Volume 41 Issue 8
Aug.  2022
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Hua Wang, Ya-Wei Luo. Top-down control on major groups of global marine diazotrophs[J]. Acta Oceanologica Sinica, 2022, 41(8): 111-119. doi: 10.1007/s13131-021-1956-2
Citation: Hua Wang, Ya-Wei Luo. Top-down control on major groups of global marine diazotrophs[J]. Acta Oceanologica Sinica, 2022, 41(8): 111-119. doi: 10.1007/s13131-021-1956-2

Top-down control on major groups of global marine diazotrophs

doi: 10.1007/s13131-021-1956-2
Funds:  The National Natural Science Foundation of China under contract Nos 41890802 and 42076153.
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  • Corresponding author: E-mail: ywluo@xmu.edu.cn
  • Received Date: 2021-07-16
  • Accepted Date: 2021-10-20
  • Available Online: 2022-04-14
  • Publish Date: 2022-08-15
  • Dinitrogen (N2) fixed by a group of prokaryotes (diazotrophs) is the dominant process adding bioavailable nitrogen into the ocean. Although it has been intensively studied how N2 fixation is controlled by resources (bottom-up factors), it is unclear whether the grazing (top-down control) effectively impacts growth and distribution of different diazotroph groups. In this study, we evaluate this question by conducting log-log regression of diazotroph biomass onto corresponding N2 fixation rates in the global ocean. The slope of the regression for Trichodesmium is ~0.8, indicating that a small portion of the increase in N2 fixation does not accumulate as its biomass. This leads to a conclusion that Trichodesmium is under a substantial top-down control, although bottom-up control still dominates. We also analyze the residuals of the regression in the North Atlantic, concluding that free trichomes of Trichodesmium are subject to stronger top-down control than its colonies. The weak correlation between the biomass and N2 fixation of unicellular cyanobacterial diazotrophs indicates that the degree of top-down control on this type of diazotrophs varies greatly. The analyses obtain unrealistic results for diatom-diazotroph assemblages due to complicated nitrogen sources of these symbioses. Our study reveals the variability of top-down control among different diazotroph groups across time and space, suggesting its importance in improving our understandings of ecology of diazotrophs and predictions of N2 fixation in biogeochemical models. Measurements of size-specific N2 fixation rates and growth rates of different diazotroph groups can be useful to more reliably analyze the top-down control on these key organisms in the global ocean.
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  • [1]
    Agawin N S R, Benavides M, Busquets A, et al. 2014. Dominance of unicellular cyanobacteria in the diazotrophic community in the Atlantic Ocean. Limnology and Oceanography, 59(2): 623–637. doi: 10.4319/lo.2014.59.2.0623
    Barton A D, Finkel Z V, Ward B A, et al. 2013. On the roles of cell size and trophic strategy in North Atlantic diatom and dinoflagellate communities. Limnology and Oceanography, 58(1): 254–266. doi: 10.4319/lo.2013.58.1.0254
    Benavides M, Agawin N S R, Arístegui J, et al. 2011. Nitrogen fixation by Trichodesmium and small diazotrophs in the subtropical northeast Atlantic. Aquatic Microbial Ecology, 65(1): 43–53. doi: 10.3354/ame01534
    Benavides M, Moisander P H, Daley M C, et al. 2016. Longitudinal variability of diazotroph abundances in the subtropical North Atlantic Ocean. Journal of Plankton Research, 38(3): 662–672. doi: 10.1093/plankt/fbv121
    Billen G, Servais P, Becquevort S. 1990. Dynamics of bacterioplankton in oligotrophic and eutrophic aquatic environments: bottom-up or top-down control? Hydrobiologia, 207(1): 37–42,doi: 10.1007/BF00041438
    Bombar D, Paerl R W, Riemann L. 2016. Marine non-cyanobacterial diazotrophs: moving beyond molecular detection. Trends in Microbiology, 24(11): 916–927. doi: 10.1016/j.tim.2016.07.002
    Boyer T P, Garcia H E, Locarnini R A, et al. 2018. World Ocean Atlas 2018. NOAA National Centers for Environmental Information. https://accession.nodc.noaa.gov/NCEI-WOA18[2021-08-30]
    Cabello A M, Cornejo-Castillo F M, Raho N, et al. 2016. Global distribution and vertical patterns of a prymnesiophyte-cyanobacteria obligate symbiosis. The ISME Journal, 10(3): 693–706. doi: 10.1038/ismej.2015.147
    Cáceres C, Taboada F G, Höfer J, et al. 2013. Phytoplankton growth and microzooplankton grazing in the subtropical northeast Atlantic. PLoS One, 8(7): e69159. doi: 10.1371/journal.pone.0069159
    Capone D G, Subramaniam A, Montoya J P, et al. 1998. An extensive bloom of the N2-fixing cyanobacterium Trichodesmium erythraeum in the central Arabian Sea. Marine Ecology Progress Series, 172: 281–292. doi: 10.3354/meps172281
    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
    Carpenter E J, Capone D G, Rueter J R. 1992. Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs. Dordrecht: Springer
    Conroy B J, Steinberg D K, Song B, et al. 2017. Mesozooplankton graze on cyanobacteria in the amazon river plume and western tropical North Atlantic. Frontiers in Microbiology, 8: 1436. doi: 10.3389/fmicb.2017.01436
    Cornejo-Castillo F M, Cabello A M, Salazar G, et al. 2016. Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton. Nature Communications, 7: 11071. doi: 10.1038/ncomms11071
    Cornejo-Castillo F M, del Carmen Muñoz-Marín M, Turk-Kubo K A, et al. 2019. UCYN-A3, a newly characterized open ocean sublineage of the symbiotic N2-fixing cyanobacterium Candidatus Atelocyanobacterium thalassa. Environmental Microbiology, 21(1): 111–124. doi: 10.1111/1462-2920.14429
    Dekaezemacker J, Bonnet S. 2011. Sensitivity of N2 fixation to combined nitrogen forms ( $\text{NO}_3^− $ and $\text{NH}_4^+ $ ) in two strains of the marine diazotroph Crocosphaera watsonii (Cyanobacteria). Marine Ecology Progress Series, 438: 33–46. doi: 10.3354/meps09297
    Detoni A M S, Costa L D F, Pacheco L A, et al. 2016. Toxic Trichodesmium bloom occurrence in the southwestern South Atlantic Ocean. Toxicon, 110: 51–55. doi: 10.1016/j.toxicon.2015.12.003
    Dufour P H, Torréton J P. 1996. Bottom-up and top-down control of bacterioplankton from eutrophic to oligotrophic sites in the tropical northeastern Atlantic Ocean. Deep-Sea Research Part I: Oceanographic Research Papers, 43(8): 1305–1320. doi: 10.1016/0967-0637(96)00060-X
    Dugenne M, Henderikx Freitas F, Wilson S T, et al. 2020. Life and death of Crocosphaera sp. in the Pacific Ocean: Fine scale predator–prey dynamics. Limnology and Oceanography, 65(11): 2603–2617. doi: 10.1002/lno.11473
    Falkowski P G, Koblfzek M, Gorbunov M, et al. 2004. Development and application of variable chlorophyll fluorescence techniques in marine ecosystems. In: Papageorgiou G C, Govindjee, eds. Chlorophyll a Fluorescence: A Signature of Photosynthesis. Dordrecht: Springer, 757–778
    Fonseca-Batista D, Li X F, Riou V, et al. 2019. Evidence of high N2 fixation rates in the temperate northeast Atlantic. Biogeosciences, 16(5): 999–1017. doi: 10.5194/bg-16-999-2019
    Foster R A, Kuypers M M M, Vagner T, et al. 2011. Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. The ISME Journal, 5(9): 1484–1493. doi: 10.1038/ismej.2011.26
    García-Gómez C, Mata M T, Van Breusegem F, et al. 2016. Low-steady-state metabolism induced by elevated CO2 increases resilience to UV radiation in the unicellular green-algae Dunaliella tertiolecta. Environmental and Experimental Botany, 132: 163–174. doi: 10.1016/j.envexpbot.2016.09.001
    Gruber N. 2008. The marine nitrogen cycle: overview and challenges. In: Capone D G, Bronk D A, Mulholland M R, et al., eds. Nitrogen in the Marine Environment. 2nd ed. San Diego: Academic Press, 1–50
    Guo C Z, Tester P A. 1994. Toxic effect of the bloom-forming Trichodesmium sp. (cyanophyta) to the copepod Acartia tonsa. Natural Toxins, 2(4): 222–227. doi: 10.1002/nt.2620020411
    Hawser S P, O′Neil J M, Roman M R, et al. 1992. Toxicity of blooms of the cyanobacterium Trichodesmium to zooplankton. Journal of Applied Phycology, 4(1): 79–86. doi: 10.1007/BF00003963
    Holl C M, Montoya J P. 2005. Interactions between nitrate uptake and nitrogen fixation in continuous cultures of the marine diazotroph Trichodesmium (cyanobacteria). Journal of Phycology, 41(6): 1178–1183. doi: 10.1111/j.1529-8817.2005.00146.x
    Holl C M, Villareal T A, Payne C D, et al. 2007. Trichodesmium in the western Gulf of Mexico: 15N2-fixation and natural abundance stable isotopic evidence. Limnology and Oceanography, 52(5): 2249–2259. doi: 10.4319/lo.2007.52.5.2249
    Hunt B P V, Bonnet S, Berthelot H, et al. 2016. Contribution and pathways of diazotroph-derived nitrogen to zooplankton during the VAHINE mesocosm experiment in the oligotrophic New Caledonia Lagoon. Biogeosciences, 13(10): 3131–3145. doi: 10.5194/bg-13-3131-2016
    Karl D M, Church M J, Dore J E, et al. 2012. Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proceedings of the National Academy of Sciences of the United States of America, 109(6): 1842–1849. doi: 10.1073/pnas.1120312109
    Karl D, Michaels A, Bergman B, et al. 2002. Dinitrogen fixation in the world′s oceans. Biogeochemistry, 57–58: 47–98,
    Keller D P, Oschlies A, Eby M. 2012. A new marine ecosystem model for the University of Victoria Earth System Climate Model. Geoscientific Model Development, 5(5): 1195–1220. doi: 10.5194/gmd-5-1195-2012
    LaRoche J, Breitbarth E. 2005. Importance of the diazotrophs as a source of new nitrogen in the ocean. Journal of Sea Research, 53(1–2): 67–91. doi: 10.1016/j.seares.2004.05.005
    Liu Hongbin, Buskey E J. 2000. The exopolymer secretions (EPS) layer surrounding Aureoumbra lagunensis cells affects growth, grazing, and behavior of protozoa. Limnology and Oceanography, 45(5): 1187–1191. doi: 10.4319/lo.2000.45.5.1187
    Lugomela C, Lyimo T J, Bryceson I, et al. 2002. Trichodesmium in coastal waters of Tanzania: diversity, seasonality, nitrogen and carbon fixation. Hydrobiologia, 477(1–3): 1–13. doi: 10.1023/A:1021017125376
    Luo Ya-Wei, Doney S C, Anderson L A, et al. 2012. Database of diazotrophs in global ocean: abundance, biomass and nitrogen fixation rates. Earth System Science Data, 4(1): 47–73. doi: 10.5194/essd-4-47-2012
    Luo Ya-Wei, Lima I D, Karl D M, et al. 2014. Data-based assessment of environmental controls on global marine nitrogen fixation. Biogeosciences, 11(3): 691–708. doi: 10.5194/bg-11-691-2014
    Moisander P H, Beinart R A, Hewson I, et al. 2010. Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science, 327(5972): 1512–1514. doi: 10.1126/science.1185468
    Montoya J P, Carpenter E J, Capone D G. 2002. Nitrogen fixation and nitrogen isotope abundances in zooplankton of the oligotrophic North Atlantic. Limnology and Oceanography, 47(6): 1617–1628. doi: 10.4319/lo.2002.47.6.1617
    Mulholland M R. 2007. The fate of nitrogen fixed by diazotrophs in the ocean. Biogeosciences, 4(1): 37–51. doi: 10.5194/bg-4-37-2007
    Neuer S, Cianca A, Helmke P, et al. 2007. Biogeochemistry and hydrography in the eastern subtropical North Atlantic gyre. Results from the European time-series station ESTOC. Progress in Oceanography, 72(1): 1–29. doi: 10.1016/j.pocean.2006.08.001
    O′Neil J M, Metzler P M, Glibert P M. 1996. Ingestion of 15N2-labelled Trichodesmium spp. and ammonium regeneration by the harpacticoid copepod Macrosetella gracilis. Marine Biology, 125(1): 89–96. doi: 10.1007/BF00350763
    Pace M L, Cole J J. 1994. Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microbial Ecology, 28(2): 181–193. doi: 10.1007/BF00166807
    Paulsen H, Ilyina T, Six K D, et al. 2017. Incorporating a prognostic representation of marine nitrogen fixers into the global ocean biogeochemical model HAMOCC. Journal of Advances in Modeling Earth Systems, 9(1): 438–464. doi: 10.1002/2016ms000737
    Raveh O, David N, Rilov G, et al. 2015. The temporal dynamics of coastal phytoplankton and bacterioplankton in the eastern Mediterranean Sea. PLoS ONE, 10(10): e0140690. doi: 10.1371/journal.pone.0140690
    Scavotto R E, Dziallas C, Bentzon-Tilia M, et al. 2015. Nitrogen-fixing bacteria associated with copepods in coastal waters of the North Atlantic Ocean. Environmental Microbiology, 17(10): 3754–3765. doi: 10.1111/1462-2920.12777
    Sheridan C C, Steinberg D K, Kling G W. 2002. The microbial and metazoan community associated with colonies of Trichodesmium spp. : a quantitative survey. Journal of Plankton Research, 24(9): 913–922. doi: 10.1093/plankt/24.9.913
    Siegel D A, Buesseler K O, Behrenfeld M J, et al. 2016. Prediction of the export and fate of global ocean net primary production: The EXPORTS science plan. Frontiers in Marine Science, 3: 22. doi: 10.3389/fmars.2016.00022
    Siegel D A, Buesseler K O, Doney S C, et al. 2014. Global assessment of ocean carbon export by combining satellite observations and food-web models. Global Biogeochemical Cycles, 28(3): 181–196. doi: 10.1002/2013gb004743
    Singh A, Gandhi N, Ramesh R. 2019. Surplus supply of bioavailable nitrogen through N2 fixation to primary producers in the eastern Arabian Sea during autumn. Continental Shelf Research, 181: 103–110. doi: 10.1016/j.csr.2019.05.012
    Sohm J A, Edwards B R, Wilson B G, et al. 2011. Constitutive extracellular polysaccharide (EPS) production by specific isolates of Crocosphaera watsonii. Frontiers in Microbiology, 2: 229. doi: 10.3389/fmicb.2011.00229
    Stukel M R, Coles V J, Brooks M T, et al. 2014. Top-down, bottom-up and physical controls on diatom-diazotroph assemblage growth in the Amazon River plume. Biogeosciences, 11(12): 3259–3278. doi: 10.5194/bg-11-3259-2014
    Tang Weiyi, Cassar N. 2019. Data-driven modeling of the distribution of diazotrophs in the global ocean. Geophysical Research Letters, 46(21): 12258–12269. doi: 10.1029/2019gl084376
    Tang Weiyi, Li Zuchuan, Cassar N. 2019. Machine learning estimates of global marine nitrogen fixation. Journal of Geophysical Research, 124(3): 717–730. doi: 10.1029/2018JG004828
    Thompson A, Carter B J, Turk-Kubo K, et al. 2014. Genetic diversity of the unicellular nitrogen-fixing cyanobacteria UCYN-A and its prymnesiophyte host. Environmental Microbiology, 16(10): 3238–3249. doi: 10.1111/1462-2920.12490
    Thompson A W, Foster R A, Krupke A, et al. 2012. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science, 337(6101): 1546–1550. doi: 10.1126/science.1222700
    Tyrrell T. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature, 400(6744): 525–531. doi: 10.1038/22941
    Verity P G, Robertson C Y, Tronzo C R, et al. 1992. Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnology and Oceanography, 37(7): 1434–1446. doi: 10.4319/lo.1992.37.7.1434
    Villareal T A. 1992. Marine nitrogen-fixing diatom-cyanobacteria symbioses. In: Carpenter E J, Capone D G, Rueter J G, eds. Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs. Dordrecht: Springer, 163–175
    Wang Weilei, Moore J K, Martiny A C, et al. 2019. Convergent estimates of marine nitrogen fixation. Nature, 566(7743): 205–211. doi: 10.1038/s41586-019-0911-2
    Webb E A, Ehrenreich I M, Brown S L, et al. 2009. Phenotypic and genotypic characterization of multiple strains of the diazotrophic cyanobacterium, Crocosphaera watsonii, isolated from the open ocean. Environmental Microbiology, 11(2): 338–348. doi: 10.1111/j.1462-2920.2008.01771.x
    White A E, Watkins-Brandt K S, Church M J. 2018. Temporal variability of Trichodesmium spp. and diatom-diazotroph assemblages in the North Pacific subtropical gyre. Frontiers in Marine Science, 5: 27. doi: 10.3389/fmars.2018.00027
    Wilson S T, Aylward F O, Ribalet F, et al. 2017. Coordinated regulation of growth, activity and transcription in natural populations of the unicellular nitrogen-fixing cyanobacterium Crocosphaera. Nature Microbiology, 2(9): 17118. doi: 10.1038/nmicrobiol.2017.118
    Yeung L Y, Berelson W M, Young E D, et al. 2012. Impact of diatom-diazotroph associations on carbon export in the Amazon River plume. Geophysical Research Letters, 39(18): L18609. doi: 10.1029/2012GL053356
    Zehr J P. 2011. Nitrogen fixation by marine cyanobacteria. Trends in Microbiology, 19(4): 162–173. doi: 10.1016/j.tim.2010.12.004
    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, Kudela R M. 2010. Nitrogen cycle of the open ocean: from genes to ecosystems. Annual Review of Marine Science, 3: 197–225. doi: 10.1146/annurev-marine-120709-142819
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