Top-down control on major groups of global marine diazotrophs

Hua Wang; Ya-Wei Luo

doi:10.1007/s13131-021-1956-2

Volume 41 Issue 8

Aug. 2022

Turn off MathJax

Article Contents

Article Navigation > Acta Oceanologica Sinica > 2022 > 41(8): 111-119

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

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

PDF( 1258 KB)

Top-down control on major groups of global marine diazotrophs

doi: 10.1007/s13131-021-1956-2

Hua Wang^{1, 2},
Ya-Wei Luo^{1, 2
,
,}

1.
State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361102, China
2.
College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China

Funds: The National Natural Science Foundation of China under contract Nos 41890802 and 42076153.

More Information

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

Abstract

Abstract

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.
- marine diazotrophs,
- nitrogen fixation,
- top-down control,
- bottom-up control,
- Trichodesmium,
- diatom-diazotroph assemblages

FullText(HTML)

References(67)

References

[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
[2]	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
[3]	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
[4]	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
[5]	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
[6]	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
[7]	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]
[8]	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
[9]	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
[10]	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
[11]	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
[12]	Carpenter E J, Capone D G, Rueter J R. 1992. Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs. Dordrecht: Springer
[13]	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
[14]	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
[15]	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
[16]	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
[17]	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
[18]	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
[19]	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
[20]	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
[21]	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
[22]	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
[23]	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
[24]	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
[25]	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
[26]	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
[27]	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
[28]	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
[29]	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
[30]	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
[31]	Karl D, Michaels A, Bergman B, et al. 2002. Dinitrogen fixation in the world′s oceans. Biogeochemistry, 57–58: 47–98,
[32]	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
[33]	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
[34]	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
[35]	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
[36]	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
[37]	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
[38]	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
[39]	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
[40]	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
[41]	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
[42]	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
[43]	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
[44]	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
[45]	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
[46]	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
[47]	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
[48]	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
[49]	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
[50]	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
[51]	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
[52]	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
[53]	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
[54]	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
[55]	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
[56]	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
[57]	Tyrrell T. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature, 400(6744): 525–531. doi: 10.1038/22941
[58]	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
[59]	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
[60]	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
[61]	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
[62]	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
[63]	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
[64]	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
[65]	Zehr J P. 2011. Nitrogen fixation by marine cyanobacteria. Trends in Microbiology, 19(4): 162–173. doi: 10.1016/j.tim.2010.12.004
[66]	Zehr J P, Capone D G. 2020. Changing perspectives in marine nitrogen fixation. Science, 368(6492): eaay9514. doi: 10.1126/science.aay9514
[67]	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