The return of crop residue and green manure into agricultural soil is known to be important agricultural management strategies, yet how they affect the anammox process remains poorly characterized. A field experiment containing four treatments: chemical fertilizer (F), F plus rice straw (FS), FS plus green manure (FSM), FSM with integrated management (FSMM), was performed to examine the effects of incorporation of rice straw and green manure residues on anammox. The results showed that the anammox activities in FS and FSM treatments (0.65 and 0.80 nmol N g?1 soil h?1, respectively) were significantly lower than those in F and FSMM treatments (1.60 and 1.28 nmol N g?1 soil h?1, respectively). Anammox contributed 4.07%?4.95% of total N loss in soil incorporated with residues, lower than soil treated with chemical fertilizer only (9.13%), the remaining being due to denitrification. However, the abundance of the hzsB gene (the hydrazine synthase ?-subunit gene) in FS and FSM treatments (1.13 ? 106 and 1.18 ? 106 copies g?1 soil) were significantly higher than soil using chemical fertilizer only (7.49 ? 105 copies g?1 soil) while showed no significant difference with FSMM treatment (8.81 ? 105 copies g?1 soil). Illumina sequencing indicated that Brocadia was the dominant anammox genus, following by Scalindua and Kuenenia. Anammox bacterial diversity was altered after 4-year incorporation of rice straw and green manure, as shown by ?-diversity indices. We concluded that rice straw and green manure incorporated with mineral fertilizer reduce N removal from paddy soil in terms of anammox in spite of stimulating anammox bacterial growth.
References
Adachi, K., Chaitep, W., Senboku, T., 1997. Promotive and inhibitory effects of rice straw and cellulose application on rice plant growth in pot and field experiments. Soil Science and Plant Nutrition 43, 369?386.
CAS? Article? Google Scholar?
Azam, F., Lodhi, A., Ashraf, M., 1991. Availability ofsoil and fertilizer nitrogen to wetland rice following wheat straw amendment. Biology and Fertility of Soils 11, 97?100.
CAS? Article? Google Scholar?
Bai, R., Chen, X., He, J.Z., Shen, J.P., Zhang, L.M., 2015a. Candidatus Brocadia and Candidatus Kuenenia predominated in anammox bacterial community in selected Chinese paddy soils. Journal of Soils and Sediments 15, 1977?1986.
CAS? Article? Google Scholar?
Bai, R., Xi, D., He, J.Z., Hu, H.W., Fang, Y.T., Zhang, L.M., 2015b. Activity, abundance and community structure of anammox bacteria along depth profiles in three different paddy soils. Soil Biology & Biochemistry 91, 212?221.
CAS? Article? Google Scholar?
Bijay, S., Shan, Y.H., Johnson-Beebout, S.E., Yadvinder, S., Buresh, R.J., 2008. Chapter 3 Crop Residue Management for Lowland Rice-Based Cropping Systems in Asia, Advances in Agronomy. Academic Press, pp. 117?199.
Dale, O.R., Tobias, C.R., Song, B., 2009. Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environmental Microbiology 11, 1194?1207.
CAS? Article? Google Scholar?
Dalsgaard, T., Thamdrup, B., Far?as, L., Revsbech, N.P., 2012. Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific. Limnology and Oceanography 57, 1331?1346.
CAS? Article? Google Scholar?
Eagle, A.J., Bird, J.A., Horwath, W.R., Linquist, B.A., Brouder, S.M., Hill, J.E., van Kessel, C., 2000. Rice yield and nitrogen utilization efficiency under alternative straw management practices. Agronomy Journal 92, 1096?1103.
CAS? Article? Google Scholar?
Erinle, K.O., Marschner, P., 2020. Phosphorus and nitrogen in the soil interface between two plant residues differing in C/nutrient ratio: A short-term laboratory incubation study. Soil Ecology Letters 2, 188?194.
CAS? Article? Google Scholar?
Gori, F., Tringe, S.G., Kartal, B., Marchiori, E., Jetten, M.S.M., 2012. The metagenomic basis of anammox metabolism in Candidatus ?Brocadia fulgida? (vol 39, pg 1799, 2011). Biochemical Society Transactions 40, 295?295.
CAS? Article? Google Scholar?
Gu, C., Zhou, H., Zhang, Q., Zhao, Y., Di, H., Liang, Y., 2017. Effects of various fertilization regimes on abundance and activity of anaerobic ammonium oxidation bacteria in rice-wheat cropping systems in China. Science of the Total Environment 599?600, 1064?1072.
Article? CAS? Google Scholar?
Guo, J.H., Liu, X.J., Zhang, Y., Shen, J.L., Han, W.X., Zhang, W.F., Christie, P., Goulding, K.W.T., Vitousek, P.M., Zhang, F.S., 2010. Significant acidification in major Chinese croplands. Science 327, 1008?1010.
CAS? Article? Google Scholar?
Hou, M.M., Xu, R., Lin, Z.Y., Xi, D., Wang, Y., Wen, J.L., Nie, S.A., Zhong, F.L., 2020. Vertical characteristics of anaerobic oxidation of ammonium (anammox) in a coastal saline-alkali field. Soil & Tillage Research 198, 198.
Article? Google Scholar?
Jetten, M., Camp, H., Kuenen, J., Strous, M., 2010. Description of the Order Brocadiales. In: Krieg, N.R., Ludwig, W., Whitman, W.B., eds. The Bacteroidetes, Spirochaetes, Tenericutes (mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes, Springer, Berlin, pp. 596?603
Google Scholar?
Li, F., Wang, Z., Dai, J., Li, Q., Wang, X., Xue, C., Liu, H., He, G., 2015. Fate of nitrogen from green manure, straw, and fertilizer applied to wheat under different summer fallow management strategies in dryland. Biology and Fertility of Soils 51, 769?780.
Article? Google Scholar?
Li, H., Yang, X.R., Weng, B.S., Su, J.Q., Nie, S.A., Gilbert, J.A., Zhu, Y. G., 2016. The phenological stage of rice growth determines anaerobic ammonium oxidation activity in rhizosphere soil. Soil Biology & Biochemistry 100, 59?65.
CAS? Article? Google Scholar?
Li, T., Gao, J.S., Bai, L.Y., Wang, Y.N., Huang, J., Kumar, M., Zeng, X. B., 2019. Influence of green manure and rice straw management on soil organic carbon, enzyme activities, and rice yield in red paddy soil. Soil & Tillage Research 195, 195.
Google Scholar?
Liu, X., Zhang, Y., Han, W., Tang, A., Shen, J., Cui, Z., Vitousek, P., Erisman, J.W., Goulding, K., Christie, P., Fangmeier, A., Zhang, F., 2013. Enhanced nitrogen deposition over China. Nature 494, 459?462.
CAS? Article? Google Scholar?
Lu, R., 2000. Analytical Methods of Soil Agricultural Chemistry. China Agriculture Press, Beijing.
Google Scholar?
Monballiu, A., Desmidt, E., Ghyselbrecht, K., De Clippeleir, H., Van Hulle, S.W.H., Verstraete, W., Meesschaert, B., 2013. Enrichment of anaerobic ammonium oxidizing (Anammox) bacteria from OLAND and conventional sludge: Features and limitations. Separation and Purification Technology 104, 130?137.
CAS? Article? Google Scholar?
Nie, S., Lei, X., Zhao, L., Wang, Y., Wang, F., Li, H., Yang, W., Xing, S., 2018a. Response of activity, abundance, and composition of anammox bacterial community to different fertilization in a paddy soil. Biology and Fertility of Soils 54, 977?984.
CAS? Article? Google Scholar?
Nie, S., Li, H., Yang, X., Zhang, Z., Weng, B., Huang, F., Zhu, G.B., Zhu, Y.G., 2015. Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere. ISME Journal 9, 2059?2067.
CAS? Article? Google Scholar?
Nie, S., Zhu, G.B., Singh, B., Zhu, Y.G., 2019. Anaerobic ammonium oxidation in agricultural soils-synthesis and prospective. Environmental Pollution 244, 127?134.
CAS? Article? Google Scholar?
Nie, S.A., Lei, X.M., Zhao, L.X., Brookes, P.C., Wang, F., Chen, C.R., Yang, W.H., Xing, S.H., 2018b. Fungal communities and functions response to long-term fertilization in paddy soils. Applied Soil Ecology 130, 251?258.
Article? Google Scholar?
Pan, F.F., Yu, W.T., Ma, Q., Zhou, H., Jiang, C.M., Xu, Y.G., Ren, J.F., 2017. Influence of 15N-labeled ammonium sulfate and straw on nitrogen retention and supply in different fertility soils. Biology and Fertility of Soils 53, 303?313.
CAS? Article? Google Scholar?
Pe?uelas, J., Poulter, B., Sardans, J., Ciais, P., van der Velde, M., Bopp, L., Boucher, O., Godderis, Y., Hinsinger, P., Llusia, J., Nardin, E., Vicca, S., Obersteiner, M., Janssens, I.A., 2013. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications 4, 2934.
Article? CAS? Google Scholar?
Rios-Del Toro, E.E., Cervantes, F.J., 2019. Anaerobic ammonium oxidation in marine environments: contribution to biogeochemical cycles and biotechnological developments for wastewater treatment. Reviews in Environmental Science and Biotechnology 18, 11?27.
CAS? Article? Google Scholar?
Roesti, D., Gaur, R., Johri, B.N., Imfeld, G., Sharma, S., Kawaljeet, K., Aragno, M., 2006. Plant growth stage, fertiliser management and bio-inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields. Soil Biology & Biochemistry 38, 1111?1120.
CAS? Article? Google Scholar?
Schmid, M., Twachtmann, U., Klein, M., Strous, M., Juretschko, S., Jetten, M., Metzger, J.W., Schleifer, K.H., Wagner, M., 2000. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Systematic and Applied Microbiology 23, 93?106.
CAS? Article? Google Scholar?
Schmid, M.C., Risgaard-Petersen, N., van de Vossenberg, J., Kuypers, M.M.M., Lavik, G., Petersen, J., Hulth, S., Thamdrup, B., Canfield, D., Dalsgaard, T., Rysgaard, S., Sejr, M.K., Strous, M., den Camp, H.J.M.O., Jetten, M.S.M., 2007. Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environmental Microbiology 9, 1476?1484.
CAS? Article? Google Scholar?
Schubert, C.J., Durisch-Kaiser, E., Wehrli, B., Thamdrup, B., Lam, P., Kuypers, M.M., 2006. Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environmental Microbiology 8, 1857?1863.
CAS? Article? Google Scholar?
Shen, J.P., Zhang, L.M., Guo, J.F., Ray, J.L., He, J.Z., 2010. Impact of long-term fertilization practices on the abundance and composition of soil bacterial communities in Northeast China. Applied Soil Ecology 46, 119?124.
Article? Google Scholar?
Shen, L.D., Liu, S., Huang, Q., Lian, X., He, Z.F., Geng, S., Jin, R.C., He, Y.F., Lou, L.P., Xu, X.Y., Zheng, P., Hu, B.L., 2014. Evidence for the cooccurrence of nitrite-dependent anaerobic ammonium and methane oxidation processes in a flooded paddy field. Applied and Environmental Microbiology 80, 7611?7619.
Article? CAS? Google Scholar?
Shen, L.D., Liu, X., Wu, H.S., Tian, M.H., Ran, P., Liu, J.Q., Yang, Y.L., Yang, W.T., Wang, H.Y., 2020. Effect of different fertilization regimes on the vertical distribution of anaerobic ammonium oxidation in paddy soils. European Journal of Soil Biology 99, 103206.
CAS? Article? Google Scholar?
Shen, L.D., Wu, H.S., Liu, X., Li, J., 2017. Vertical distribution and activity of anaerobic ammonium-oxidising bacteria in a vegetable field. Geoderma 288, 56?63.
CAS? Article? Google Scholar?
Simmons, B.L., Coleman, D.C., 2008. Microbial community response to transition from conventional to conservation tillage in cotton fields. Applied Soil Ecology 40, 518?528.
Article? Google Scholar?
Song, A., Li, Z., Liao, Y., Liang, Y., Wang, E., Wang, S., Li, X., Bi, J., Si, Z., Lu, Y., Nie, J., Fan, F., 2021. Soil bacterial communities interact with silicon fraction transformation and promote rice yield after long-term straw return. Soil Ecology Letters https://doi.org/10.1007/s42832-021-0076-4
Spedding, T.A., Hamel, C., Mehuys, G.R., Madramootoo, C.A., 2004. Soil microbial dynamics in maize-growing soil under different tillage and residue management systems. Soil Biology & Biochemistry 36, 499?512.
CAS? Article? Google Scholar?
Strous, M., Heijnen, J.J., Kuenen, J.G., Jetten, M.S.M., 1998. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Applied Microbiology and Biotechnology 50, 589?596.
CAS? Article? Google Scholar?
Thamdrup, B., Dalsgaard, T., 2002. Production of N(2) through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Applied and Environmental Microbiology 68, 1312?1318.
CAS? Article? Google Scholar?
Verma, T.S., Bhagat, R.M., 1992. Impact of rice straw management practices on yield, nitrogen uptake and soil properties in a wheat-rice rotation in northern India. Fertilizer Research 33, 97?106.
CAS? Article? Google Scholar?
Voisin, A.S., Gueguen, J., Huyghe, C., Jeuffroy, M.H., Magrini, M.B., Meynard, J.M., Mougel, C., Pellerin, S., Pelzer, E., 2014. Legumes for feed, food, biomaterials and bioenergy in Europe: a review. Agronomy for Sustainable Development 34, 361?380.
CAS? Article? Google Scholar?
Wang, J., Gu, J.D., 2013. Dominance of Candidatus Scalindua species in anammox community revealed in soils with different duration of rice paddy cultivation in Northeast China. Applied Microbiology and Biotechnology 97, 1785?1798.
CAS? Article? Google Scholar?
Wang, S., Zhu, G., Peng, Y, Jetten, M.S.M., Yin, C., 2012a. Anammox bacterial abundance, activity, and contribution in riparian sediments of the Pearl River estuary. Environmental Science & Technology 46, 8834?8842.
CAS? Article? Google Scholar?
Wang, Y., Zhu, G., Harhangi, H.R., Zhu, B., Jetten, M.S.M., Yin, C., Op den Camp, H.J.M., 2012b. Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane-oxidizing bacteria in a paddy soil. FEMS Microbiology Letters 336, 79?88.
CAS? Article? Google Scholar?
Xu, L., Zhang, B., Wang, E., Zhu, B., Yao, M., Li, C., Li, X., 2021. Soil total organic carbon/total nitrogen ratio as a key driver deterministically shapes diazotrophic community assemblages during the succession of biological soil crusts. Soil Ecology Letters https://doi.org/10.1007/s42832-020-0075-x
Yang, L., Zhou, X., Liao, Y.L., Lu, Y.H., Nie, J., Cao, W.D., 2019. Co-incorporation of rice straw and green manure benefits rice yield and nutrient uptake. Crop Science 59, 749?759.
Article? CAS? Google Scholar?
Yang, X.R., Li, H., Nie, S.A., Su, J.Q., Weng, B.S., Zhu, G.B., Yao, H. Y, Gilbert, J.A., Zhu, Y.G., 2015. Potential contribution of anammox to nitrogen loss from paddy soils in Southern China. Applied and Environmental Microbiology 81, 938?947.
Article? CAS? Google Scholar?
Yoshinaga, I., Amano, T., Yamagishi, T., Okada, K., Ueda, S., Sako, Y., Suwa, Y., 2011. Distribution and diversity of anaerobic ammonium oxidation (anammox) bacteria in the sediment of a eutrophic freshwater lake, Lake Kitaura, Japan. Microbes and Environments 26, 189?197.
Article? Google Scholar?
Yu, F., Shi, W., 2015. Nitrogen use efficiencies of major grain crops in China in recent 10 years. Acta Pedologica Sinica 52, 1311?1324.
Google Scholar?
Zhang, J.B., Zhu, T.B., Cai, Z.C., Qin, S.W., Muller, C., 2012. Effects of long-term repeated mineral and organic fertilizer applications on soil nitrogen transformations. European Journal of Soil Science 63, 75?85.
CAS? Article? Google Scholar?
Zhang, Y.Q., Wen, M.X., Li, X.P., Shi, X.J., 2014. Long-term fertilisation causes excess supply and loss of phosphorus in purple paddy soil. Journal of the Science of Food and Agriculture 94, 1175?1183.
CAS? Article? Google Scholar?
Zhou, G., Cao, W., Bai, J., Xu, C., Zeng, N., Gao, S., Rees, R.M., 2019. Non-additive responses of soil C and N to rice straw and hairy vetch (Vicia villosa Roth L.) mixtures in a paddy soil. Plant and Soil 436, 229?244.
CAS? Article? Google Scholar?
Zhou, G.P., Gao, S.J., Lu, Y.H., Liao, Y.L., Nie, J., Cao, W.D., 2020a. Co-incorporation of green manure and rice straw improves rice production, soil chemical, biochemical and microbiological properties in a typical paddy field in southern China. Soil & Tillage Research 197, 197.
Google Scholar?
Zhou, G.P., Gao, S.J., Xu, C.X., Zeng, N.H., Rees, R.M., Cao, W.D., 2020b. Co-incorporation of Chinese milk vetch (Astragalus sinicus L.) and rice (Oryza sativa L.) straw minimizes CH4 emissions by changing the methanogenic and methanotrophic communities in a paddy soil. European Journal of Soil Science 71, 924?939.
CAS? Google Scholar?
Zhu, B., Yi, L.X., Hu, Y.G., Zeng, Z.H., Lin, C.W., Tang, H.M., Yang, G. L., Xiao, X.P., 2014. Nitrogen release from incorporated N15-labelled Chinese milk vetch (Astragalus sinicus L.) residue and its dynamics in a double rice cropping system. Plant and Soil 374, 331?344.
CAS? Article? Google Scholar?
Zhu, G., Wang, S., Wang, C., Zhou, L., Zhao, S., Li, Y., Li, F., Jetten, M. S.M., Lu, Y., Schwark, L., 2019. Resuscitation of anammox bacteria after >10,000 years of dormancy. ISME Journal 13, 1098?1109.
CAS? Article? Google Scholar?
Zhu, G., Wang, S., Wang, Y., Wang, C., Risgaard-Petersen, N., Jetten, M.S.M., Yin, C., 2011. Anaerobic ammonia oxidation in a fertilized paddy soil. ISME Journal 5, 1905?1912.
CAS? Article? Google Scholar?
Zhu, G., Wang, S., Zhou, L., Wang, Y., Zhao, S., Xia, C., Wang, W., Zhou, R., Wang, C., Jetten, M.S.M., Hefting, M.M., Yin, C., Qu, J., 2015. Ubiquitous anaerobic ammonium oxidation in inland waters of China: an overlooked nitrous oxide mitigation process. Scientific Reports 5, 17306.
CAS? Article? Google Scholar?
Zhu, Z., 2008. Research on soil nitrogen in China. Acta Pedologica Sinca 45, 778?783.
Google Scholar?
This study was financially supported by Joint Regional Innovation and Development Fund (UI9A2048), the National Key Research and Development Program of China (2016YFD0300901, 2016YFD0300906), and the Natural Science Foundation of Hunan Province (2019JJ50338). The author San?an Nie greatly thanks the National Natural Science Foundation of China (4170010194), as well as Dr. Dan Xi and Miss Yi Wang, for their kindly help in the stable isotope experiment.
Authorship statement: San?an Nie and Hua Wang designed the work. Geng Sun and Mei Sun carried out the 15N-isotope experiment, analyzed the data, and wrote the manuscript with support from all authors. Zunchang Luo, Chao Li, and Xiaoping Xiao were involved in planting and supervised the study. Xiaojing Li and Junjie Zhong participated in soil sampling and soil physicochemical analysis. All authors provided critical feedback and helped shape the research.
The authors declare no known conflict of interest.
? Anammox responded to different fertilization practices.
? Organic residues treated soils contributed lower (4.07%?4.95%) N loss than solely chemical fertilizer (9.13%) in terms of anammox.
? Incorporation of organic residues increased the abundance of anammox bacteria but decreased the activity.
? The anammox activity was not related to functional gene abundance and soil physico-chemical properties.
Sun, G., Sun, M., Luo, Z. et al. Effects of different fertilization practices on anammox activity, abundance, and community compositions in a paddy soil. Soil Ecol. Lett. 4, 254?263 (2022). https://doi.org/10.1007/s42832-021-0103-5
