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Contrasting resistance of prokaryotic plankton biomass and community composition to experimental nutrient inputs in a coastal upwelling system (NW Spain)

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Abstract

Increasing nutrient inputs driven by global environmental pressures may lead to changes in prokaryotic plankton biomass and community composition in coastal environments. Nutrient addition experiments (inorganic, organic, and mixed) were performed at the continental shelf outside the Ría de Vigo, in spring, summer and autumn 2014, and the results contrasted with those from similar previous experiments carried out inside the ría in 2013. The mixed nutrient additions caused the greatest changes in community composition, mostly consisting of blooms of Vibrionales. Inorganic nutrients yielded increased proportions of Oceanospirillales and Alteromonadales. Euclidean distances among samples were used to estimate compositional resistance to disturbances derived from nutrient additions. Changes in prokaryotic biomass were used as an indicator of biomass resistance. Generally, prokaryotic communities were more resistant to inorganic than organic nutrient additions. Communities sampled inside the ría, presumably exposed to greater perturbations, showed milder variability in the non-amended control than those from outside the ría. By contrast, shelf communities, with higher ambient organic matter concentrations, were more resistant to organic and mixed nutrient additions than those from the ría. Our data suggest that the perturbation history is related to the resistance of microbial communities to changes in nutrient inputs into the coastal ocean.

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Data availability

The prokaryotic DNA sequences are publicly available at the European Nucleotide Archive, https://www.ebi.ac.uk/ena (PRJEB47591).

References

  • Allen, R., L. J. Hoffmann, C. S. Law & T. C. Summerfield, 2020. Subtle bacterioplankton community responses to elevated CO2 and warming in the oligotrophic South Pacific gyre. Environmental Microbiology Reports 12: 377–386.

    Article  CAS  PubMed  Google Scholar 

  • Allison, S. D. & J. B. H. Martiny, 2008. Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences 105: 11512–11519.

    Article  ADS  CAS  Google Scholar 

  • Alonso-Pérez, F., T. Ysebaert & C. G. Castro, 2010. Effects of suspended mussel culture on benthic-pelagic coupling in a coastal upwelling system (Ría de Vigo, NW Iberian Peninsula). Journal of Experimental Marine Biology and Ecology 382: 96–107.

    Article  Google Scholar 

  • Altschul, S. F., W. Gish, W. Miller, E. W. Myers & D. J. Lipman, 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.

    Article  CAS  PubMed  Google Scholar 

  • Álvarez-Salgado, X. A. & A. E. J. Miller, 1998. Simultaneous determination of dissolved organic carbon and total dissolved nitrogen in seawater by high temperature catalytic oxidation: conditions for precise shipboard measurements. Marine Chemistry 62: 325–333.

    Article  Google Scholar 

  • Álvarez-Salgado, X. A., M. D. Doval & F. F. Pérez, 1999. Dissolved organic matter in shelf waters off the Ria de Vigo (NW Iberian upwelling system). Journal of Marine Systems 18: 383–394.

    Article  ADS  Google Scholar 

  • Andrade-Linares, D. R., A. Lehmann & M. C. Rillig, 2016. Microbial stress priming: a meta-analysis. Environmental Microbiology 18: 1277–1288.

    Article  PubMed  Google Scholar 

  • Awasthi, A., M. Singh, S. K. Soni, R. Singh & A. Kalra, 2014. Biodiversity acts as insurance of productivity of bacterial communities under abiotic perturbations. ISME Journal Nature Publishing Group 8: 2445–2452.

    Google Scholar 

  • Baert, J. M., F. De Laender, K. Sabbe & C. R. Janssen, 2016. Biodiversity increases functional and compositional resistance, but decreases resilience in phytoplankton communities. Ecology 97: 3433–3440.

    Article  PubMed  Google Scholar 

  • Barton, E. D., J. L. Largier, R. Torres, M. Sheridan, A. Trasviña, A. Souza, Y. Pazos & A. Valle-Levinson, 2015. Coastal upwelling and downwelling forcing of circulation in a semi-enclosed bay: Ria de Vigo. Progress in Oceanography 134: 173–189.

    Article  ADS  Google Scholar 

  • Bonilla-Findji, O., J. P. Gattuso, M. D. Pizay & M. G. Weinbauer, 2010. Autotrophic and heterotrophic metabolism of microbial planktonic communities in an oligotrophic coastal marine ecosystem: Seasonal dynamics and episodic events. Biogeosciences 7: 3491–3503.

    Article  ADS  CAS  Google Scholar 

  • Bôto, M. L., C. Magalhães, R. Perdigão, D. A. M. Alexandrino, J. P. Fernandes, A. M. Bernabeu, S. Ramos, M. F. Carvalho, M. Semedo, J. Laroche, C. M. R. Almeida & A. P. Mucha, 2021. Harnessing the potential of native microbial communities for bioremediation of oil spills in the iberian peninsula NW coast. Frontiers in Microbiology 12: 633659.

    Article  PubMed  PubMed Central  Google Scholar 

  • Broullón, E., P. J. S. Franks, B. Fernández Castro, M. Gilcoto, A. Fuentes-Lema, M. Pérez-Lorenzo, E. Fernández & B. Mouriño-Carballido, 2023. Rapid phytoplankton response to wind forcing influences productivity in upwelling bays, Wiley, Limnology And Oceanography Letters:

    Book  Google Scholar 

  • Calvo-Díaz, A. & X. A. G. Morán, 2006. Seasonal dynamics of picoplankton in shelf waters of the southern Bay of Biscay. Aquatic Microbial Ecology 42: 159–174.

    Article  Google Scholar 

  • Clarke, K., & R. Gorley, 2009. PRIMER6 & PERMANOVA+. Plymouth, UK.

  • Comte, J., L. Fauteux & P. A. Del Giorgio, 2013. Links between metabolic plasticity and functional redundancy in freshwater bacterioplankton communities. Frontiers in Microbiology 4: 1–11.

    Article  Google Scholar 

  • Des, M., M. DeCastro, M. C. Sousa, J. M. Dias & M. Gómez-Gesteira, 2019. Hydrodynamics of river plume intrusion into an adjacent estuary: the Minho River and Ria de Vigo. Journal of Marine Systems 189: 87–97. https://doi.org/10.1016/j.jmarsys.2018.10.003.

    Article  ADS  Google Scholar 

  • Downing, J. A., C. W. Osenberg & O. Sarnelle, 1999. Meta-analysis of marine nutrient-enrichment experiments: variation in the magnitude of nutrient limitation. Ecological Society of America 80: 1157–1167.

    Google Scholar 

  • Durán-Romero, C., V. E. Villafañe, M. S. Valiñas, R. J. Gonçalves & E. W. Helbling, 2017. Solar UVR sensitivity of phyto- and bacterioplankton communities from Patagonian coastal waters under increased nutrients and acidification. ICES Journal of Marine Science 74: 1062–1073.

    Article  Google Scholar 

  • Fernández, E., X. A. Álvarez-Salgado, R. Beiras, A. Ovejero & G. Méndez, 2016. Coexistence of urban uses and shellfish production in an upwelling-driven, highly productive marine environment: the case of the Ría de Vigo (Galicia, Spain). Regional Studies in Marine Science 8: 362–370.

    Article  Google Scholar 

  • Fraga, F., 1981. Upelling off the Galician coast, northwest Spain. Coastal and Estuarine Sciences 1: 176–182.

    Article  Google Scholar 

  • Fuhrman, J. A., I. Hewson, M. S. Schwalbach, J. A. Steele, M. V. Brown & S. Naeem, 2006. Annually reoccurring bacterial communities are predictable from ocean conditions. Proceedings of the National Academy of Sciences of the United States of America 103: 13104–131099.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Gago, J., X. A. Álvarez-Salgado, M. Nieto-Cid, S. Brea & S. Piedracoba, 2005. Continental inputs of C, N, P and Si species to the Ría de Vigo (NW Spain). Estuarine, Coastal and Shelf Science 65: 74–82.

    Article  ADS  CAS  Google Scholar 

  • Gago, J., J. M. Cabanas, G. Casas & A. Miranda, 2011. Thermohaline measurements in the continental shelf zone of the NW Iberian Peninsula, 1994–2006. Climate Research 48: 219–229.

    Article  ADS  Google Scholar 

  • Galand, P. E., O. Pereira, C. Hochart, J. C. Auguet & D. Debroas, 2018. A strong link between marine microbial community composition and function challenges the idea of functional redundancy. ISME Journal Springer, US 12: 2470–2478.

    Article  CAS  Google Scholar 

  • Giovannoni, S. J., 2017. SAR11 bacteria: the most abundant plankton in the oceans. Annual Review of Marine Science 9: 231–255.

    Article  ADS  PubMed  Google Scholar 

  • Glaeser, S. P., H. P. Grossart & J. Glaeser, 2010. Singlet oxygen, a neglected but important environmental factor: short-term and long-term effects on bacterioplankton composition in a humic lake. Environmental Microbiology 12: 3124–3136.

    Article  CAS  PubMed  Google Scholar 

  • Glasby, T. M., & A. J. Underwood, 1995. Sampling to differentiate between pulse and press perturbations.

  • Gloor, G. B., J. M. Macklaim, V. Pawlowsky-Glahn & J. J. Egozcue, 2017. Microbiome datasets are compositional: and this is not optional. Frontiers in Microbiology 8: 1–6.

    Article  Google Scholar 

  • Golyshin, P., M. Ferrer, T. Chernikova, O. Golyshina & M. Yakimov, 2010. Oleispira. In McGenity, T., J. van der Meer & V. de Lorenzo (eds), Handbook of hydrocarbon and lipid microbiology Springer, Berlin: 1755–1763.

    Chapter  Google Scholar 

  • Grasshof, K., K. Kremiling, & M. Ehrhardt, 1999. Methods of seawater analysis.

  • Griffiths, B. S. & L. Philippot, 2013. Insights into the resistance and resilience of the soil microbial community. FEMS Microbiology Reviews 37: 112–129.

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez-Barral, A., E. Teira, M. Hernández-Ruiz & E. Fernández, 2021. Response of prokaryote community composition to riverine and atmospheric nutrients in a coastal embayment: role of organic matter on Vibrionales. Estuarine, Coastal and Shelf Science 251: 107196.

    Article  Google Scholar 

  • Hernández-Ruiz, M., E. Barber-Lluch, A. Prieto, R. Logares & E. Teira, 2020. Response of pico-nano-eukaryotes to inorganic and organic nutrient additions. Estuarine, Coastal and Shelf Science 235: 106565.

    Article  Google Scholar 

  • Hillebrand, H., S. Langenheder, K. Lebret, E. Lindström, Ö. Östman & M. Striebel, 2018. Decomposing multiple dimensions of stability in global change experiments. Ecology Letters 21: 21–30.

    Article  PubMed  Google Scholar 

  • Jickells, T. D., E. Buitenhuis, K. Altieri, A. R. Baker, D. Capone, R. A. Duce, F. Dentener, K. Fennel, M. Kanakidou, J. LaRoche, K. Lee, P. Liss, J. J. Middelburg, J. K. Moore, G. Okin, A. Oschlies, M. Sarin, S. Seitzinger, J. Sharples, A. Singh, P. Suntharalingam, M. Uematsu & L. M. Zamora, 2017. A reevaluation of the magnitude and impacts of anthropogenic atmospheric nitrogen inputs on the ocean. Global Biogeochemical Cycles 31: 289–305.

    Article  ADS  CAS  Google Scholar 

  • Joglar, V., A. Prieto, E. Barber-Lluch, M. Hernández-Ruiz, E. Fernández & E. Teira, 2020. Spatial and temporal variability in the response of phytoplankton and prokaryotes to B-vitamin amendments in an upwelling system. Biogeosciences 17: 2807–2823.

    Article  ADS  Google Scholar 

  • Justel-Díez, M., E. Delgadillo-Nuño, A. Gutiérrez-Barral, P. García-Otero, I. Alonso-Barciela, P. Pereira-Villanueva, X. A. Álvarez-Salgado, A. Velando, E. Teira & E. Fernández, 2023. Inputs of seabird guano alter microbial growth, community composition and the phytoplankton–bacterial interactions in a coastal system. Environmental Microbiology 25: 1155–1173.

    Article  PubMed  Google Scholar 

  • Kennedy, K., M. W. Hall, M. D. J. Lynch, G. Moreno-Hagelsieb & J. D. Neufeld, 2014. Evaluating bias of Illumina-based bacterial 16S rRNA gene profiles. Applied and Environmental Microbiology American Society for Microbiology 80: 5717–5722.

    Article  ADS  Google Scholar 

  • Kérouel, R. & A. Aminot, 1997. Fluorometric determination of ammonia in sea and estuarine waters by direct segmented flow analysis. Marine Chemistry 57: 265–275.

    Article  Google Scholar 

  • Largier, J. L., 2019. Upwelling bays: how coastal upwelling controls circulation. Habitat, and Productivity in Bays. https://doi.org/10.1146/annurev-marine-010419-.

    Article  Google Scholar 

  • Liao, J., J. Xu, X. Yuan, Y. Liang, Y. Guo, W. Zhou, H. Huang, S. Liu & A. Long, 2019. Interactive effects of ultraviolet radiation and dissolved organic carbon on phytoplankton growth and photosynthesis in Sanya Bay, Northern South China sea. Ocean Science Journal Korea Ocean Research and Development Institute 54: 581–593.

    CAS  Google Scholar 

  • Lindh, M. V. & J. Pinhassi, 2018. Sensitivity of bacterioplankton to environmental disturbance: A review of Baltic Sea field studies and experiments. Frontiers in Marine Science 5: 1–17.

    Article  Google Scholar 

  • Logares, R., 2017. Workflow for analysing miseq amplicons based on uparse.

  • Lorenzo, L. M., B. Arbones, G. H. Tilstone & F. G. Figueiras, 2005. Across-shelf variability of phytoplankton composition, photosynthetic parameters and primary production in the NW Iberian upwelling system. Journal of Marine Systems 54: 157–173.

    Article  ADS  Google Scholar 

  • Louca, S., M. F. Polz, F. Mazel, M. B. N. Albright, J. A. Huber, M. I. O’Connor, M. Ackermann, A. S. Hahn, D. S. Srivastava, S. A. Crowe, M. Doebeli & L. W. Parfrey, 2018. Function and functional redundancy in microbial systems. Nature Ecology and Evolution 2: 936–943.

    Article  PubMed  Google Scholar 

  • Manrique, J. M., A. Y. Calvo, S. R. Halac, V. E. Villafañe, L. R. Jones & E. Walter Helbling, 2012. Effects of UV radiation on the taxonomic composition of natural bacterioplankton communities from Bahía Engaño (Patagonia, Argentina). Journal of Photochemistry and Photobiology b: Biology 117: 171–178. https://doi.org/10.1016/j.jphotobiol.2012.09.019.

    Article  CAS  PubMed  Google Scholar 

  • Marotz, C., A. Sharma, G. Humphrey, N. Gottel, C. Daum, J. A. Gilbert, E. Eloe-Fadrosh & R. Knight, 2019. Triplicate PCR reactions for 16S rRNA gene amplicon sequencing are unnecessary. BioTechniques Future Science 67: 29–32.

    Article  CAS  Google Scholar 

  • Martínez-García, S., E. Fernández, X. A. Álvarez-Salgado, J. González, C. Lønborg, E. Marañón, X. A. G. Morán & E. Teira, 2010. Differential responses of phytoplankton and heterotrophic bacteria to organic and inorganic nutrient additions in coastal waters off the NW Iberian Peninsula. Marine Ecology Progress Series 416: 17–33.

    Article  ADS  Google Scholar 

  • Messié, M. & F. P. Chavez, 2015. Seasonal regulation of primary production in eastern boundary upwelling systems. Progress in Oceanography Elsevier Ltd 134: 1–18.

    Article  ADS  Google Scholar 

  • Nikolenko, S. I., A. I. Korobeynikov & M. A. Alekseyev, 2013. BayesHammer: Bayesian clustering for error correction in single-cell sequencing. BMC Genomics 14: S7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Norland, S., 1993. The relationship between biomass and volume of bacteria. In Kemp, P., B. Sherr, E. Sherr & J. Cole (eds), Handbook of methods in aquatic microbial ecology Lewis Publishers, Boca Raton, FL: 303–307.

    Google Scholar 

  • Oksanen, J., G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. Minchin, R. O’Hara, G. Simpson, P. Solymos, M. Stevens, E. Szoecs, & H. Wagner, 2020. Community Ecology Package.

  • Oliver, A. E., L. K. Newbold, A. S. Whiteley & C. J. van der Gast, 2014. Marine bacterial communities are resistant to elevated carbon dioxide levels. Environmental Microbiology Reports 6: 574–582.

    Article  CAS  PubMed  Google Scholar 

  • Orwin, K. H. & D. A. Wardle, 2004. New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biology and Biochemistry 36: 1907–1912.

    Article  CAS  Google Scholar 

  • Parada, A. E., D. M. Needham & J. A. Fuhrman, 2016. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environmental Microbiology 18: 1403–1414.

    Article  CAS  PubMed  Google Scholar 

  • Prego, R., 1993. General aspects of carbon biogeochemistry in the ria of Vigo, northwestern Spain. Geochimica Et Cosmochimica Acta 57: 2041–2052.

    Article  ADS  CAS  Google Scholar 

  • Quast, C., E. Pruesse, P. Yilmaz, J. Gerken, T. Schweer, F. O. Glo, P. Yarza, J. Peplies & F. O. Glöckner, 2013. The SILVA ribosomal RNA gene database project : improved data processing and web-based tools. Nucleic Acids Research 41: 590–596.

    Article  Google Scholar 

  • Renes, S. E., J. Sjöstedt, I. Fetzer & S. Langenheder, 2020. Disturbance history can increase functional stability in the face of both repeated disturbances of the same type and novel disturbances. Scientific Reports Nature Publishing Group UK 10: 1–13.

    ADS  Google Scholar 

  • Ríos, A. F., M. Á. Nombela, F. F. Pérez, G. Rosón & F. Fraga, 1992. Calculation of runoff to an estuary. ria de Vigo. Scientia Marina Scientia Marina 56: 29–33.

    Google Scholar 

  • Rognes, T., T. Flouri, B. Nichols, C. Quince & F. Mahé, 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ 2016: 1–22.

    Google Scholar 

  • Román, M., E. Fernández & G. Méndez, 2019. Anthropogenic nutrient inputs in the NW Iberian Peninsula estuaries determined by nitrogen and carbon isotopic signatures of Zostera noltei seagrass meadows. Marine Environmental Research 143: 30–38.

    Article  PubMed  Google Scholar 

  • Santos, A. A., D. O. Guedes, M. U. G. Barros, S. Oliveira, A. B. F. Pacheco, S. M. F. O. Azevedo, V. F. Magalhães, C. J. Pestana, C. Edwards, L. A. Lawton & J. Capelo-Neto, 2021. Effect of hydrogen peroxide on natural phytoplankton and bacterioplankton in a drinking water reservoir: Mesocosm-scale study. Water Research 197: 117069. https://doi.org/10.1016/j.watres.2021.117069.

    Article  CAS  PubMed  Google Scholar 

  • de Scally, S. Z., S. Chaffron, & T. P. Makhalanyane, 2020. Polar opposites; bacterioplankton susceptibility and mycoplankton resistance to ocean acidification. bioRxiv.

  • Schirmer, M., U. Z. Ijaz, R. D’Amore, N. Hall, W. T. Sloan & C. Quince, 2015. Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform. Nucleic Acids Research 43: e37.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shade, A., J. S. Read, D. G. Welkie, T. K. Kratz, C. H. Wu & K. D. McMahon, 2011. Resistance, resilience and recovery: Aquatic bacterial dynamics after water column disturbance. Environmental Microbiology 13: 2752–2767.

    Article  CAS  PubMed  Google Scholar 

  • Shade, A., H. Peter, S. D. Allison, D. L. Baho, M. Berga, H. Bürgmann, D. H. Huber, S. Langenheder, J. T. Lennon, J. B. H. Martiny, K. L. Matulich, T. M. Schmidt & J. Handelsman, 2012. Fundamentals of microbial community resistance and resilience. Frontiers in Microbiology 3: 1–19.

    Article  Google Scholar 

  • Sjöstedt, J., S. Langenheder, E. Kritzberg, C. M. G. Karlsson & E. S. Lindström, 2018. Repeated disturbances affect functional but not compositional resistance and resilience in an aquatic bacterioplankton community. Environmental Microbiology Reports 10: 493–500.

    Article  PubMed  Google Scholar 

  • Székely, A. J. & S. Langenheder, 2017. Dispersal timing and drought history influence the response of bacterioplankton to drying-rewetting stress. ISME Journal Nature Publishing Group 11: 1764–1776. https://doi.org/10.1038/ismej.2017.55.

    Article  Google Scholar 

  • Teira, E., S. Martínez-García, C. Carreira & X. A. G. Morán, 2011. Changes in bacterioplankton and phytoplankton community composition in response to nutrient additions in coastal waters off the NW Iberian Peninsula. Marine Ecology Progress Series 426: 87–104.

    Article  ADS  CAS  Google Scholar 

  • Teira, E., V. Hernando-Morales, A. Fernández, S. Martínez-García, X. A. Álvarez-Salgado, A. Bode & M. M. Varela, 2015. Local differences in phytoplankton-bacterioplankton coupling in the coastal upwelling off Galicia (NW Spain). Marine Ecology Progress Series 528: 53–69.

    Article  ADS  Google Scholar 

  • Teira, E., M. Hernández-Ruiz, E. Barber-Lluch, C. Sobrino, I. G. Teixeira, X. A. Álvarez-Salgado, M. Nieto-Cid, S. Martínez-García, F. G. Figueiras & E. Fernández, 2016. Bacterioplankton responses to riverine and atmospheric inputs in a coastal upwelling system (Ría de Vigo, NW Spain). Marine Ecology Progress Series 542: 39–50.

    Article  ADS  CAS  Google Scholar 

  • Teira, E., R. Logares, A. Gutiérrez-Barral, I. Ferrera, M. M. Varela, X. A. G. Morán & J. M. Gasol, 2019. Impact of grazing, resource availability and light on prokaryotic growth and diversity in the oligotrophic surface global ocean. Environmental Microbiology 21: 1482–1496.

    Article  CAS  PubMed  Google Scholar 

  • Traving, S. J., O. Rowe, N. M. Jakobsen, H. Sørensen, J. Dinasquet, C. A. Stedmon, A. Andersson, L. Riemann & O. Rowe, 2017. The effect of increased loads of dissolved organic matter on estuarine microbial community composition and function. Frontiers in Microbiology 8: 351.

    Article  PubMed  PubMed Central  Google Scholar 

  • von Scheibner, M., U. Sommer & K. Jürgens, 2017. Tight coupling of glaciecola spp. and diatoms during cold-water phytoplankton spring blooms. Frontiers in Microbiology 8: 1–11.

    Google Scholar 

  • Wear, E. K., C. A. Carlson, A. K. James, M. A. Brzezinski, L. A. Windecker & C. E. Nelson, 2015. Synchronous shifts in dissolved organic carbon bioavailability and bacterial community responses over the course of an upwelling-driven phytoplankton bloom. Limnology and Oceanography 60: 657–677.

    Article  ADS  Google Scholar 

  • Xiong, J., S. Xiong, P. Qian, D. Zhang, L. Liu & Y. Fei, 2016. Thermal discharge-created increasing temperatures alter the bacterioplankton composition and functional redundancy. AMB Express 6: 68.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., K. Kobert, T. Flouri & A. Stamatakis, 2014. PEAR: a fast and accurate illumina paired-end reAd mergeR. Bioinformatics 30: 614–620.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was carried out in the Centro de Investigación Mariña from the Universidade de Vigo. The shelf samples were taken onboard R/V José Navaz, and the ría water onboard R/V Mytilus. We thank all personnel who took part in the obtention of seawater, experiments, analysis, and support.

Funding

This work was supported by the Xunta de Galicia, DIMENSION project [EM2013/023]; and the Ministerio de Ciencia e Innovación, REIMAGE project [CTM2011-30155-C03-01].

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AG: Writing—Original draft, Writing- Review and Editing, Formal Analysis, Visualization. EF: Writing—Review and Editing, Methodology, Resources, Conceptualization, Project Administration, Funding Acquisition. MH: Investigation. ET: Writing—Review and Editing, Methodology, Resources, Conceptualization, Project Administration, Funding Acquisition.

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Correspondence to A. Gutiérrez-Barral.

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Gutiérrez-Barral, A., Fernández, E., Hernández-Ruiz, M. et al. Contrasting resistance of prokaryotic plankton biomass and community composition to experimental nutrient inputs in a coastal upwelling system (NW Spain). Hydrobiologia 851, 1907–1921 (2024). https://doi.org/10.1007/s10750-023-05424-y

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