Relative contributions of ammonia-oxidizing microorganisms to nitrification potential in sediments from Bohai Sea and South Yellow Sea

Li Mingyue; Zhen Yu; Li Siqi; Mi Tiezhu; He Hui

doi:10.12284/hyxb2023018

Volume 45 Issue 1

Jan. 2023

Turn off MathJax

Article Contents

Article Navigation > Haiyang Xuebao > 2023 > 45(1): 89-101

Li Mingyue，Zhen Yu，Li Siqi, et al. Relative contributions of ammonia-oxidizing microorganisms to nitrification potential in sediments from Bohai Sea and South Yellow Sea[J]. Haiyang Xuebao，2023, 45(1)：89–101 doi: 10.12284/hyxb2023018

Citation:

PDF( 2479 KB)

Relative contributions of ammonia-oxidizing microorganisms to nitrification potential in sediments from Bohai Sea and South Yellow Sea

doi: 10.12284/hyxb2023018

Li Mingyue^1
,,
Zhen Yu^{2, 3
,
,},
Li Siqi^{2, 3, 4},
Mi Tiezhu^{2, 3},
He Hui⁴

1.
School of Resources and Environmental Engineering, Shandong University of Technology, Zibo 255049, China
2.
Marine Ecology and Environmental Science Laboratory, Pilot National Laboratory for Marine science and Technology (Qingdao), Qingdao 266071, China
3.
Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, China
4.
College of Marine Life Science, Ocean University of China, Qingdao 266003, China

Received Date: 2022-05-18
Rev Recd Date: 2022-08-26

Available Online: 2022-09-08

Publish Date: 2023-01-09

Abstract

Abstract

Nitrification is a pivotal process in the marine nitrogen cycle. Ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) drive the ammonia oxidation, which is the first and rate-limiting step in nitrification, and their relative contributions to nitrification are ones of the most important topics related to the nitrogen cycle in ocean. In this study, surface sediment samples at 20 sites from Bohai Sea and South Yellow Sea were collected in April and May, 2019. The relative contributions of AOA and AOB to nitrification potential were studied in the microcosmic experiment. The results showed that the potential nitrification rates (PNRs, in terms of nitrogen) ranged from 0.004 6 μmol/(g·d) to 0.283 1 μmol/(g·d), in which potential nitrification rate of AOA and AOB ranged from 0.004 3 μmol/(g·d) to 0.274 3 μmol/(g·d) and 0.000 4 μmol/(g·d) to 0.056 0 μmol/(g·d), respectively. AOA was the main contributor to the nitrification therein, whose contribution rate was 59.79%−97.95% in Bohai Sea and 18.47%−94.26% in South Yellow Sea, respectively. The potential nitrification rates in surface sediments from Bohai Sea were significantly higher than those from South Yellow Sea. Besides, salinity was a key environmental factor for potential nitrification rates, and high ${{\rm {NO}}_3^-} $ concentration might indicated high nitrification potential. It was speculated that AOA played a more vital role than AOB in estuarine and coastal areas, and nitrification potential decreased from estuarine and near-shore region to the open sea. This study provides evidences for further evaluation of nitrogen cycle in coastal areas.
- sediment,
- ammonia-oxidizing archaea,
- ammonia-oxidizing bacteria,
- nitrification,
- potential nitrification rates

FullText(HTML)

References(43)

References

[1]	Seitzinger S. Nitrogen cycle: Out of reach[J]. Nature, 2008, 452(7184): 162−163. doi: 10.1038/452162a
[2]	Jensen K, Sloth N P, Risgaard-Petersen N, et al. Estimation of nitrification and denitrification from microprofiles of oxygen and nitrate in model sediment systems[J]. Applied and Environmental Microbiology, 1994, 60(6): 2094−2100. doi: 10.1128/aem.60.6.2094-2100.1994
[3]	徐颢铭, 宋国栋, 刘素美, 等. 基于次溴酸钠氧化−氨基磺酸还原测定沉积物¹⁵N加富培养样品中的 ${^{15}{\rm {NH}}_4^+}$的方法探索[J]. 海洋学报, 2022, 44(1): 147−154. Xu Haoming, Song Guodong, Liu Sumei, et al. A sodium hypobromite oxidation-sulfamic acid reduction method for determination of ${^{15}{\rm {NH}}_4^+} $ in ¹⁵N enrichment sediment slurry incubation samples[J]. Haiyang Xuebao, 2022, 44(1): 147−154.
[4]	Kowalchuk G A, Stephen J R. Ammonia-oxidizing bacteria: a model for molecular microbial ecology[J]. Annual Review of Microbiology, 2001, 55: 485−529. doi: 10.1146/annurev.micro.55.1.485
[5]	Norton J M, Stark J M. Regulation and measurement of nitrification in terrestrial systems[J]. Methods in Enzymology, 2011, 486: 343−368.
[6]	李如忠, 阙凤翔, 熊鸿斌, 等. 巢湖十五里河河床地貌单元沉积物硝化速率及污染特征[J]. 环境科学, 2019, 40(1): 211−218. Li Ruzhong, Que Fengxiang, Xiong Hongbin, et al. Nitrification rates and pollution characteristics of sediments with different geomorphic features in the Shiwuli Stream, Chaohu Lake Basin[J]. Environmental Science, 2019, 40(1): 211−218.
[7]	Venter J C, Remington K, Heidelberg J F, et al. Environmental genome shotgun sequencing of the Sargasso Sea[J]. Science, 2004, 304(5667): 66−74. doi: 10.1126/science.1093857
[8]	Treusch A H, Leininger S, Kletzin A, et al. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling[J]. Environmental Microbiology, 2005, 7(12): 1985−1995. doi: 10.1111/j.1462-2920.2005.00906.x
[9]	Könneke M, Bernhard A E, de la Torre J R, et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon[J]. Nature, 2005, 437(7058): 543−546. doi: 10.1038/nature03911
[10]	Hou Jie, Song Chunlei, Cao Xiuyun, et al. Shifts between ammonia-oxidizing bacteria and archaea in relation to nitrification potential across trophic gradients in two large Chinese lakes (Lake Taihu and Lake Chaohu)[J]. Water Research, 2013, 47(7): 2285−2296. doi: 10.1016/j.watres.2013.01.042
[11]	Sims A, Horton J, Gajaraj S, et al. Temporal and spatial distributions of ammonia-oxidizing archaea and bacteria and their ratio as an indicator of oligotrophic conditions in natural wetlands[J]. Water Research, 2012, 46(13): 4121−4129. doi: 10.1016/j.watres.2012.05.007
[12]	Ouyang Yang, Norton J M, Stark J M. Ammonium availability and temperature control contributions of ammonia oxidizing bacteria and archaea to nitrification in an agricultural soil[J]. Soil Biology and Biochemistry, 2017, 113: 161−172. doi: 10.1016/j.soilbio.2017.06.010
[13]	Islam G M, Vi P, Gilbride K A. Functional relationship between ammonia-oxidizing bacteria and ammonia-oxidizing archaea populations in the secondary treatment system of a full-scale municipal wastewater treatment plant[J]. Journal of Environmental Sciences, 2019, 86: 120−130. doi: 10.1016/j.jes.2019.04.031
[14]	Caffrey J M, Bano N, Kalanetra K, et al. Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia[J]. The ISME Journal, 2007, 1(7): 660−662. doi: 10.1038/ismej.2007.79
[15]	Bernhard A E, Landry Z C, Blevins A, et al. Abundance of ammonia-oxidizing Archaea and Bacteria along an estuarine salinity gradient in relation to potential nitrification rates[J]. Applied and Environmental Microbiology, 2010, 76(4): 1285−1289. doi: 10.1128/AEM.02018-09
[16]	Zheng Yanling, Hou Lijun, Newell S, et al. Community dynamics and activity of ammonia-oxidizing prokaryotes in intertidal sediments of the Yangtze Estuary[J]. Applied and Environmental Microbiology, 2014, 80(1): 408−419. doi: 10.1128/AEM.03035-13
[17]	Christman G D, Cottrell M T, Popp B N, et al. Abundance, diversity, and activity of ammonia-oxidizing prokaryotes in the coastal Arctic Ocean in summer and winter[J]. Applied and Environmental Microbiology, 2011, 77(6): 2026−2034. doi: 10.1128/AEM.01907-10
[18]	贺惠, 甄毓, 米铁柱, 等. 乳山湾邻近海域沉积物中好氧氨氧化微生物分布特征[J]. 环境科学, 2015, 36(11): 4068−4073. He Hui, Zhen Yu, Mi Tiezhu, et al. Distribution of aerobic ammonia-oxidizing microorganisms in sediments from adjacent waters of Rushan Bay[J]. Environmental Science, 2015, 36(11): 4068−4073.
[19]	He Hui, Zhen Yu, Mi Tiezhu, et al. Ammonia-oxidizing archaea and bacteria differentially contribute to ammonia oxidation in sediments from adjacent waters of Rushan Bay, China[J]. Frontiers in Microbiology, 2018, 9: 116. doi: 10.3389/fmicb.2018.00116
[20]	Prosser J I, Hink L, Gubry-Rangin C, et al. Nitrous oxide production by ammonia oxidizers: physiological diversity, niche differentiation and potential mitigation strategies[J]. Global Change Biology, 2020, 26(1): 103−118. doi: 10.1111/gcb.14877
[21]	He Hui, Zhen Yu, Mi Tiezhu, et al. Seasonal and spatial distribution of ammonia-oxidizing microorganism communities in surface sediments from the East China Sea[J]. Acta Oceanologica Sinica, 2015, 34(8): 83−92. doi: 10.1007/s13131-015-0710-z
[22]	Jia Zhongjun, Conrad R. Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil[J]. Environmental Microbiology, 2009, 11(7): 1658−1671. doi: 10.1111/j.1462-2920.2009.01891.x
[23]	Bernhard A E, Tucker J, Giblin A E, et al. Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient[J]. Environmental Microbiology, 2007, 9(6): 1439−1447. doi: 10.1111/j.1462-2920.2007.01260.x
[24]	Chang Yongkai, Fan Jingfeng, Su Jie, et al. Spatial abundance, diversity, and activity of ammonia-oxidizing bacteria in coastal sediments of the Liaohe Estuary[J]. Current Microbiology, 2017, 74(5): 632−640. doi: 10.1007/s00284-017-1226-x
[25]	Alcamán-Arias M E, Cifuentes-Anticevic J, Díez B, et al. Surface ammonia-oxidizer abundance during the late summer in the West Antarctic coastal system[J]. Frontiers in Microbiology, 2022, 13: 821902. doi: 10.3389/fmicb.2022.821902
[26]	杨韦玲, 胡佳杰, 胡宝兰. 抑制剂在氨氧化微生物研究中的应用[J]. 微生物学报, 2018, 58(10): 1722−1731. Yang Weiling, Hu Jiajie, Hu Baolan. Application of inhibitors in research of ammonia oxidizing microorganisms[J]. Acta Microbiologica Sinica, 2018, 58(10): 1722−1731.
[27]	Tatti E, Duff A M, Kostrytsia A, et al. Potential nitrification activity reflects ammonia oxidizing bacteria but not archaea activity across a soil-sediment gradient[J]. Estuarine, Coastal and Shelf Science, 2022, 264: 107666. doi: 10.1016/j.ecss.2021.107666
[28]	Ning Xiuren, Lin Chuanlan, Su Jilan, et al. Long-term environmental changes and the responses of the ecosystems in the Bohai Sea during 1960−1996[J]. Deep-Sea Research Part II: Topical Studies in Oceanography, 2010, 57(11/12): 1079−1091.
[29]	Liu S M, Zhang J, Chen S Z, et al. Inventory of nutrient compounds in the Yellow Sea[J]. Continental Shelf Research, 2003, 23(11−13): 1161−1174. doi: 10.1016/S0278-4343(03)00089-X
[30]	Li Xinyu, Chen H T, Jiang Xueyan, et al. Impacts of human activities on nutrient transport in the Yellow River: the role of the Water-Sediment Regulation Scheme[J]. Science of the Total Environment, 2017, 592: 161−170. doi: 10.1016/j.scitotenv.2017.03.098
[31]	de Souza M P, Chu D, Zhao M, et al. Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard[J]. Plant Physiology, 1999, 119(2): 565−574. doi: 10.1104/pp.119.2.565
[32]	Zheng Yanling, Hou Lijun, Liu Min, et al. Diversity, abundance, and activity of ammonia-oxidizing bacteria and archaea in Chongming eastern intertidal sediments[J]. Applied Microbiology and Biotechnology, 2013, 97(18): 8351−8363. doi: 10.1007/s00253-012-4512-3
[33]	Dang Chenyuan, Liu Wen, Lin Yaxuan, et al. Dominant role of ammonia-oxidizing bacteria in nitrification due to ammonia accumulation in sediments of Danjiangkou reservoir, China[J]. Applied Microbiology and Biotechnology, 2018, 102(7): 3399−3410. doi: 10.1007/s00253-018-8865-0
[34]	Henriksen K, Hansen J I, Blackburn T H. Rates of nitrification, distribution of nitrifying bacteria, and nitrate fluxes in different types of sediment from Danish waters[J]. Marine Biology, 1981, 61(4): 299−304. doi: 10.1007/BF00401569
[35]	Kemp W M, Sampou P, Caffrey J, et al. Ammonium recycling versus denitrification in Chesapeake Bay sediments[J]. Limnology and Oceanography, 1990, 35(7): 1545−1563. doi: 10.4319/lo.1990.35.7.1545
[36]	Tourna M, Stieglmeier M, Spang A, et al. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(20): 8420−8425. doi: 10.1073/pnas.1013488108
[37]	Tu Renjie, Jin Wenbiao, Han Songfang, et al. Rapid enrichment and ammonia oxidation performance of ammonia-oxidizing archaea from an urban polluted river of China[J]. Environmental Pollution, 2019, 255: 113258. doi: 10.1016/j.envpol.2019.113258
[38]	Wang Jianhua, He Yan, Zhu Jin, et al. Screening and optimizing of inhibitors for ammonia-oxidizing bacteria in sediments of malodorous river[J]. Applied Microbiology and Biotechnology, 2017, 101(15): 6193−6203. doi: 10.1007/s00253-017-8318-1
[39]	Boatman C D, Murray J W. Modeling exchangeable ${{\rm {NH}}_4^+} $ adsorption in marine sediments: Process and controls of adsorption[J]. Limnology and Oceanography, 1982, 27(1): 99−110. doi: 10.4319/lo.1982.27.1.0099
[40]	Rysgaard S, Thastum P, Dalsgaard T, et al. Effects of salinity on ${{\rm {NH}}_4^+} $ adsorption capacity, nitrification, and denitrification in Danish estuarine sediments[J]. Estuaries, 1999, 22(1): 21−30. doi: 10.2307/1352923
[41]	Molina V, Dorador C, Fernández C, et al. The activity of nitrifying microorganisms in a high-altitude Andean wetland[J]. FEMS Microbiology Ecology, 2018, 94(6): fiy062.
[42]	于少兰, 乔延路, 韩彦琼, 等. 好氧氨氧化微生物系统发育及生理生态学差异[J]. 微生物学通报, 2015, 42(12): 2457−2465. Yu Shaolan, Qiao Yanlu, Han Yanqiong, et al. Differences between ammonia-oxidizing microorganisms in phylogeny and physiological ecology[J]. Microbiology China, 2015, 42(12): 2457−2465.
[43]	Schleper C, Jurgens G, Jonuscheit M. Genomic studies of uncultivated archaea[J]. Nature Reviews Microbiology, 2005, 3(6): 479−488. doi: 10.1038/nrmicro1159