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N2 fixation rate and diazotroph community structure in the western tropical North Pacific Ocean

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Abstract

In the present study, we report N2 fixation rate (15N isotope tracer assay) and the diazotroph community structure (using the molecular method) in the western tropical North Pacific Ocean (WTNP) (13°–20°N, 120°–160°E). Our independent evidence on the basis of both in situ N2 fixation activity and diazotroph community structure showed the dominance of unicellular N2 fixation over majority of the WTNP surface waters during the sampling periods. Moreover, a shift in the diazotrophic composition from unicellular cyanobacteria group B-dominated to Trichodesmium spp.-dominated toward the western boundary current (Kuroshio) was also observed in 2013. We hypothesize that nutrient availability may have played a major role in regulating the biogeography of N2 fixation. In surface waters, volumetric N2 fixation rate (calculated by nitrogen) ranged between 0.6 and 2.6 nmol/(L·d) and averaged (1.2±0.5) nmol/(L·d), with <10 μm size fraction contributed predominantly (88%±6%) to the total rate between 135°E and 160°E. Depth-integrated N2 fixation rate over the upper 200 m ranged between 150 μmol/(m2·d) and 480 μmol/(m2·d) (average (225±105) μmol/(m2·d). N2 fixation can account for 6.2%±3.7% of the depth-integrated primary production, suggesting that N2 fixation is a significant N source sustaining new and export production in the WTNP. The role of N2 fixation in biogeochemical cycling in this climate change-vulnerable region calls for further investigations.

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References

  • Bonnet S, Biegala I C, Dutrieux P, et al. 2009. Nitrogen fixation in the western equatorial Pacific: Rates, diazotrophic cyanobacterial size class distribution, and biogeochemical significance. Global Biogeochemical Cycles, 23(3): GB3012

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Brown M T, Landing W M, Measures C I. 2005. Dissolved and particulate Fe in the western and central North Pacific: Results from the 2002 IOC cruise. Geochemistry, Geophysics, Geosystems, 6(10): Q10001, doi: 10.1029/2004GC000893

    Article  Google Scholar 

  • Cabrera O, Villanoy C, Alabia I D, et al. 2015. Shifts in chlorophyll a off Eastern Luzon, Philippines, associated with the North Equatorial Current bifurcation latitude. Oceanography (Washington D.C.), 28(4): 46–53, doi: 10.5670/oceanog.2015.80

    Article  Google Scholar 

  • Capone D G, Zehr J P, Paerl H W, et al. 1997. Trichodesmium, a globally significant marine cyanobacterium. Science, 276(5316): 1221–1229, doi: 10.1126/science.276.5316.1221

    Article  Google Scholar 

  • Caporaso J G, Kuczynski J, Stombaugh J, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5): 335–336, doi: 10.1038/nmeth.f.303

    Article  Google Scholar 

  • Carpenter K E. 1998. An introduction to the oceanography, geology, biogeography, and fisheries of the tropical and subtropical western and central Pacific. In: Carpenter K E, Niem V H, eds. FAO Species Identification Guide for Fishery Purposes. Rome: The Living Marine Resources of the Western Central Pacific

    Google Scholar 

  • Carpenter E J, Harvey H R, Fry B, et al. 1997. Biogeochemical tracers of the marine cyanobacterium Trichodesmium. Deep Sea Research Part I: Oceanographic Research Papers, 44(1): 27–38

    Article  Google Scholar 

  • Carpenter E J, Montoya J P, Burns J, et al. 1999. Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean. Marine Ecology Progress Series, 185: 273–283, doi: 10.3354/meps185273

    Article  Google Scholar 

  • Chen Y L L, Chen H Y, Lin Y H, 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

    Article  Google Scholar 

  • Church M J, Björkman K M, Karl D M, et al. 2008. Regional distributions of nitrogenfixing bacteria in the Pacific Ocean. Limnology and Oceanography, 53(1): 63–77, doi: 10.4319/lo.2008. 53.1.0063

    Article  Google Scholar 

  • Church M J, Mahaffey C, Letelier R M, et al. 2009. Physical forcing of nitrogen fixation and diazotroph community structure in the North Pacific subtropical gyre. Global Biogeochemical Cycles, 23(2): GB2020

    Article  Google Scholar 

  • Clement A, DiNezio P. 2014. The tropical Pacific Ocean-back in the driver’s seat? Science, 343(6174): 976–978, doi: 10.1126/science. 1248115

    Article  Google Scholar 

  • Cravatte S, Delcroix T, Zhang Dongxiao, et al. 2009. Observed freshening and warming of the western Pacific Warm Pool. Climate Dynamics, 33(4): 565–589, doi: 10.1007/s00382-009-0526-7

    Article  Google Scholar 

  • Deutsch C, Sarmiento J L, Sigman D M, et al. 2007. Spatial coupling of nitrogen inputs and losses in the ocean. Nature, 445(7124): 163–167, doi: 10.1038/nature05392

    Article  Google Scholar 

  • Dyhrman S T, Chappell P D, Haley S T, et al. 2006. Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature, 439(7072): 68–71, doi: 10.1038/nature04203

    Article  Google Scholar 

  • Dyhrman S T, Haley S T. 2006. Phosphorus scavenging in the unicellular marine diazotroph Crocosphaera watsonii. Applied and Environmental Microbiology, 72(2): 1452–1458, doi: 10.1128/

    Article  Google Scholar 

  • Fish J A, Chai Benli, Wang Qiong, et al. 2013. FunGene: the functional gene pipeline and repository. Fronters in Microbiology, 4: 291, doi: 10.3389/fmicb.2013.00291

    Google Scholar 

  • Fu F X, Yu E, Garcia N S, et al. 2014. Differing responses of marine N2 fixers to warming and consequences for future diazotroph community structure. Aquatic Microbial Ecology, 72(1): 33–46, doi: 10.3354/ame01683

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hansen H P, Koroleff F. 1999. Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M, eds. Methods of Seawater Analysis. 3rd ed. Weinheim: Wiley-VCH, 170–198

    Google Scholar 

  • Hashihama F, Furuya K, Kitajima S, et al. 2009. Macro-scale exhaustion of surface phosphate by dinitrogen fixation in the western North Pacific. Geophysical Research Letters, 36(3): L03610

    Article  Google Scholar 

  • Jacq V, Ridame C, L’Helguen S, et al. 2014. Response of the unicellular diazotrophic cyanobacterium Crocosphaera watsonii to iron limitation. PLoS One, 9(1): e86749, doi: 10.1371/journal.pone. 0086749

    Article  Google Scholar 

  • Jiang Z B, Li H L, Zhai H C, et al. 2018. Seasonal and spatial changes in Trichodesmium associated with physicochemical properties in East China Sea and southern Yellow Sea. Journal of Geophysical Research: Biogeosciences, 123(2): 509–530, doi: 10.1002/2017JG004275

    Google Scholar 

  • Jickells T, Moore C M. 2015. The importance of atmospheric deposition for ocean productivity. Annual Review of Ecology, Evolution, and Systematics, 46: 481–501, doi: 10.1146/annurev-ecolsys-112414-054118

    Article  Google Scholar 

  • Karl D M, Michaels A F, Bergman B, et al. 2002. Dinitrogen fixation in the world’s oceans. Biogeochemistry, 57(1): 47–98, doi: 10.1023/ A:1015798105851

    Article  Google Scholar 

  • Kim D, Jeong J H, Kim T W, et al. 2017. The reduction in the biomass of cyanobacterial N2 fixer and the biological pump in the Northwestern Pacific Ocean. Scientific Reports, 7: 41810, doi: 10.1038/srep41810

    Article  Google Scholar 

  • Kitajima S, Furuya K, Hashihama F, et al. 2009. Latitudinal distribution of diazotrophs and their nitrogen fixation in the tropical and subtropical western North Pacific. Limnology and Oceanography, 54(2): 537–547, doi: 10.4319/lo.2009.54.2.0537

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kodama T, Furuya K, Hashihama F, et al. 2011. Occurrence of rain-origin nitrate patches at the nutrient-depleted surface in the East China Sea and the Philippine Sea during summer. Journal of Geophysical Research: Oceans, 116(C8): C08003

    Article  Google Scholar 

  • Lehodey P, Bertignac M, Hampton J, et al. 1997. El Nino Southern Oscillation and tuna in the Western Pacific. Nature, 389(6652): 715–718, doi: 10.1038/39575

    Article  Google Scholar 

  • Martino M, Hamilton D, Baker A R, et al. 2014. Western Pacific atmospheric nutrient deposition fluxes, their impact on surface ocean productivity. Global Biogeochemical Cycles, 28(7): 712–728, doi: 10.1002/2013GB004794

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Montoya J P, Voss M, Kähler P, et al. 1996. A simple, high-precision, high-sensitivity tracer assay for N2 fixation. Applied and Environmental Microbiology, 62(3): 986–993

    Google Scholar 

  • Montoya J P, Holl C M, Zehr J P, et al. 2004. High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature, 430(7003): 1027–1031, doi: 10.1038/nature02824

    Article  Google Scholar 

  • Qiu Bo, Rudnick D L, Cerovecki I, et al. 2015. The pacific north equatorial current: new insights from the origins of the Kuroshio and Mindanao Currents (OKMC) Project. Oceanography, 28(4): 24–33, doi: 10.5670/oceanog.2015.78

    Article  Google Scholar 

  • Ren Haojia, Chen Yichi, Wang X 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

    Article  Google Scholar 

  • Saito M A, Bertrand E M, Dutkiewicz S, et al. 2011. Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Croc osphaera watsonii. Proceedings of the National Academy of Sciences of the United States of America, 108(6): 2184–2189, doi: 10.1073/pnas.1006943108

    Article  Google Scholar 

  • Shiozaki T, Kodama T, Furuya K. 2014. Largescale impact of the island mass effect through nitrogen fixation in the western South Pacific Ocean. Geophysical Research Letters, 41(8): 2907–2913, doi: 10.1002/2014GL059835

    Article  Google Scholar 

  • Shiozaki T, Kodama T, Kitajima S, et al. 2013. Advective transport of diazotrophs and importance of their nitrogen fixation on new and primary production in the western Pacific warm pool. Limnology and Oceanography, 58(1): 49–60, doi: 10.4319/lo.2013. 58.1.0049

    Article  Google Scholar 

  • Shiozaki T, Bombar D, Riemann L, et al. 2017. Basin scale variability of active diazotrophs and nitrogen fixation in the North Pacific, from the tropics to the subarctic Bering Sea. Global Biogeo-chemical Cycles, 31(6): 996–1009, doi: 10.1002/2017GB005681

    Article  Google Scholar 

  • Wang Q, Garrity G M, Tiedje J M, et al. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261–5267, doi: 10.1128/AEM.00062-07

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wolfe D A, Schelske C L. 1967. Liquid scintillation and Geiger counting efficiencies for Carbon-14 incorporated by marine phyto-plankton in productivity measurements. ICES Journal of Mar-ine Science, 31(1): 31–37, doi: 10.1093/icesjms/31.1.31

    Article  Google Scholar 

  • Yang Guang, Li Chaolun, Guilini K, et al. 2017. Regional patterns of δ13C and δ15N stable isotopes of size-fractionated zooplankton in the western tropical North Pacific Ocean. Deep Sea Research Part I: Oceanographic Research Papers, 120: 39–47, doi: 10.1016/j.dsr.2016.12.007

    Article  Google Scholar 

  • Zehr J P, Turner P J. 2001. Nitrogen fixation: Nitrogenase genes and gene expression. Methods in Microbiology, 30: 271–286, doi: 10.1016/S0580-9517(01)30049-1

    Article  Google Scholar 

  • Zehr J P, Waterbury J B, Turner P J, et al. 2001. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature, 412(6847): 635–638, doi: 10.1038/35088063

    Article  Google Scholar 

  • Zhang Run, Chen Min, Cao Jianping, et al. 2012. Nitrogen fixation in the East China Sea and southern Yellow Sea during summer 2006. Marine Ecology Progress Series, 447: 77–86, doi: 10.3354/ meps09509

    Article  Google Scholar 

  • Zhang Run, Chen Min, Ma Qiang, et al. 2011. Latitudinal distribution of nitrogen isotopic composition in suspended particulate organic matter in tropical/subtropical seas. Isotopes in Environmental and Health Studies, 47(4): 489–497, doi: 10.1080/10256016. 2011.622442

    Article  Google Scholar 

  • Zhang Dongsheng, Lu Douding, Li Hongliang, et al. 2014. Seasonal dynamics of Trichodesmium in the northern East China Sea. Continental Shelf Research, 88: 161–170, doi: 10.1016/j.csr.2014. 05.016

    Article  Google Scholar 

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Acknowledgements

We are grateful to China Ocean Mineral Resources R&D Association (COMRA) for arranging the cruise and providing background data. We thank the captain and crew of the R/V Haiyang Liuhao for their invaluable assistance while sampling on the sea. We thank Xiguang Deng, Binbin Guo, Youcheng Bai, Xinyu Xu for technical assistance. Thanks are also due to COMRA scientists, Jianfang Chen, Zhi Yang and Wei Zhuang, for helpful discussions. We also thank the invaluable comment by anonymous reviewers.

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Correspondence to Run Zhang or Chunsheng Wang.

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Foundation item: The National Basic Research Program of China under contract No. 2015CB452903; the Foundation of China Ocean Mineral Resources R&D Association under contract No. DY135-E2-2-03; the Science and Technology Basic Resources Investigation Program of China under contract No. 2017FY201403; the National Natural Science Foundation of China under contract Nos 41676174, 41206104 and 41876198.

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Zhang, R., Zhang, D., Chen, M. et al. N2 fixation rate and diazotroph community structure in the western tropical North Pacific Ocean. Acta Oceanol. Sin. 38, 26–34 (2019). https://doi.org/10.1007/s13131-019-1513-4

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