Comparative assessment of nitrogen fixation rate by 15N2 tracer assays in the South China Sea

Danyang Li Minfang Zheng Yusheng Qiu Limin Lai Nengwang Chen Hongmei Jing Run Zhang Min Chen

Danyang Li, Minfang Zheng, Yusheng Qiu, Limin Lai, Nengwang Chen, Hongmei Jing, Run Zhang, Min Chen. Comparative assessment of nitrogen fixation rate by 15N2 tracer assays in the South China Sea[J]. Acta Oceanologica Sinica, 2023, 42(1): 75-82. doi: 10.1007/s13131-022-2092-3
Citation: Danyang Li, Minfang Zheng, Yusheng Qiu, Limin Lai, Nengwang Chen, Hongmei Jing, Run Zhang, Min Chen. Comparative assessment of nitrogen fixation rate by 15N2 tracer assays in the South China Sea[J]. Acta Oceanologica Sinica, 2023, 42(1): 75-82. doi: 10.1007/s13131-022-2092-3

doi: 10.1007/s13131-022-2092-3

Comparative assessment of nitrogen fixation rate by 15N2 tracer assays in the South China Sea

Funds: The National Natural Science Foundation of China under contract Nos 42076042 and 41721005; the Fund of Ministry of Science and Technology of China under contract No. 2017FY201403; the Fund of China Ocean Mineral Resources R&D Association under contract No. DY135-13-E2-03.
More Information
    • 关键词:
    •  / 
    •  / 
    •  
  • Figure  1.  Sampling locations in the South China Sea (SCS): a. stations in the open areas of the SCS from 2013 to 2017 (“A-”, “K-”, “C-”, “G-” and “D-” indicate cruises in August 2013, July 2014, March 2017, July 2017 and June 2018, “□” indicates the sampling stations of nifH in March 2017); b. stations in the Daya Bay (prefixed with “E-”, July 2015, December 2015, April 2016 and January 2018).

    Figure  2.  The range of NFRs in the open area of the SCS (the top margins and the bottom margins of the boxes represent the third quartile (Q3) and the first quartile (Q1) respectively. The upper limit and the lower limit were calculated as follows: upper limit = Q3 + (Q3 − Q1) × 1.5, lower limit = Q1 − (Q3 − Q1) × 1.5. Values larger than the upper limit or less than the lower limit were defined as outliers. The solid lines in the boxes represent the medians, and the dotted lines represent the average values).

    Figure  3.  Surface distribution of NFRs (nmol/(L·d)) in the open waters of the South China Sea (“A-”, “K-”, “C-”, “G-” and “D-” indicate cruises in August 2013, July 2014, March 2017, July 2017 and June 2018, respectively).

    Figure  4.  Diazotrophic composition derived from nifH gene sequences in the open waters of South China Sea (March 2017). UCYN: unicellular cyanobacterium group; DDA: diatom diazotroph associations.

    Figure  5.  The relationship between N2 fixation rates (NFRs) measured by the original bubble (B) method and the 15N2-enriched seawater (S) methods: the unit of NFRs observed in this study and in Großkopf et al. (2012) is nmol/(L·d) , and the unit of NFRs (depth-integrated NFRs) in Wilson et al. (2012) is µmol/(m2·d). To improve the visibility of Fig. 5, the unit of NFRs in the Daya Bay (DB) are converted to nmol/(L·d).

    Figure  6.  The correlation between N2 fixation rates measured by the original bubble (B) and modified bubble (MB) methods: a. the Daya Bay, January 2018; b. the northeastern SCS, June 2018.

  • Bombar D, Dippner J W, Doan H N, et al. 2010. Sources of new nitrogen in the Vietnamese upwelling region of the South China Sea. Journal of Geophysical Research: Oceans, 115(C6): C06018
    Bombar D, Paerl R W, Anderson R, et al. 2018. Filtration via conventional glass fiber filters in 15N2 tracer assays fails to capture all nitrogen-fixing prokaryotes. Frontiers in Marine Science, 5: 6. doi: 10.3389/fmars.2018.00006
    Böttjer D, Dore J E, Karl D M, et al. 2017. Temporal variability of nitrogen fixation and particulate nitrogen export at Station ALOHA. Limnology and Oceanography, 62(1): 200–216. doi: 10.1002/lno.10386
    Casciotti K L. 2016. Nitrogen and oxygen isotopic studies of the marine nitrogen cycle. Annual Review of Marine Science, 8: 379–407. doi: 10.1146/annurev-marine-010213-135052
    Chang B X, Jayakumar A, Widner B, et al. 2019. Low rates of dinitrogen fixation in the eastern tropical South Pacific. Limnology and Oceanography, 64(5): 1913–1923. doi: 10.1002/lno.11159
    Chen Yuh-Ling Lee, Chen Houng-Yung, Lin Yen-Huei, et al. 2014. The relative contributions of unicellular and filamentous diazotrophs to N2 fixation in the South China Sea and the upstream Kuroshio. Deep-Sea Research Part I: Oceanographic Research Papers, 85: 56–71. doi: 10.1016/j.dsr.2013.11.006
    Chen Yuh-Ling Lee, Chen Houng-Yung, Tuo Sing-How, et al. 2008. Seasonal dynamics of new production from Trichodesmium N2 fixation and nitrate uptake in the upstream Kuroshio and South China Sea Basin. Limnology and Oceanography, 53(5): 1705–1721. doi: 10.4319/lo.2008.53.5.1705
    Chen Shengbao, Zhang Run, Chen Nengwang, et al. 2018. On the introduction of 15N2 tracer in marine N2 fixation rate assay. Haiyang Xuebao (in Chinese), 40(10): 42–50
    Codispoti L A. 2007. An oceanic fixed nitrogen sink exceeding 400 Tg N a-1 vs the concept of homeostasis in the fixed-nitrogen inventory. Biogeosciences, 4(2): 233–253. doi: 10.5194/bg-4-233-2007
    Dabundo R, Lehmann M F, Treibergs L, et al. 2014. The contamination of commercial 15N2 gas stocks with 15N–labeled nitrate and ammonium and consequences for nitrogen fixation measurements. PLoS ONE, 9(10): e110335. doi: 10.1371/journal.pone.0110335
    Ding Changling, Sun Jun, Xue Bing. 2016. Winter and summer diazotrophic cyanobacteria in the western South China Sea. Haiyang Xuebao (in Chinese), 38(4): 84–94
    Dugdale R C, Menzel D W, Ryther J H. 1961. Nitrogen fixation in the Sargasso Sea. Deep-Sea Research, 7(4): 297–300. doi: 10.1016/0146-6313(61)90051-X
    Gradoville M R, Bombar D, Crump B C, et al. 2017. Diversity and activity of nitrogen-fixing communities across ocean basins. Limnology and Oceanography, 62(5): 1895–1909. doi: 10.1002/lno.10542
    Grosse J, Bombar D, Doan H N, et al. 2010. The Mekong River plume fuels nitrogen fixation and determines phytoplankton species distribution in the South China Sea during low and high discharge season. Limnology and Oceanography, 55(4): 1668–1680. doi: 10.4319/lo.2010.55.4.1668
    Großkopf T, Mohr W, Baustian T, et al. 2012. Doubling of marine dinitrogen-fixation rates based on direct measurements. Nature, 488(7411): 361–364. doi: 10.1038/nature11338
    Gruber N, Sarmiento J L. 1997. Global patterns of marine nitrogen fixation and denitrification. Global Biogeochemical Cycles, 11(2): 235–266. doi: 10.1029/97GB00077
    Kim T W, Lee K, Duce R, et al. 2014. Impact of atmospheric nitrogen deposition on phytoplankton productivity in the South China Sea. Geophysical Research Letters, 41(9): 3156–3162. doi: 10.1002/2014GL059665
    Klawonn I, Lavik G, Böning P, et al. 2015. Simple approach for the preparation of 15-15N2-enriched water for nitrogen fixation assessments: evaluation, application and recommendations. Frontiers in Microbiology, 6: 769
    Kong Liangliang, Jing Hongmei, Kataoka T, et al. 2011. Phylogenetic diversity and spatio-temporal distribution of nitrogenase genes (nifH) in the northern South China Sea. Aquatic Microbial Ecology, 65(1): 15–27. doi: 10.3354/ame01531
    Li Danyang, Liu Jiaxing, Zhang Run, et al. 2019. N2 fixation impacted by carbon fixation via dissolved organic carbon in the changing Daya Bay, South China Sea. Science of the Total Environment, 674: 592–602. doi: 10.1016/j.scitotenv.2019.04.176
    Li Danyang, Zhang Run. 2018. Research progresses in biological nitrogen fixation in the South China Sea. Journal of Xiamen University: Natural Science (in Chinese), 57(6): 760–767
    Lin Feng. 2013. Spatial and temporal variations of biological N2 fixation rate and its controlling factors in the China marginal seas (in Chinese) [dissertation]. Xiamen: Xiamen University
    Liu Jiaxing, Zhou Linbin, Li Gang, et al. 2016. Nitrogen fixation and its contribution of nitrogen to primary production in the surface waters of the northeastern South China Sea during October 2014. Journal of Tropical Oceanography (in Chinese), 35(5): 38–47
    Liu Jiaxing, Zhou Linbin, Li Jiajun, et al. 2020. Effect of mesoscale eddies on diazotroph community structure and nitrogen fixation rates in the South China Sea. Regional Studies in Marine Science, 35: 101106. doi: 10.1016/j.rsma.2020.101106
    Mohr W, Großkopf T, Wallace D W R, et al. 2010. Methodological underestimation of oceanic nitrogen fixation Rates. PLoS ONE, 5(9): e12583. doi: 10.1371/journal.pone.0012583
    Montoya J P, Voss M, Kahler P, et al. 1996. A simple, high-precision, high-sensitivity tracer assay for N2 fixation. Applied and Environmental Microbiology, 62(3): 986–993. doi: 10.1128/aem.62.3.986-993.1996
    Osorio-Santos K, Pietrasiak N, Bohunická M, et al. 2014. Seven new species of Oculatella (Pseudanabaenales, Cyanobacteria): taxonomically recognizing cryptic diversification. European Journal of Phycology, 49(4): 450–470. doi: 10.1080/09670262.2014.976843
    Ren Haojia, Chen Yi-Chi, Wang Xingchen T, et al. 2017. 21st-century rise in anthropogenic nitrogen deposition on a remote coral reef. Science, 356(6339): 749–752. doi: 10.1126/science.aal3869
    Schloss P D. 2009. A high-throughput DNA sequence aligner for microbial ecology studies. PLoS ONE, 4(12): e8230. doi: 10.1371/journal.pone.0008230
    Shiozaki T, Chen Yuh-Ling Lee, Lin Yen-Huei, et al. 2014. Seasonal variations of unicellular diazotroph groups A and B, and Trichodesmium in the northern South China Sea and neighboring upstream Kuroshio Current. Continental Shelf Research, 80: 20–31. doi: 10.1016/j.csr.2014.02.015
    Van Wambeke F, Gimenez A, Duhamel S, et al. 2018. Dynamics and controls of heterotrophic prokaryotic production in the western tropical South Pacific Ocean: links with diazotrophic and photosynthetic activity. Biogeosciences, 15(9): 2669–2689. doi: 10.5194/bg-15-2669-2018
    Voss M, Bombar D, Loick N, et al. 2006. Riverine influence on nitrogen fixation in the upwelling region off Vietnam, South China Sea. Geophysical Research Letters, 33(7): L07604
    Wannicke N, Benavides M, Dalsgaard T, et al. 2018. New perspectives on nitrogen fixation measurements using 15N2 gas. Frontiers in Marine Science, 5: 120. doi: 10.3389/fmars.2018.00120
    Wen Zuozhu, Lin Wenfang, Shen Rong, et al. 2017. Nitrogen fixation in two coastal upwelling regions of the Taiwan Strait. Scientific Reports, 7(1): 17601. doi: 10.1038/s41598-017-18006-5
    White A E, Granger J, Selden C, et al. 2020. A critical review of the 15N2 tracer method to measure diazotrophic production in pelagic ecosystems. Limnology and Oceanography: Methods, 18(4): 129–147. doi: 10.1002/lom3.10353
    Wilson S T, Böttjer D, Church M J, et al. 2012. Comparative assessment of nitrogen fixation methodologies, conducted in the oligotrophic North Pacific Ocean. Applied and Environmental Microbiology, 78(18): 6516–6523. doi: 10.1128/AEM.01146-12
    Wong George T F, Tseng Chun-Mao, Wen Liang-Saw, et al. 2007. Nutrient dynamics and N-anomaly at the SEATS station. Deep-Sea Research Part II: Topical Studies in Oceanography, 54(14–15): 1528–1545
    Yang Jin-Yu Terence, Kao Shui-Ji, Dai Minhan, et al. 2017. Examining N cycling in the northern South China Sea from N isotopic signals in nitrate and particulate phases. Journal of Geophysical Research: Biogeosciences, 122(8): 2188–2136
    Zehr J P, Capone D G. 2020. Changing perspectives in marine nitrogen fixation. Science, 368(6492): eaay9514. doi: 10.1126/science.aay9514
    Zehr J P, Montoya J P, Jenkins B D, et al. 2007. Experiments linking nitrogenase gene expression to nitrogen fixation in the North Pacific subtropical gyre. Limnology and Oceanography, 52(1): 169–183. doi: 10.4319/lo.2007.52.1.0169
    Zehr J P, Turner P J. 2001. Nitrogen fixation: Nitrogenase genes and gene expression. Methods in Microbiology, 30: 271–286
    Zhang Run, Chen Min, Yang Qing, et al. 2015. Physical-biological coupling of N2 fixation in the northwestern South China Sea coastal upwelling during summer. Limnology and Oceanography, 60(4): 1411–1425. doi: 10.1002/lno.10111
    Zhang Run, Wang Xingchen T, Ren Haojia, et al. 2020. Dissolved organic nitrogen cycling in the South China Sea from an isotopic perspective. Global Biogeochemical Cycles, 34(12): e2020GB006551
    Zhang Run, Zhang Dongsheng, Chen Min, et al. 2019. N2 fixation rate and diazotroph community structure in the western tropical North Pacific Ocean. Acta Oceanologica Sinica, 38(12): 26–34. doi: 10.1007/s13131-019-1513-4
  • Li Danyang Supplement material.docx
  • 加载中
图(6)
计量
  • 文章访问数:  271
  • HTML全文浏览量:  97
  • PDF下载量:  15
  • 被引次数: 0
出版历程
  • 收稿日期:  2022-01-13
  • 录用日期:  2022-03-18
  • 网络出版日期:  2023-01-17
  • 刊出日期:  2023-01-25

目录

    /

    返回文章
    返回