INORGANIC NITROGEN STIMULATES METHANE OXIDATION IN COASTAL LAGOON SEDIMENTS
Palavras-chave:
CH4, greenhouse gas, NH4 , NO3-, methanotrophyResumo
Methane (CH4) oxidation is a critical process to reduce CH4 emissions from aquatic environments to the atmosphere. Considering the continuous increase in nitrogen in rivers, lakes, and lagoons from human sources, we re-evaluated the still controversial potential effect of inorganic nitrogen on CH4 oxidation. Here, we approached three shallow coastal lagoons that represent great environmental heterogeneity and used slurry sediments as a model system. The addition of ammonium chloride (NH4Cl) and potassium nitrate (KNO3) significantly stimulated CH4 oxidation in the sediments of all studied lagoons, indicating the potential limitation of nitrogen for the growth of CH4 oxidizing bacteria. Our findings contrast to some previous reports, where ammonium and nitrate inhibited CH4 oxidation in sediments. Indeed, our experiment was performed in a more realistic range in relation to natural concentrations of inorganic nitrogen in aquatic systems (0.5 to 1 mM) and was opposed to extreme concentrations previously used (2 to 50 mM). Our results point to the need to further assess the connection between nitrogen inputs and CH4 budgets in aquatic sediments, considering the potential fuel for CH4 oxidation that may affect the global greenhouse gas balance.
Referências
Anthony, C. 1978. The prediction of growth yields in methylotrophs. Microbiology, 104(1), 91–104.
Arshad, A., Speth, D. R., de Graaf, R. M., Op den Camp, H. J. M., Jetten, M. S. M., & Welte, C. U. 2015. A metagenomics-based metabolic model of nitrate-dependent anaerobic oxidation of methane by Methanoperedens-like archaea. Frontiers in Microbiology, 6, 1423.
Banger, K., Tian, H., & Lu, C. 2012. Do nitrogen fertilizers stimulate or inhibit methane emissions from rice fields? Global Change Biology, 18(10), 3259–3267.
Bižić, M., Klintzsch, T., Ionescu, D., Hindyieh, M., Guenthel, M., Muro-Pastor, A. M., Eckert, W., Urich, T., Keppler, F. & Grossart, H. P. 2020. Aquatic and terrestrial Cyanobacteria produce methane. Science Advances, 6(3), eaax5343.
Bodelier, P. L. E. 2011. Interactions between nitrogenous fertilizers and methane cycling in wetland and upland soils. Current Opinion in Environmental Sustainability, 3(5), 379–388. DOI: 10.1016/j.cosust.2011.06.002
Bodelier, P. L. E., & Laanbroek, H. J. 2004. Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiology Ecology, 47(3), 265–277.
Bodelier, P. L. E., & Steenbergh, A. K. 2014. Interactions between methane and the nitrogen cycle in light of climate change. Current Opinion in Environmental Sustainability, 9–10, 26–36. DOI: 10.1016/j.cosust.2014.07.004
Bodelier, P. L. E., Roslev, P., Henckel, T., & Frenzel, P. 2000. Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature, 403(6768), 421–424.
Boon, P. I., & K. Lee 1997. Methane oxidation in sediments of a floodplain wetland in south-eastern Australia. Letters in Applied Microbiology, 25, 138–142.
Bosse, U., Frenzel, P., & Conrad, R. 1993. Inhibition of methane oxidation by ammonium in the surface layer of a littoral sediment. FEMS Microbiology Ecology, 13(2), 123–134.
Bower, C. E., & Holm-Hansen, T. 1980. A salicylate–hypochlorite method for determining ammonia in seawater. Canadian Journal of Fisheries and Aquatic Sciences, 37(5), 794–798.
Cai, Z. C., & A. R. Mosier 2000. Effect of NH4Cl addition on methane oxidation by paddy soils. Soil Biology and Biochemistry. 32(11–12), 1537–1545.
Conrad, R, & Rothfuss, F. 1991. Methane oxidation in the soil surface layer of a flooded rice field and the effect of ammonium. Biology and Fertility of Soils, 12(1), 28–32.
Conrad, Ralf. 2007. Microbial ecology of methanogens and methanotrophs. Advances in Agronomy, 96, 1–63.
de Angelis, M. A., & M. I. Scranton 1993. Fate of methane in the Hudson River and Estuary. Global Biogeochemical Cycles. 7, 509–523.
Dedysh, S. N., Knief, C., & Dunfield, P. F. 2005. Methylocella species are facultatively methanotrophic. Journal of Bacteriology, 187(13), 4665–4670.
DelSontro, T., del Giorgio, P. A. & Prairie, Y. T. 2018. No longer a Paradox: The interaction between physical transport and biological processes explains the spatial distribution of surface water methane within and across lakes. Ecosystems, 21(6), 560 1073–1087.
Deutzmann, J. S., & B. Schink 2011. Anaerobic oxidation of methane in sediments of Lake Constance, an oligotrophic freshwater lake. Applied and Environmental Microbiology. 77(13), 4429–4436.
Downing, J. A., Prairie, Y. T., Cole, J. J., Duarte, C. M., Tranvik, L. J., Striegl, R. G., McDowell, W. H., Kortelainen, P., Caraco, N. F., Melack, J. M., & Middelburg, J. J. 2006. The global abundance and size distribution of lakes, ponds, and impoundments. Limnology and Oceanography, 51(5), 2388–2397.
Duan, Y., Elsgaard, L., & Petersen, S. O. 2013. Inhibition of methane oxidation in a slurry surface crust by inorganic nitrogen: an incubation study. Journal of Environmental Quality, 42(2), 507–515.
Dunfield, P., & Knowles, R. 1995. Kinetics of inhibition of methane oxidation by nitrate, nitrite, and ammonium in a humisol. Applied and Environmental Microbiology, 61(8), 3129–3135.
Esteves, Francisco de Assis, A. Caliman, J. M. Santangelo, R. D. Guariento, V. F. Farjalla, & Bozelli, R. L. 2008. Neotropical coastal lagoons: an appraisal of their biodiversity, functioning, threats and conservation management. Brazilian Journal of Biology, 68(4), 967–981.
Fistarol, G. O., Coutinho, F. H., Moreira, A. P. B., Venas, T., Cánovas, A., de Paula, S. E. M., Coutinho, R., Moura, R L., Valentin, J. L., Tenenbaum, D. R., Paranhos, R., do Valle, R. A. B., Vicente, A. C. P., Amado Filho, G. M., Pereira, R. C., Kruger, R., Rezende, C. E., Thompson, C. C., Salomon, P. S., & Thompson, F. L. 2015. Environmental and Sanitary Conditions of Guanabara Bay, Rio de Janeiro. Frontiers in Microbiology, 6, 1232.
Frenzel, P., Thebrath, B., & Conrad, R. 1990. Oxidation of methane in the oxic surface layer of a deep lake sediment (Lake Constance). FEMS Microbiology Ecology, 6(2), 149–158.
Galloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., et al. 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science, 320(5878), 889–892.
Golterman, H. L., Clymo, R. S., & Ohnstad, M. A. M. 1978. Methods for physical and chemical analysis of freshwater. Londres: Blackwell Scientific Publications. p. 213.
Haroon, M. F., Hu, S., Shi, Y., Imelfort, M., Keller, J., Hugenholtz, P., Yuan, Z., & Tyson, G. W. 2013. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature, 500(7464), 567–570.
He, R., Chen, M., Ma, R.-C., Su, Y., & Zhang, X. 2017. Ammonium conversion and its feedback effect on methane oxidation of Methylosinus sporium. Journal of Bioscience and Bioengineering, 123(4), 466–473.
Henriques, R. P. B., Araújo, D. S. D., Esteves, F. A. & Franco, A. C. 1988: Análise preliminar das comunidades de macrófitas aquáticas da lagoa Cabiúnas, Rio de Janeiro, Brasil. Acta Limnologica Brasiliensia 11, 783–802.
Hu, S., Raymond, J., Zeng, J., Keller, P., Lant, A., & Z. Yuan. 2011. Effect of nitrate and nitrite on the selection of microorganisms in the denitrifying anaerobic methane oxidation process. Environmental Microbiology Reports. 3(3), 315–319.
Hu, M., Wilson, B. J., Sun, Z., Huang, J., & Tong, C. 2018. Effects of nitrogen and sulphate addition on methane oxidation in the marsh soil of a typical subtropical estuary (Min River) in China. Chemistry and Ecology, 34(7), 610–623.
Kim, J., Kim, D. D., & Yoon, S. 2018. Rapid isolation of fast-growing methanotrophs from environmental samples using continuous cultivation with gradually increased dilution rates. Applied Microbiology and Biotechnology, 102(13), 5707–5715.
Kruger, M., & Frenzel, P. 2003. Effects of N-fertilisation on CH 4 oxidation and production, and consequences for CH 4 emissions from microcosms and rice fields. Global Change Biology, 9(5), 773–784.
Krüger, M., Eller, G., Conrad, R., & Frenzel, P. 2002. Seasonal variation in pathways of CH4 production and in CH4 oxidation in rice fields determined by stable carbon isotopes and specific inhibitors. Global Change Biology, 8(3), 265–280.
Liikanen, A., L. Flojt, & P. Martikainen 2002. Gas dynamics in eutrophic lake sediments affected by oxygen, nitrate, and sulfate. Journal of Environmental Quality, 31, 338–349.
Liikanen, A., E. Ratilainen, S. Saarnio, J. Alm, P. J. Martikainen, & J. Silvola. 2003. Greenhouse gas dynamics in boreal, littoral sediments under raised CO2 and nitrogen supply. Freshwater Biology, 48, 500–511.
Liu, L., & Greaver, T. L. 2009. A review of nitrogen enrichment effects on three biogenic GHGs: the CO2 sink may be largely offset by stimulated N 2 O and CH 4 emission. Ecology Letters, 12(10), 1103–1117. DOI: 10.1111/j.1461-0248.2009.01351.x
Mancinelli, R. L. (1995). The regulation of methane oxidation in soil. Annual Review of Microbiology, 49(1), 581–605.
Marotta, H., Duarte, C.M., Pinho, L., Enrich-Prast, A. 2010. Rainfall leads to increased pCO2 in Brazilian coastal lakes. Biogeosciences 7, 1607–1614.
Martinelli, L. A., Howarth, R. W., Cuevas, E., Filoso, S., Austin, A. T., Donoso, L., Huszar, V., Keeney, D., Lara, L. L., Llerena, C., Mcissac, G., Medina, E., Ortiz-Zayas, J., Scavia, D., Schindler, D. W., Soto, D., & Townsend, A. 2006. Sources of reactive nitrogen affecting ecosystems in Latin America and the Caribbean: current trends and future perspectives. Biogeochemistry, 79, 3–24. DOI: 10.1007/978-1-4020-5517-1_1
Mohammadi, S. S., Pol, A., van Alen, T., Jetten, M. S. M., & Op den Camp, H. J. M. 2017. Ammonia Oxidation and Nitrite Reduction in the Verrucomicrobial Methanotroph Methylacidiphilum fumariolicum SolV. Frontiers in Microbiology, 8. DOI: 10.3389/fmicb.2017.01901
Murase, J., & A. Sugimoto 2005. Inhibitory effect of light on methane oxidation in the pelagic water column of a mesotrophic lake (Lake Biwa, Japan). Limnology and Oceanography 50, 1339–1343.
Myhre, G., D. Shindell, F.-M. Bréon, W. Collins, J. Fuglestvedt, J. Huang, D. Koch, J.-F. Lamarque, D. Lee, B. Mendoza, T. Nakajima, A. Robock, G. Stephens, T. Takemura & Zhang, H. 2013. Anthropogenic and Natural Radiative Forcing. In: Stocker, T. F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S. K., Boschung, J., Nauels, A., Xia, Y., Bex, V., & Midgley, P. M. (Eds.), Climate Change 2013 - The Physical Science Basis; Working Group I contribution to the fifth assessment report of the Intergovernmental Panel on Climate Change pp. 659–740. Cambridge: Cambridge University Press. DOI: 10.1017/CBO9781107415324.018
Van der Nat, F., De Brouwer, J., Middelburg, J. J., & Laanbroek, H. J. 1997. Spatial distribution and inhibition by ammonium of methane oxidation in intertidal freshwater marshes. Applied and Environmental Microbiology, 63(12), 4734–4740.
Nold, S. C., Boschker, H. T. S., Pel, R., & Laanbroek, H. J. 1999. Ammonium addition inhibits 13C-methane incorporation into methanotroph membrane lipids in a freshwater sediment. FEMS Microbiology Ecology, 29(1), 81–89.
Noll, M., Frenzel, P., & Conrad, R. 2008. Selective stimulation of type I methanotrophs in a rice paddy soil by urea fertilization revealed by RNA-based stable isotope probing. FEMS Microbiology Ecology, 65(1), 125–132.
O’neill, J. G., & Wilkinson, J. F. 1977. Oxidation of ammonia by methane-oxidizing bacteria and the effects of ammonia on methane oxidation. Microbiology, 100(2), 407–412.
Osudar, R., Klings, K. W., Wagner, D., Bussmann, I. 2017. Effect of salinity on microbial methane oxidation in freshwater and marine environments. Aquatic Microbial Ecology, 80, 181–192.
Parker, R. J., Boesch, H., McNorton, J., Comyn-Platt, E., Gloor, M., Wilson, C., Chipperfield, M. P., Haymanf, G. D., & Bloom, A. 2018. Evaluating year-to-year anomalies in tropical wetland methane emissions using satellite CH4 observations. Remote Sensing of Environment, 211, 261–275.
Rissanen, A. J., Jilbert, T., Simojoki, A., Mangayil, R., Aalto, S. L., Peura, S., & H. Jäntti 2021. Nitrate Enhances Anaerobic Oxidation Of Methane In Boreal Lake Sediments. Biorxiv Preprint.
Rockström, J., Steffen, W., Noone, K., Persson, Å., Chapin III, F. S., Lambin, E., Lenton, T. M., Scheffer, M., Folke, C., Schellnhuber, H., Nykvist, B., De Wit, C. A., Hughes, T., van der Leeuw, S., Rodhe, H., Sörlin, S., Snyder, P. K., Costanza, R., Svedin, U., Falkenmark, M., Karlberg, L., Corell, R. W., Fabry, V. J., Hansen, J., Walker, B., Liverman, D., Richardson, K., Crutzen, P., & Foley, J. 2009. Planetary boundaries: exploring the safe operating space for humanity. Ecology and Society, 14(2).
Rudd, J. W. M., A. Furutani, R. J. Flett, & R. D. Hamilton. 1976. Factors controlling methane oxidation in shield lakes: The role of nitrogen fixation and oxygen concentration. Limnology and Oceanography, 21, 357–364.
Sabrekov, A. F., Glagolev, M. V, Alekseychik, P. K., Smolentsev, B. A., Terentieva, I. E., Krivenok, L. A., & Maksyutov, S. S. 2016. A process-based model of methane consumption by upland soils. Environmental Research Letters, 11(7), 75001.
Saunois, M., Stavert, A. R., Poulter, B., Bousquet, P., Canadell, J. G., Jackson, R. B., Raymond, P. A., Dlugokencky, E. J., Houweling, S., Patra, P. K., Ciais, P., Arora, V. K., Bastviken, D., Bergamaschi, P., Blake, D. R., Brailsford, G., Bruhwiler, L., Carlson, K. M., Carrol, M., Castaldi, S., Chandra, N., Crevoisier, C., Crill, P. M., Covey, K., Curry, C. L., Etiope, G., Frankenberg, C., Gedney, N., Hegglin, M. I., Höglund-Isaksson, L., Hugelius, G., Ishizawa, M., Ito, A., Janssens-Maenhout, G., Jensen, K. M., Joos, F., Kleinen, T., Krumme, P. B., Langenfelds, R. L., Laruelle, G. G., Liu, L., Machida, T., Maksyutov, S., McDonald, K. C. McNorton, J., Miller, P. A., Melton, J. R., Morino, I. Müller, J., Murguia-Flores, F., Naik, V., Niwa, Y., Noce, S., O’Doherty, S., Parker, R. J., Peng, C., Peng, S., Peters, G. P., Prigent, C., Prinn, R., Ramonet, M., Regnier, P., Riley, W. J., Rosentreter, J., Segers, A., Simpson, I. J., Shi, H., Smith, S. J., Steele, L. P., Thornton, B. F., Tian, H., Tohjima, Y., Tubiello, F. N., Tsuruta, A., Viovy, N., Voulgarakis, A., Weber, T. S., van Weele, M., van der Werf, G. R., Weiss, R. F., Worthy, D., Wunch, D., Yin, Y., Yoshida, Y., Zhang, W., Zhang, Z., Zhao, Y., Zheng, B., Zhu, Q., Zhu, Q., & Zhuang, Q. 2020. The Global Methane Budget 2000–2017. Earth System Science Data, 12(3), 1561–1623. DOI: 10.5194/essd-12-1561-2020
Sawakuchi, H. O., Bastviken, D., Sawakuchi, A. O., Ward, N. D., Borges, C. D., Tsai, S. M., Richey, J. E., Ballester, M. V. R., & Krusche, A. V. 2016. Oxidative mitigation of aquatic methane emissions in large Amazonian rivers. Global Change Biology, 22(3), 1075–1085. DOI: 10.1111/gcb.13169
Sawakuchi, H. O., Bastviken, D., Enrich-Prast, A., Ward, N. D., Camargo, P. B., & Richey, J. E. 2021. Low Diffusive Methane Emissions From the Main Channel of a Large Amazonian Run-of-the-River Reservoir Attributed to High Methane Oxidation. Frontiers in Environmental Science, 9. DOI: 10.3389/fenvs.2021.655455
Shen, L., Tian, D., Hui, M., Cheng, H., Liu, X., Yang, Y., & L. Liu. 2020. Different responses of nitrite- and nitrate-dependent anaerobic methanotrophs to increasing nitrogen loading in a freshwater reservoir. Environmental Pollution. 263, 114623.
Shrestha, M., Shrestha, P. M., Frenzel, P., & Conrad, R. 2010. Effect of nitrogen fertilization on methane oxidation, abundance, community structure, and gene expression of methanotrophs in the rice rhizosphere. The ISME Journal, 4(12), 1545–1556.
Tang, K. W., McGinnis, D. F., Frindte, K., Brüchert, V. and Grossart, H. P. 2014. Paradox reconsidered: Methane oversaturation in well-oxygenated lake waters, Limnology and Oceanography, 59(1), 275–284.
Tays, C., Guarnieri, M. T., Sauvageau, D., & Stein, L. Y. 2018. Combined effects of carbon and nitrogen source to optimize growth of proteobacterial methanotrophs. Frontiers in Microbiology, 9, 2239.
Theisen, A. R., Ali, M. H., Radajewski, S., Dumont, M. G., Dunfield, P. F., McDonald, I. R., Dedysh, S. N., Miguez, C. B., & Murrell, J. C. 2005. Regulation of methane oxidation in the facultative methanotroph Methylocella silvestris BL2. Molecular Microbiology, 58(3), 682–692.
van der Nat, F. J. W. A., de Brouwer, J. F. C., Middelburg, J. J., & Laanbroek, H. J. 1997. Spatial distribution and inhibition by ammonium of methane oxidation in intertidal freshwater marshes. Applied and Environmental Microbiology, 63, 4734–4740.
Yang, Y., Tong, T., Chen, J., Liu, Y., & Xie, S. 2020. Ammonium Impacts Methane Oxidation and Methanotrophic Community in Freshwater Sediment. Frontiers in Bioengineering and Biotechnology, 8, 250.
Woszczyk M, Tylmann W, Je¸drasik J, Szarafin T, Stach A, Skrzypczak J, Lutyńska M. 2014. Recent sedimentation dynamics in a shallow coastal lake (Lake Sarbsko, northern Poland): Driving factors, processes and effects. Marine and Freshwater Research, 65, 1102–1115.
Zhu, B., van Dijk, G., Fritz, C., Smolders, A. J. P., Pol, A., Jetten, M. S. M., & K. F. Ettwiga. 2012. Anaerobic oxidization of methane in a minerotrophic peatland: Enrichment of nitrite-dependent methane-oxidizing bacteria. Applied and Environmental Microbiology. 78(24), 8657–8665.
