Research Progress and Prospect of Nitrogen Cycling and Corresponding Functional Microbes in Aquaculture Environments

doi:10.11924/j.issn.1000-6850.casb2025-0062

Abstract

Abstract:

Microbial driven nitrogen cycle processes play a crucial role in promoting material cycling within aquaculture systems, purifying aquaculture water environments, and maintaining ecosystem balance. Compared to natural ecosystems, aquaculture systems receive higher anthropogenic inputs of nitrogen, exhibit a rich diversity of nitrogen forms, and have their nitrogen cycling processes and associated microorganisms influenced and regulated by intertwined, complex, and easily fluctuating environmental factors. This article elucidates the ecological characteristics of aquaculture environments and reviews research progress on the major nitrogen cycle processes, including nitrogen fixation, ammonification, nitrification, denitrification, anaerobic ammonium oxidation (anammox), and dissimilatory nitrate reduction to ammonium (DNRA) and their associated microbial communities within aquaculture ecosystems. It summarizes the environmental impact characteristics of nitrogen-cycling functional microorganisms. It discusses other potential ion redox reactions coupled with nitrogen cycling processes in aquaculture environments. Finally, the future research directions for the nitrogen cycle in aquaculture environments are prospected. The aim is to deepen the understanding of nitrogen cycling processes and their functional microorganisms in aquaculture systems, thereby providing a theoretical foundation for the purification of nitrogen in aquaculture environments.

Key words: aquaculture, nitrogen cycle, functional gene abundance, environmental impact

XU Chengpeng, SHEN Feng, XU Huimin, MENG Shunlong, SONG Chao, FAN Limin, QIU Liping, LI Dandan, FANG Longxiang, LIU Zhuping, BING Xuwen. Research Progress and Prospect of Nitrogen Cycling and Corresponding Functional Microbes in Aquaculture Environments[J]. Chinese Agricultural Science Bulletin, 2025, 41(27): 157-164.

Figures/Tables 1

References 55

[1]	LAI X S, LI X G, SONG J M, et al. Nitrogen loss from the coastal shelf of the East China Sea: implications of the organic matter[J]. Science of the total environment, 2023, 854:158805.
[2]	NIU S H, ZHANG K, LI Z F, et al. Nitrification and denitrification processes in a zero-water exchange aquaculture system: characteristics of the microbial community and potential rates[J]. Frontiers in marine science, 2023,10:1072911.
[3]	KATHARINA K, HANNAH K M, LAURA A B, et al. Single cell analyses reveal contrasting life strategies of the two main nitrifiers in the ocean[J]. Nature communications, 2020,11:767.
[4]	SUZUKI Y, MARUYAMA T, NUMATA H, et al. Performance of a closed recirculating system with foam separation, nitrification and denitrification units for intensive culture of eel: towards zero emission[J]. Aquacultural engineering, 2003, 9(3-4):165-182.
[5]	刘凤坤, 赵吉臣, 许敬轩, 等. 耐盐好氧反硝化菌黏质沙雷氏菌HL4的分离鉴定及脱氮性能[J]. 广东海洋大学学报, 2024, 44(4):38-46.
[6]	YAO L, CHEN C, LIU G, et al. Sediment nitrogen cycling rates and microbial abundance along a submerged vegetation gradient in a eutrophic lake[J]. Science of the total environment, 2018,616-617:899-907.
[7]	金赞芳, 龚嘉临, 施伊丽, 等. 沉积物-水界面氮的源解析和硝化反硝化[J]. 环境科学, 2017, 38(4):1423-1430.
[8]	LI Z, LI L, SUN H Y, et al. Ammonia assimilation: A double-edged sword influencing denitrification of Rhodobacter azotoformans and for nitrogen removal of aquaculture wastewater[J]. Bioresource technology, 2022(345):126495.
[9]	LIU Z B, ZHANG C J, WEI Q Y, et al. Temperature and salinity drive comammox community composition in mangrove ecosystems across southeastern China[J]. Science of the total environment, 2020(742):140456.
[10]	HU Z Y, HANS J C T W, THEO V A, et al. Nitric oxide-dependent anaerobic ammonium oxidation[J]. Nature communications, 2019, 10(1):1244. doi: 10.1038/s41467-019-09268-w pmid: 30886150
[11]	吴军伟, 赵俊松, 钟先锦. 底泥污染物及其原位修复技术研究进展[J]. 中国多媒体与网络教学学报(中旬刊), 2018(4):106-107.
[12]	JIA B C, LI Y F, ZI X Y, et al. Nutrient enrichment drives the sediment microbial communities in Chinese mitten crab Eriocheir sinensis culture[J]. Environmental research, 2023, 223:115281.
[13]	朱佳睿. 池塘工程化循环水养殖模式中底泥有机负荷和菌群结构的分析[D]. 南京: 南京农业大学, 2020.
[14]	DANUTA D, KRYSTYNA M, JAKUB M, et al. Fish pond sediment from aquaculture production-current practices and the potential for nutrient recovery: a review[J]. International agrophysics, 2020, 34(1):33-41.
[15]	GARG S K, BHATNAGAR A, NARULA N. Application of Azotobacter enhances pond productivity and fish biomass in still water ponds[J]. Aquaculture international, 1998, 6(3):219-231.
[16]	ZALA S, JEAN-CLAUDE W, CARLOS A E, et al. Microbial diversity across compartments in an aquaponic system and its connection to the nitrogen cycle[J]. Science of the total environment, 2022, 852:158426.
[17]	尧诚. 近海养殖区沉积物固氮及氧化亚氮源汇过程对季节性低氧的响应探究[D]. 烟台: 中国科学院大学(中国科学院烟台海岸带研究所), 2023.
[18]	叶琳琳, 张民, 孔繁翔, 等. 水生生态系统蓝藻固氮作用研究进展与展望[J]. 湖泊科学, 2014, 26(1):9-18.
[19]	YANG X Q, WU Y J, SHU L F, et al. Unraveling the important role of comammox Nitrospira to nitrification in the coastal aquaculture system[J]. Frontiers in microbiology, 2024,15:1355859.
[20]	YAO S, JIANG Y Y, WANG S Y, et al. Biogeographic distribution of comammox bacteria in diverse terrestrial habitats[J]. Science of the total environment, 2020, 717:137257.
[21]	EMILIE S, JACKSON M T, LAURA A H, et al. High functional diversity among Nitrospira populations that dominate rotating biological contactor microbial communities in a municipal wastewater treatment plant[J]. The ISME journal, 2020, 14(7):1857-1872.
[22]	HOU D W, ZHOU R J, ZENG S Z, et al. Stochastic processes shape the bacterial community assembly in shrimp cultural pond sediments[J]. Applied microbiology and biotechnology, 2021, 105(12):5013-5022. doi: 10.1007/s00253-021-11378-9 pmid: 34097120
[23]	YANG Y Y, LI N N, ZHAO Q, et al. Ammonia-oxidizing archaea and bacteria in water columns and sediments of a highly eutrophic plateau freshwater lake[J]. Environmental science and pollution research, 2016, 23(15):15358-15369.
[24]	LU S M, LIU X G, MA Z J, et al. Vertical segregation and phylogenetic characterization of ammonia-oxidizing bacteria and archaea in the sediment of a freshwater aquaculture pond[J]. Frontiers in microbiology, 2016,6:1786-1797.
[25]	ZHOU Z J, LI H, SONG C L, et al. Prevalence of ammonia-oxidizing bacteria over ammonia-oxidizing archaea in sediments as related to nutrient loading in Chinese aquaculture ponds[J]. Journal of soils and sediments, 2017,17:1928-1938.
[26]	ATTARD E, POLY F, COMMEAUX C, et al. Shifts between nitrospira- and nitrobacter-like nitrite oxidizers underlie the response of soil potential nitrite oxidation to changes in tillage practices[J]. Environmental microbiology, 2010, 12(2):315-326. doi: 10.1111/j.1462-2920.2009.02070.x pmid: 19807778
[27]	SUN X, CLAUDIA F, EMILIO G R, et al. Microbial niche differentiation explains nitrite oxidation in marine oxygen minimum zones[J]. The ISME journal, 2021, 15(5):1317-1329.
[28]	LIU Q, LEI X J, LI J N, et al. Microbial communities and nitrogen cycling in Litopenaeus vannamei and Mercenaria mercenaria polyculture ponds[J]. Aquaculture reports, 2023,33:101769.
[29]	MURPHY A E, ANDERSON I C, SMYTH A R, et al. Microbial nitrogen processing in hard clam (Mercenaria mercenaria) aquaculture sediments: the relative importance of denitrification and dissimilatory nitrate reduction to ammonium (DNRA)[J]. Limnology and oceanography, 2016, 61(5):1589-1604.
[30]	王谨. 典型淡水养殖池塘厌氧氨氧化细菌的菌群结构、多样性和定量研究[D]. 青岛: 中国海洋大学, 2013.
[31]	LI M, GU J D. The diversity and distribution of anammox bacteria in the marine aquaculture zones[J]. Applied microbiology and biotechnology, 2016, 100(20):8943-8953. doi: 10.1007/s00253-016-7690-6 pmid: 27368740
[32]	CHEN D Q, TIAN C, YUAN H Q, et al. Nitrogen removal performance and microbial community structure of IMTA ponds (Apostistius japonicus-Penaeus japonicus-Ulva)[J]. Microbial ecology, 2024,87:82.
[33]	RAGHOEBARSING A A, POL A, PAS-SCHOONEN K T V D, et al. A microbial consortium couples anaerobic methane oxidation to denitrification[J]. Nature, 2006, 440(7086):918-921.
[34]	陈佳, 赵璐峰, 戴然欣, 等. 稻鱼共生系统的土壤产甲烷和甲烷氧化微生物群落[J]. 生态学杂志, 2023, 42(12):2961-2971.
[35]	PREENA P G, REJISH K V J, SINGH I S B. Nitrification and denitrification in recirculating aquaculture systems: the processes and players[J]. Reviews in aquaculture, 2021, 13(4):2053-2075.
[36]	HHUANG S, PETER R J. Isolation and characterization of an ammonium-oxidizing iron reducer: Acidimicrobiaceae sp. A6[J]. PloS one, 2018, 13(4):e0194007.
[37]	HHUANG S, PETER R J. Characterization of incubation experiments and development of an enrichment culture capable of ammonium oxidation under iron-reducing conditions[J]. Biogeosciences, 2015, 12(3):769-779.
[38]	QIN Y B, CHEN Z H, DING B J, et al. Impact of sand mining on the carbon sequestration and nitrogen removal ability of soil in the riparian area of Lijiang River, China[J]. Environmental pollution, 2020, 261:114220.
[39]	ASHAR A, MUNEEB M, BHUTTA Z A, et al. Chapter 5 - Diversity of ammonia-oxidizing bacteria[M]. Amsterdam: Elsevier Inc.,2022:83-91.
[40]	LU S M, LIAO M J, XIE C X, et al. Seasonal dynamics of ammonia-oxidizing microorganisms in freshwater aquaculture ponds[J]. Annals of microbiology, 2015,65:651-657.
[41]	ALAWI M, OFF S, KAYA M, et al. Temperature influences the population structure of nitrite-oxidizing bacteria in activated sludge[J]. Environmental microbiology reports, 2009, 1(3):184-190. doi: 10.1111/j.1758-2229.2009.00029.x pmid: 23765792
[42]	ZHOU R F, LI Y Y, XIAO S W, et al. Ecophysiological characterization of a nitrite-oxidizing bacterial culture from a freshwater aquaculture pond[J]. Biotechnology & biotechnological equipment, 2022, 36(1):891-901.
[43]	DIEN L D, SANG N V, FAGGOTTER S J, et al. Seasonal nutrient cycling in integrated rice-shrimp ponds[J]. Marine pollution bulletin, 2019,149:110647.
[44]	WURTS W A, DURBOROW R M, et al. Interactions of pH, carbon dioxide, alkalinity and hardness in fish ponds[J]. SRAC, 1992,464:1-4.
[45]	SONG T, ZHANG X L, LI J, et al. A review of research progress of heterotrophic nitrification and aerobic denitrification microorganisms (HNADMs)[J]. Science of the total environment, 2021,801:149319.
[46]	HANFENBRADL D, KELLER M, DIRMEIER R, et al. Ferroglobus placidus gen. nov., sp. nov., a novel hyperthermophilic archaeum that oxidizes Fe²⁺ at neutral pH under anoxic conditions[J]. Archives of microbiology, 1996, 166:308-314.
[47]	张宁博, 李祥, 黄勇. pH值对零价铁自养反硝化过程的影响[J]. 环境科学, 2017, 38(12):5208-5214.
[48]	NIELSEN J L, NIELSEN P H. Microbial nitrate-dependent oxidation of ferrous iron in activated sludge[J]. Environmental science & technology (Washington), 1998, 32(22):3556-3561.
[49]	YANG X R, LI H, NIE S A, et al. Potential contribution of anammox to nitrogen loss from paddy soils in Southern China[J]. Applied and environmental microbiology, 2015, 81(3):938-947.
[50]	HU H W, MACDONALD C A, TRIVEDI P, et al. Water addition regulates the metabolic activity of ammonia oxidizers responding to environmental perturbations in dry subhumid ecosystems[J]. Environmental microbiology, 2015, 17(2):444-461.
[51]	LI X W, BAI D, DENG Q H, et al. DNRA was limited by sulfide and nrfA abundance in sediments of Xiamen Bay where heterotrophic sulfide-producing genus (Pelobacter) prevailed among DNRA bacteria[J]. Journal of soils and sediments, 2021, 21(10):3493-3504.
[52]	ONLEY J R, AHSAN S H, SANFORD R A, et al. Denitrification by Anaeromyxobacter dehalogenans, a common soil bacterium lacking the nitrite reductase genes nirS and nirK[J]. Applied and environmental microbiology, 2018, 84(4):e01985-17.
[53]	杨柳燕, 王楚楚, 孙旭, 等. 淡水湖泊微生物硝化反硝化过程与影响因素研究[J]. 水资源保护, 2016, 32(1):12-22.
[54]	徐慧敏, 陈曦, 孟顺龙, 等. 鱼菜共生系统中的微生物群落研究进展与展望[J]. 渔业科学进展, 2025, 46(2):15-26.
[55]	DING B J, CHEN Z H, LI Z K, et al. Nitrogen loss through anaerobic ammonium oxidation coupled to Iron reduction from ecosystem habitats in the Taihu estuary region[J]. Science of the total environment, 2019,662:600-606.