natural waters. Analytica Chimica Acta 26(1): 31–36.

    Article  Google Scholar 

  • Nurnberg, G. K., L. A. Molot, E. O’Connor, H. Jarjanazi, J. Winter & J. Young, 2013. Evidence for internal phosphorus loading, hypoxia and effects on phytoplankton in partially polymictic Lake Simcoe, Ontario. Journal of Great Lakes Research 39(2): 259–270.

    Article  CAS  Google Scholar 

  • Penn, M. R., M. T. Auer, S. M. Doerr, C. T. Driscoll, C. M. Brooks & S. W. Effler, 2000. Seasonality in phosphorus release rates from the sediments of a hypereutrophic lake under a matrix of pH and redox conditions. Canadian Journal of Fisheries and Aquatic Sciences 57(5): 1033–1041.

    Article  CAS  Google Scholar 

  • Rabenhorst, M. C. & K. L. Castenson, 2005. Temperature effects on iron reduction in a hydric soil. Soil Science 170(9): 734–742.

    Article  CAS  Google Scholar 

  • Reddy, K. R., E. M. D’angelo & W. G. Harris, 1998. Biogeochemistry of wetlands. In Summer, M. E. (ed.), Handbook of Soil Science. CRC Press, Boca Raton: 89–119.

    Google Scholar 

  • Reeve, J. R., C. W. Schadt, L. Carpenter-Boggs, S. Kang, J. Z. Zhou & J. P. Reganold, 2010. Effects of soil type and farm management on soil ecological functional genes and microbial activities. ISME Journal 4(9): 1099–1107.

    Article  PubMed  Google Scholar 

  • Reitzel, K., J. Ahlgren, H. DeBrabandere, M. Waldeback, A. Gogoll, L. Tranvik & E. Rydin, 2007. Degradation rates of organic phosphorus in lake sediment. Biogeochemistry 82(1): 15–28.

    Article  CAS  Google Scholar 

  • Sanz-Lazaro, C., T. Valdemarsen, A. Marin & M. Holmer, 2011. Effect of temperature on biogeochemistry of marine organic-enriched systems: implications in a global warming scenario. Ecological Applications 21(7): 2664–2677.

    Article  PubMed  Google Scholar 

  • Smayda, T. J., 2005. Benthic phosphorus release from sediment to water. In Wassmann, P. & K. Olli (eds), Drainage Basin Nutrient Inputs and Eutrophication: An Integrated Approach. Univ Tromsoe, Norway, http://www.ut.ee/~olli/eutr/.

  • Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor, & H. L. Miller, 2007. Climate change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the IPCC. Cambridge University Press, Cambridge.

  • Sondergaard, M., J. P. Jensen & E. Jeppesen, 2003. Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506(1–3): 135–145.

    Article  Google Scholar 

  • Vaughan, K. L., M. C. Rabenhorst & B. A. Needelman, 2009. Saturation and temperature effects on the development of reducing conditions in soils. Soil Science Society of America Journal 73(2): 663–667.

    Article  CAS  Google Scholar 

  • Verhoeven, J. T. A., B. Arheimer, C. Q. Yin & M. M. Hefting, 2006. Regional and global concerns over wetlands and water quality. Trends in Ecology and Evolution 21(2): 96–103.

    Article  PubMed  Google Scholar 

  • Vuillemin, A., D. Ariztegui & P. S. Team, 2013. Geomicrobiological investigations in subsaline maar lake sediments over the last 1500 years. Quaternary Science Reviews 71: 119–130.

    Article  Google Scholar 

  • Wang, H., Z. L. He, Z. M. Lu, J. Z. Zhou, J. D. Van Nostrand, X. H. Xu & Z. J. Zhang, 2012. Genetic linkage of soil carbon pools and microbial functions in subtropical freshwater wetlands in response to experimental warming. Applied and Environmental Microbiology 78(21): 7652–7661.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang, H., J. Holden, K. Spera, X. H. Xu, Z. D. Wang, J. H. Luan, X. Xu & Z. J. Zhang, 2013. Phosphorus fluxes at the sediment-water interface in subtropical wetlands subjected to experimental warming: a microcosm study. Chemosphere 90(6): 1794–1804.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Z. D., J. X. Yao, S. A. Li, J. Y. Zhang, J. J. Li, X. Y. Lin & Z. J. Zhang, 2010. Spatial status and retention potential of phosphorus in riparian wetlands of the Southern Taihu Basin, China. Wetlands 30(1): 149–157.

    Article  CAS  Google Scholar 

  • Weedon, J. T., R. Aerts, G. A. Kowalchuk, R. van Logtestijn, D. Andringa & P. M. van Bodegom, 2013. Temperature sensitivity of peatland C and N cycling: does substrate supply play a role? Soil Biology and Biochemistry 61: 109–120.

    Article  CAS  Google Scholar 

  • Wei, F., 2002. Water and Wastewater Monitoring and Analysis. Environmental Science Press, Beijing.

    Google Scholar 

  • Yergeau, E., S. Bokhorst, S. Kang, J. Z. Zhou, C. W. Greer, R. Aerts & G. A. Kowalchuk, 2012. Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. ISME Journal 6(3): 692–702.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang, Z. J., Z. D. Wang, J. Holden, X. H. Xu, H. Wang, J. H. Ruan & X. Xu, 2012. The release of phosphorus from sediment into water in subtropical wetlands: a warming microcosm experiment. Hydrological Processes 26(1): 15–26.

    Article  Google Scholar 

  • Zhou, J. Z., K. Xue, J. P. Xie, Y. Deng, L. Y. Wu, X. H. Cheng, S. F. Fei, S. P. Deng, Z. L. He, J. D. Van Nostrand & Y. Q. Luo, 2012. Microbial mediation of carbon-cycle feedbacks to climate warming. Nature Climate Change 2(2): 106–110.

    Article  CAS  Google Scholar 

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Acknowledgment

This work was supported by the National Natural Science Foundation of China (41373074), National Ministry of Science and Technology (2013GB23600658), and National Ministry of Water Resources (201301092). This work was also partially supported by the United States Department of Energy, Biological Systems Research on the Role of Microbial Communities in Carbon Cycling Program (DE-SC0004601), and the Oklahoma Bioenergy Center (OBC).

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Zhang, Z., Wang, H., Zhou, J. et al. Redox potential and microbial functional gene diversity in wetland sediments under simulated warming conditions: implications for phosphorus mobilization. Hydrobiologia 743, 221–235 (2015). https://doi.org/10.1007/s10750-014-2039-6

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