Bacteria enhance the production of extracellular polymeric substances by the green dinoflagellate Lepidodinium chlorophorum

Siano, R. et al. Citizen participation in monitoring phytoplankton seawater discolorations. Mar. Policy 117, 1–11. https://doi.org/10.1016/j.marpol.2018.01.022 (2018).

Article  Google Scholar 

Elbrächter, M. & Schnepf, E. Gymnodinium chlorophorum, a new, green, bloom-forming dinoflagellate (Gymnodiniales, Dinophyceae) with a vestigial prasinophyte endosymbiont. Phycologia 35, 381–393 (1996).

Article  Google Scholar 

Hansen, G., Botes, L. & De Salas, M. Ultrastructure and large subunit rDNA sequences of Lepidodinium viride reveal a close relationship to Lepidodinium chlorophorum comb. Nov. (=Gymnodinium chlorophorum). Phycol. Res. 55, 25–41. https://doi.org/10.1111/j.1440-1835.2006.00442.x (2007).

CAS  Article  Google Scholar 

Gavalás-Olea, A. et al. 19,19′-diacyloxy signature: An atypical level of structural evolution in carotenoid pigments. Org. Lett. 18, 4642–4645. https://doi.org/10.1021/acs.orglett.6b02272 (2016).

CAS  Article  PubMed  Google Scholar 

Jackson, C., Knoll, A. H., Chan, C. X. & Verbruggen, H. Plastid phylogenomics with broad taxon sampling further elucidates the distinct evolutionary origins and timing of secondary green plastids. Sci. Rep. 8, 1523. https://doi.org/10.1038/s41598-017-18805-w (2018).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Kamikawa, R. et al. Plastid genome-based phylogeny pinpointed the origin of the green-colored plastid in the dinoflagellate Lepidodinium chlorophorum. Genome Biol. Evol. 7, 1133–1140. https://doi.org/10.1093/gbe/evv060 (2015).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Chapelle, A., Lazure, P. & Ménesguen, A. Modelling eutrophication events in a coastal ecosystem. Sensitivity analysis. Estuar. Coast. Shelf Sci. 39, 529–548. https://doi.org/10.1016/S0272-7714(06)80008-9 (1994).

ADS  CAS  Article  Google Scholar 

Sournia, A. et al. The repetitive and expanding occurrence of a green, bloom-forming dinoflagellate (Dinophyceae) on the coast of France. Cryptogam. Algol. 13, 1–13 (1992).

Google Scholar 

Claquin, P., Probert, I., Lefebvre, S. & Veron, B. Effects of temperature on photosynthetic parameters and TEP production in eight species of marine microalgae. Aquat. Microb. Ecol. 51, 1–11. https://doi.org/10.3354/ame01187 (2008).

Article  Google Scholar 

Alldredge, A. L., Passow, U. & Logan, B. E. The abundance and significance of a class of large, transparent organic particles in the ocean. Deep-Sea Res. 40, 1131–1140. https://doi.org/10.1016/0967-0637(93)90129-Q (1993).

CAS  Article  Google Scholar 

Passow, U. Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr. 55, 287–333. https://doi.org/10.1016/S0079-6611(02)00138-6 (2002).

ADS  Article  Google Scholar 

Verdugo, P. et al. The oceanic gel phase: A bridge in the DOM-POM continuum. Mar. Chem. 92, 67–85. https://doi.org/10.1016/j.marchem.2004.06.017 (2004).

CAS  Article  Google Scholar 

Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nature 5, 782–791. https://doi.org/10.1038/nrmicro1747 (2007).

CAS  Article  Google Scholar 

Bittar, T. B., Passow, U., Hamaraty, L., Bidle, K. D. & Harvey, E. L. An updated method for the calibration of transparent exopolymer particle measurements. Limnol. Oceanogr. Methods. 16, 621–628. https://doi.org/10.1002/lom3.10268 (2018).

Article  Google Scholar 

Mari, X., Passow, U., Migon, C., Burd, A. B. & Legendre, L. Transparent exopolymer particles: Effects on carbon cycling in the ocean. Prog. Oceanogr. 151, 13–37. https://doi.org/10.1016/j.pocean.2016.11.002 (2017).

ADS  Article  Google Scholar 

Passow, U. et al. The origin of transparent exopolymer particles (TEP) and their role in the sedimentation of particulate matter. Cont. Shelf. Res. 21, 327–346. https://doi.org/10.1016/S0278-4343(00)00101-1 (2001).

ADS  Article  Google Scholar 

Jenkinson, I. R. Oceanographic implications of non-newtonian properties found in phytoplankton cultures. Nature 323, 435–437. https://doi.org/10.1038/323435a0 (1986).

ADS  Article  Google Scholar 

Alldredge, A. L. & Gotschalk, C. C. Direct observations of the mass flocculation of diatom blooms: Characteristics, settling velocities and formation of diatom aggregates. Deep-Sea Res. 36, 159–171. https://doi.org/10.1016/0198-0149(89)90131-3 (1989).

ADS  CAS  Article  Google Scholar 

Schapira, M., McQuaid, C. D. & Froneman, P. W. Free-living and particle-associated prokaryote metabolism in giant kelp forests: Implications for carbon flux in a sub-Antarctic coastal area. Estuar. Coast. Shelf. Sci. 106, 69–79. https://doi.org/10.1016/j.ecss.2012.04.031 (2012).

ADS  CAS  Article  Google Scholar 

Schapira, M., McQuaid, C. D. & Froneman, P. W. Metabolism of free-living particle-associated prokaryotes: Consequences for carbon flux around a Southern Ocean archipelago. J. Mar. Syst. 90, 58–66. https://doi.org/10.1016/j.jmarsys.2011.08.009 (2012).

Article  Google Scholar 

Bhaskar, P.V. & Bhosle, N.B. Microbial extracellular polymeric substances in marine biogeochemical processes. Curr. Sci. 88, 45–53. http://drs.nio.org/drs/handle/2264/89 (2005).

Passow, U. & Alldredge, A. L. A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol. Oceanogr. 40, 1326–1335. https://doi.org/10.4319/lo.1995.40.7.1326 (1995).

ADS  CAS  Article  Google Scholar 

Gärdes, A., Iversen, M. H., Grossart, H. P., Passow, U. & Ullrich, M. S. Diatom-associated bacteria are required for aggregation of Thalassiosira weissflogii. ISME J. 5, 436–445. https://doi.org/10.1038/ismej.2010.145 (2011).

CAS  Article  PubMed  Google Scholar 

Nosaka, Y., Yamashita, Y. & Suzuki, K. Dynamics and origin of transparent exopolymer particles in the Oyashio region of the Western Subarctic Pacific during the spring diatom bloom. Front. Mar. Sci. 4, 1–16. https://doi.org/10.3389/fmars.2017.00079 (2017).

Article  Google Scholar 

Burns, W. G., Marchetti, A. & Ziervogel, K. Enhanced formation of transparent exopolymer particles (TEP) under turbulence during phytoplankton growth. J. Plankton Res. 41, 349–361. https://doi.org/10.1093/plankt/fbz018 (2019).

CAS  Article  Google Scholar 

Riebesell, U., Reigstad, M., Wassmann, P., Noji, T. & Passow, U. On the trophic fate of Phaeocystis pouchetii (hariot): Significance of Phaeocystis-derived mucus for vertical flux. Neth. J. Sea Res. 33, 193–203. https://doi.org/10.1016/0077-7579(95)90006-3 (1995).

Article  Google Scholar 

Alderkamp, A. C., Buma, A. G. J. & van Rijssel, M. The carbohydrates of Phaeocystis and their degradation in the microbial food web. Biogeochemistry 83, 1–3. https://doi.org/10.1007/s10533-007-9078-2 (2007).

CAS  Article  Google Scholar 

Grossart, H. P., Simon, M. & Logan, B. E. Formation of macroscopic organic aggregates (lake snow) in a large lake: The significance of transparent exopolymer particles, phytoplankton, and zooplankton. Limnol. Oceanogr. 42, 1651–1659. https://doi.org/10.4319/lo.1997.42.8.1651 (1997).

ADS  CAS  Article  Google Scholar 

Iuculano, F., Mazuecos, I. P., Reche, I. & Agusti, S. Prochlorococcus as a possible source for transparent exopolymer particles (TEP). Front. Microbiol. 8, 1–11. https://doi.org/10.3389/fmicb.2017.00709 (2017).

Article  Google Scholar 

Thornton, D. C. O. Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. Eur. J. Phycol. 49, 20–46. https://doi.org/10.1080/09670262.2013.875596 (2014).

CAS  Article  Google Scholar 

Zhang, Z. et al. The fate of marine bacterial exopolysaccharide in natural marine microbial communities. PLoS One 10, 1–16. https://doi.org/10.1371/journal.pone.0142690 (2015).

CAS  Article  Google Scholar 

Xiao, R. & Zheng, Y. Overview of microalgal extracellular polymeric substances (EPS) and their applications. Biotechnol. Adv. 34, 1225–1244. https://doi.org/10.1016/j.biotechadv.2016.08.004 (2016).

CAS  Article  PubMed  Google Scholar 

Thavasi, R. & Banat, I. M. Biosurfactant and bioemulsifiers from marine sources. In Biosurfactants: Research Trends and Applications, ***Chap 5 (eds Mulligan, C. N. et al.) 125–146 (CRC Press, Boca Raton, 2014).

Google Scholar 

Decho, A. W. & Gutierrez, T. Microbial extracellular polymeric substances (EPSs) in ocean systems. Front. Microbiol. 8, 1–28. https://doi.org/10.3389/fmicb.2017.00922 (2017).

Article  Google Scholar 

Parker, C. The effect of environmental stressors on biofilm formation of Chlorella vulgaris. Master thesis Appalachian State University (2013).

Zhou, J., Mopper, K. & Passow, U. The role of surface-active carbohydrates in the formation of transparent exopolymer particles by bubble adsorption of seawater. Limnol. Oceanogr. 43, 1860–1871. https://doi.org/10.4319/lo.1998.43.8.1860 (1998).

ADS  CAS  Article  Google Scholar 

Fukao, T., Kimoto, K. & Kotani, Y. Production of transparent exopolymer particles by four diatom species. Fish Sci. 76, 755–760. https://doi.org/10.1007/s12562-010-0265-z (2010).

CAS  Article  Google Scholar 

Seebah, S., Fairfield, C., Ullrich, M. S. & Passow, U. Aggregation and sedimentation of Thalassiosira weissflogii (diatom) in a warmer and more acidified Future Ocean. PLoS One 9, 1–9. https://doi.org/10.1371/journal.pone.0112379 (2014).

CAS  Article  Google Scholar 

Staats, N., Stal, L. J. & Mur, L. R. Exopolysaccharide production by the epipelic diatom Cylindrotheca fusiformis: Effects of nutrient conditions. J. Exp. Mar. Biol. Ecol. 249, 13–27. https://doi.org/10.1016/S0022-0981(00)00166-0 (2000).

CAS  Article  PubMed  Google Scholar 

Underwood, G. J. C., Boulcott, M., Raines, C. A. & Waldron, K. Environmental effects on exopolymer production by marine benthic diatoms: Dynamics, changes in composition, and pathways of production. J. Phycol. 40, 293–304. https://doi.org/10.1111/j.1529-8817.2004.03076.x (2004).

CAS  Article  Google Scholar 

Engel, A. et al. Impact of CO₂ enrichment on organic matter dynamics during nutrient induced coastal phytoplankton blooms. J. Plankton Res. 36, 641–657. https://doi.org/10.1093/plankt/fbt125 (2014).

CAS  Article  Google Scholar 

Thornton, D. C. O. & Chen, J. Exopolymer production as a function of cell permeability and death in a diatom (Thalassiosira weissflogii) and a cyanobacterium (Synechococcus elongatus). J. Phycol. 53, 245–260. https://doi.org/10.1111/jpy.12470 (2017).

CAS  Article  PubMed  Google Scholar 

Sugimoto, K., Fukuda, H., Abdul Baki, M. & Koike, I. Bacterial contribution to formation of transparent exopolymer particles (TEP) and seasonal trends in coastal waters of Sagami Bay, Japan. Aquat. Microb. Ecol. 46, 31–41. https://doi.org/10.3354/ame046031 (2007).

Article  Google Scholar 

Gordillo, F. J. L., Jiménez, C., Chavarria, J. & Niell, F. X. Photosynthetic acclimation to photon irradiance and its relation to chlorophyll fluorescence and carbon assimilation in the halotolerant green alga Dunaliella viridis. Photosynth. Res. 68, 225–235. https://doi.org/10.1023/a:1012969324756 (2001).

CAS  Article  PubMed  Google Scholar 

Ekelund, N. G. A. & Aronsson, K. A. Changes in chlorophyll a fluorescence in Euglena gracilis and Chlamydomonas reinhardii after exposure to wood-ash. Environ. Exp. Bot. 59, 92–98. https://doi.org/10.1016/j.envexpbot.2005.10.004 (2007).

CAS  Article  Google Scholar 

Cole, J. J. Interactions between bacteria and algae in aquatic ecosystems. Ann. Rev. Ecol. Syst. 13, 291–314. https://doi.org/10.1146/annurev.es.13.110182.001451 (1982).

Article  Google Scholar 

Joint, I. et al. Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquat. Microb. Ecol. 29, 145–159. https://doi.org/10.3354/ame029145 (2002).

Article  Google Scholar 

Amin, S. A., Parker, M. S. & Armbrust, E. V. Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76, 667–684. https://doi.org/10.1128/MMBR.00007-12 (2012).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Ramanan, R., Kim, B. H., Cho, D. H., Oh, H. M. & Kim, H. S. Algae-bacteria interactions: Evolution, ecology and emerging applications. Biotechnol. Adv. 34, 14–29. https://doi.org/10.1016/j.biotechadv.2015.12.003 (2016).

CAS  Article  PubMed  Google Scholar 

Ray, S. & Bagchi, S. N. Nutrients and pH regulate algicide accumulation in cultures of the cyanobacterium Oscillatoria laetevirens. New Phytol. 149, 455–460. https://doi.org/10.1046/j.1469-8137.2001.00061.x (2001).

CAS  Article  Google Scholar 

Oremland, R. S. & Capone, D. G. Use of “specific” inhibitors in biogeochemistry and microbial ecology. Adv. Microb. Ecol. 10, 285–383. https://doi.org/10.1007/978-1-4684-5409-3_8 (1988).

CAS  Article  Google Scholar 

Middelburg, J. J. & Nieuwenhuize, J. Nitrogen uptake by heterotrophic bacteria and phytoplankton in the nitrate-rich Thames estuary. Mar. Ecol. Prog. Ser. 203, 13–21. https://doi.org/10.3354/meps203013 (2000).

ADS  CAS  Article  Google Scholar 

Mulholland, M. R., Rocha, A. M. & Boncillo, G. E. Incorporation of leucine and thymidine by estuarine phytoplankton: Implications for bacteria productivity estimates. Estuar. Coasts 34, 310–325. https://doi.org/10.1007/s12237-010-9366-2 (2010).

CAS  Article  Google Scholar 

Prieto, A. et al. Assessing the role of phytoplankton–bacterioplankton coupling in the response of microbial plankton to nutrient additions. J. Plankton Res. 38, 55–63. https://doi.org/10.1093/plankt/fbv101 (2016).

CAS  Article  Google Scholar 

Dakhama, A., de la Noüe, J. & Lavoie, M. C. Isolation and identification of antialgal substances produced by Pseudomonas aeruginosa. J. Appl. Phycol. 5, 297–306. https://doi.org/10.1007/BF02186232 (1993).

CAS  Article  Google Scholar 

Bowman, L. P. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Mar. Drugs 5, 220–241. https://doi.org/10.3390/md504220 (2007).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Meseck, S. L., Smith, B. C., Wikfors, G. H., Alix, J. H. & Kapareiko, D. Nutrient interactions between phytoplankton and bacterioplankton under different carbon dioxide regimes. J. Appl. Phycol. 19, 229–237. https://doi.org/10.1007/s10811-006-9128-5 (2007).

CAS  Article  Google Scholar 

Guerrini, F., Mazzotti, A., Boni, L. & Pistocchi, R. Bacterial-algal interactions in polysaccharide production. Aquat. Microb. Ecol. 15, 247–253. https://doi.org/10.3354/ame015247 (1998).

Article  Google Scholar 

Lu, X. et al. A marine algicidal Thalassiosira and its active substance against the harmful algal bloom species Karenia mikimotoi. Appl. Microbiol. Biotechnol. 100, 5131–5139. https://doi.org/10.1007/s00253-016-7352-8 (2016).

CAS  Article  PubMed  Google Scholar 

Li, Y. et al. Chitinase producing bacteria with direct algicidal activity on marine diatoms. Sci. Rep. 6, 1–13. https://doi.org/10.1038/srep21984 (2016).

CAS  Article  Google Scholar 

Li, Y. et al. The first evidence of deinoxanthin from Deinococcus sp Y35 with strong algicidal effect on the toxic dinoflagellate Alexandrium tamarense. J. Hazard. Mater. 290, 87–95. https://doi.org/10.1016/j.jhazmat.2015.02.070 (2015).

ADS  CAS  Article  PubMed  Google Scholar 

Lovejoy, C., Bowman, J. P. & Hallegraeff, G. M. Algicidal effects of a novel marine Pseudomonas isolate (class Proteobacteria, gamma subdivision) on harmful algal bloom species of the genera Chattonella, Gymnodinium and Heterosigma. Appl. Environ. Microbiol. 64, 2806–2813 (1998).

CAS  Article  Google Scholar 

Honsell, G. & Talarico, L. Gymnodinium chlorophorum (Dinophyceae) in the Adriatic Sea: Electron microscopical observations. Bot. Mar. 47, 152–166. https://doi.org/10.1515/BOT.2004.016 (2004).

Article  Google Scholar 

Iriarte, J. L., Quiñones, R. A. & González, R. R. Relationship between biomass and enzymatic activity of a bloom-forming dinoflagellate (Dinophyceae) in southern Chile (41°S): A field approach. J. Plankton. Res. 27, 159–161. https://doi.org/10.1093/plankt/fbh167 (2005).

CAS  Article  Google Scholar 

Gárate-Lizárraga, I., Muñetón-Gómez, M. S., Pérez-Cruz, B. & Díaz-Ortíz, J. A. Bloom of Gonyaulax spinifera (Dinophyceae: Gonyaulacales) in Ensenada de la Paz Lagoon, Gulf of California. CICIMAR Oceán. 29, 1–18 (2014).

Google Scholar 

McCarthy, P.M. Census of Australian Marine Dinoflagellates. Australian Biological Resources Study, Canberra. http://www.anbg.gov.au/abrs/Dinoflagellates/index_Dino.html. Accessed 11 July 2013 (2013).

Azam, F. & Smith, D. C. Bacterial influence on the variability in the ocean’s biogeochemical state: A mechanistic view. In Particle Analysis in Oceanography. NATO ASI Series (Series G: Ecological Sciences), ***27 (ed. Demers, S.) (Springer, Berlin, 1991). https://doi.org/10.1007/978-3-642-75121-9_9.

Google Scholar 

Smith, D. C., Steward, G. F., Long, R. A. & Azam, F. Bacterial mediation of carbon fluxes during a diatom bloom in a mesocosm. Deep-Sea Res. 442, 75–97. https://doi.org/10.1016/0967-0645(95)00005-B (1995).

ADS  Article  Google Scholar 

Schuster, S. & Herndl, G. J. Formation and significance of transparent exopolymeric particles in the northern Adriatic Sea. Mar. Ecol. Prog. Ser. 124, 227–236. https://doi.org/10.3354/meps124227 (1995).

ADS  Article  Google Scholar 

Engel, A. & Passow, U. Carbon and nitrogen content of transparent exopolymer particles (TEP) in relation to their Alcian Blue adsorption. Mar. Ecol. Prog. Ser. 219, 1–10. https://doi.org/10.3354/meps219001 (2001).

ADS  CAS  Article  Google Scholar 

Hasui, M., Matsuda, M., Okutani, K. & Shigeta, S. In vitro antiviral activities of sulfated polysaccharides from a marine microalga (Cochlodinium polykrikoides) against human immunodeficiency virus and other enveloped viruses. Int. J. Biol. Macromol. 17, 293–297. https://doi.org/10.1016/0141-8130(95)98157-T (1995).

CAS  Article  PubMed  Google Scholar 

Yim, J. H., Kim, S. J., Ahn, S. H. & Lee, H. K. Characterization of a novel bioflocculant, p-KG03, from a marine dinoflagellate, Gyrodinium impudicum KG03. Bioresour. Technol. 98, 361–367. https://doi.org/10.1016/j.biortech.2005.12.021 (2007).

CAS  Article  PubMed  Google Scholar 

Mandal, S. K., Singh, R. P. & Patel, V. Isolation and characterization of exopolysaccharide secreted by a toxic dinoflagellate, Amphidinium carterae Hulburt 1957 and its probable role in harmful algal blooms (HABs). Microb. Ecol. 62, 518–527. https://doi.org/10.1007/s00248-011-9852-5 (2011).

CAS  Article  PubMed  Google Scholar 

Kesaulya, I., Leterme, S. C., Mitchell, J. G. & Seuront, L. The impact of turbulence and phytoplankton dynamics on foam formation, seawater viscosity and chlorophyll concentration in the eastern English Channel. Oceanologia 50, 167–182 (2008).

Google Scholar 

Seuront, L. & Vincent, D. Increased seawater viscosity, Phaeocystis globosa spring bloom and Temora longicornis feeding and swimming behaviours. Mar. Ecol. Prog. Ser. 363, 131–145. https://doi.org/10.3354/meps07373 (2008).

ADS  CAS  Article  Google Scholar 

Seuront, L., Vincent, D. & Mitchell, J. G. Biologically induced modification of seawater viscosity in the Eastern English Channel during a Phaeocystis globosa spring bloom. J. Mar. Syst. 61, 118–133. https://doi.org/10.1016/j.jmarsys.2005.04.010 (2006).

Article  Google Scholar 

Seuront, L. et al. The influence of Phaeocystis globosa on microscale spatial patterns of chlorophylla and bulk-phase seawater viscosity. Biogeochemistry 83, 173–188. https://doi.org/10.1007/s10533-007-9097-z (2007).

CAS  Article  Google Scholar 

Seuront, L. et al. Role of microbial and phytoplankton communities in the control of seawater viscosity off East Antarctica (30–80° E). Deep-Sea Res. 57, 877–886. https://doi.org/10.1016/j.dsr2.2008.09.018 (2010).

ADS  CAS  Article  Google Scholar 

Stoderegger, K. E. & Herndl, G. J. Production of exopolymer particles by marine bacterioplankton under contrasting turbulence conditions. Mar. Ecol. Prog. Ser. 189, 9–16. https://doi.org/10.3354/meps189009 (1999).

ADS  CAS  Article  Google Scholar 

Alunno-Bruscia, M. et al. A single bio-energetics growth and reproduction model for the oyster Crassostrea gigas in six Atlantic ecosystems. J. Sea Res. 66, 340–348. https://doi.org/10.1016/j.seares.2011.07.008 (2011).

ADS  Article  Google Scholar 

Thomas, Y. et al. Global change and climate-driven invasion of the Pacific oyster (Crassostrea gigas) along European coasts: A bioenergetics modelling approach. J. Biogeogr. 43, 568–579. https://doi.org/10.1111/jbi.12665 (2016).

Article  Google Scholar 

Guillard, R. & Hargraves, P. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32, 234–236. https://doi.org/10.2216/i0031-8884-32-3-234.1 (1993).

Article  Google Scholar 

Scholin, C. A., Herzog, M., Sogin, M. & Anderson, D. M. Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30, 999–1011. https://doi.org/10.1111/j.0022-3646.1994.00999.x (1994).

CAS  Article  Google Scholar 

Nunn, G. B., Theisen, B. F., Christensen, B. & Arctander, P. Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D₃ expansion segment in the crustacean order Isopoda. J. Mol. Evol. 42, 211–223. https://doi.org/10.1007/BF02198847 (1996).

ADS  CAS  Article  PubMed  Google Scholar 

Marie, D., Partensky, F., Jacquet, S. & Vaulot, D. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl. Environ. Microbiol. 63, 186–193. https://doi.org/10.1128/aem.63.1.186-193.1997 (1997).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Wood, A. M., Everroad, R. C. & Wingard, L. M. Measuring growth rates in microalgal cultures. In Algal Culturing Techniques (ed. Anderson, R. A.) 269–285 (Elsevier, Amsterdam, 2005).

Google Scholar 

Kromkamp, J. C. & Forster, R. M. The use of variable fluorescence measurements in aquatic ecosystems: Differences between multiple and single turnover measuring protocols and suggested terminology. Eur. J. Phycol. 38, 103–112. https://doi.org/10.1080/0967026031000094094 (2003).

Article  Google Scholar 

Aminot, A. & Kérouel, R. Dosage Automatique des Nutriments dans les Eaux Marines: Méthodes en flux Continu (in French) (Ed. Ifremer, Plouzané, 2007).

Google Scholar 

Smith, P. K. et al. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76–85. https://doi.org/10.1016/0003-2697(85)90442-7 (1985).

CAS  Article  PubMed  Google Scholar 

Kamerling, J. P., Gerwig, G. J., Vliegenthart, J. F. G. & Clamp, J. R. Characterization by gas-liquid chromatography mass spectrometry of pertrimethylsilyl methyl glycosides obtained in the methanolysis of glycoproteins and glycolipids. Biochem. J. 151, 491–495. https://doi.org/10.1042/bj1510491 (1975).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 22, 680–685. https://doi.org/10.1038/227680a0 (1970).

ADS  Article  Google Scholar 

Rigouin, C., Delbarre Ladrat, C., Sinquin, C., Colliec-Jouault, S. & Dion, M. Assessment of biochemical methods to detect enzymatic depolymerization of polysaccharides. Carbohydr. Polym. 76, 279–284. https://doi.org/10.1016/j.carbpol.2008.10.022 (2009).

CAS  Article  Google Scholar 

Dubray, G. & Bezard, G. A highly sensitive periodic acid-silver stain for 1,2-diol groups of glycoproteins and polysaccharides in polyacrylamide gels. Anal. Biochem. 119, 325–329. https://doi.org/10.1016/0003-2697(82)90593-0 (1982).

CAS  Article  PubMed  Google Scholar 

Aminot, A. & Kérouel, R. Hydrologie des Écosystèmes Marins: Paramètres et Analyses (in French) (Ed Ifremer, Plouzané, 2004).

Google Scholar 

R Core Team R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org (2018).

Lê, S., Josse, J. & Husson, F. FactoMineR: An R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).

Article  Google Scholar