Transparent Exopolymer Particles (TEP), phytoplankton and picocyanobacteria a littoral-to-pelagic depth-gradient in a large subalpine lake


  • Cristiana Callieri | National Research Council, Water Research Institute CNR-IRSA, Verbania, Italy.
  • J. Salvador Hernández-Avilés Laboratory of Limnology, UMIEZ, Biology Department, FES Zaragoza, Universidad Nacional Autónoma de México, Mexico City, Mexico.
  • Ester M. Eckert National Research Council, Water Research Institute CNR-IRSA, Verbania, Italy.
  • Michela Rogora National Research Council, Water Research Institute CNR-IRSA, Verbania, Italy.
  • Gabriele Tartari National Research Council (CNR), Water Research Institute (IRSA), Verbania, Italy, Italy.
  • Tommaso Sforzi National Research Council, Water Research Institute CNR-IRSA, Verbania, Italy.
  • Raffaella Sabatino National Research Council, Water Research Institute CNR-IRSA, Verbania, Italy.
  • Roberto Bertoni National Research Council, Water Research Institute CNR-IRSA, Verbania, Italy.


Transparent Exopolymer Particles (TEP) play an important role in the organic carbon cycle of many aquatic systems but the production and distribution of TEP have been studied mainly in the marine environment, neglecting the large oligotrophic lakes. We selected Lake Maggiore, one of the most important freshwater reserve in Northern Italy, to study the horizontal and vertical distribution of TEP and of its possible drivers. Samplings along a transect in the Borromeo basin were performed in May, July and September 2019. Total Organic Carbon (TOC), TEP, chlorophyll-a (Chl) of different algal groups, picocyanobacteria, bacteria and eukaryotes counting, were measured at six stations and five depths. Our study showed that TEP exhibited a clear vertical heterogeneity from surface to the bottom related to the autotrophic microorganisms that are the main source of TEP and are prevalent in the euphotic zone of the lake. On the other hand, TEP was fairly evenly distributed along the horizontal transect from littoral to pelagic zone, although patches were present in spring, when TEP concentrations were low. In contrast to TEP, TOC and to a lesser extent Chl and bacteria showed horizontal heterogeneity, in some months. In Lake Maggiore TEP indeed was an important fraction of Total Organic Carbon (TOC), making up to 54% of TOC (in carbon units: 910 µg C L-1) and it was significantly correlated with Chl. The highest TEP concentration (1.44 mg GX eq L-1) was measured in September 2019, in coincidence with an episode of superficial foam appearance. Considering the biomass as Chl concentrations, the algal group mostly related to TEP was that of brown algae, particularly diatoms; but considering the numbers, the picocyanobacteria and bacteria were more significantly correlated to TEP. The presence of pennate diatoms in May and July, with their TEP-related chlorophyll, did not produce TEP in as high concentration as that observed in September in the presence of centric diatoms and of very high numbers of picocyanobacteria and bacteria.



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Alldredge AL, Passow U, Haddock HD, 1998. The characteristics and transparent exopolymer particle (TEP) content of marine snow formed from thecate dinoflagellates. J. Plankton Res. 20:393–406. DOI:

Alldredge AL, Passow U, Logan BE, 1993. The abundance and significance of a class of large, transparent organic particles in the ocean. Deep Sea Res. Part I Oceanogr. Res. Pap. 40:1131–1140. DOI:

Ambrosetti W, Barbanti L, Sala N, 2003. Residence time and physical processes in lakes. J. Limnol. 62:s1.1. DOI:

American Public Health Association, American Water Works Association, Water Environment Federation (eds.), 2012. Standard Methods for the Examination of Water and Wastewater., Washington: American Public Health Association; 1120 pp.

Agenzia per la Protezione dell’Ambiente e per i Servizi Tecnici, Istituto di Ricerca sulle Acque -­‐ Consiglio Nazionale delle Ricerche, 2003. [Metodi analitici per le acque].[in Italian].APAT, Roma.

Austoni M, Eckert EM, Sforzi T, Marchetto A, 2020. [Struttura delle associazioni fitoplanctoniche nel Lago Maggiore e loro modificazioni in relazione a fattori di controllo trofici e climatici], p. 62–70 In: CNR IRSA (ed.), [Ricerche sull’evoluzione del Lago Maggiore. Aspetti limnologici. Programma triennale 2019‐2021. Campagna 2019].[Book in Italian]. Commissione Internazionale per la Protezione delle Acque Italo‐Svizzere.

Berman‐Frank I, Rosenberg G, Levitan O, Haramaty L, Mari X, 2007. Coupling between autocatalytic cell death and transparent exopolymeric particle production in the marine cyanobacterium Trichodesmium. Environ. Microbiol. 9:1415–1422. DOI:

Berman‐Frank I, Spungin D, Rahav E, Van Wambeke F, Turk-Kubo K, Moutin T, 2016. Dynamics of transparent exopolymer particles (TEP) during the VAHINE mesocosm experiment in the New Caledonian lagoon. Biogeosciences 13:3793–3805. DOI:

Bertoni R, Bertoni M, Morabito G, Rogora M, Callieri C, 2016. A non-­‐deterministic approach to forecasting the trophic evolution of lakes. J. Limnol. 75:1374. DOI:

Bertoni R, Callieri C, Corno G, Rasconi S, Caravati E, Contesini M, 2010. Long‐term trends of epilimnetic and hypolimnetic bacteria and organic carbon in a deep holo‐oligomictic lake. Hydrobiologia 644:279–287. DOI:

Bidle KD, 2015. The molecular ecophysiology of programmed cell death in marine phytoplankton. Annu. Rev. Mar. Sci. 7:341–375. DOI:

Bittar TB, Vieira AAH, 2010. Transparent exopolymer particles formation from capsules of Anabaena Spiroides (cyanobacteria) in culture1. J. Phycol. 46:243–247. DOI:

Callieri C, Amalfitano S, Corno G, Bertoni R, 2016. Grazing-­‐induced Synechococcus microcolony formation: experimental insights from two freshwater phylotypes. FEMS Microbiol. Ecol. 92. DOI:

Callieri C, Bertoni R, Contesini M, Bertoni F, 2014. Lake level fluctuations boost toxic cyanobacterial “oligotrophic blooms.” PLoS One 9:e109526. DOI:

Callieri C, Bertoni R, Crippa E, Contesini M, Di Cesare A, Eckert EM, 2019a. [Il carbonio organico nel Lago Maggiore: tendenza evolutiva, origine e caratteristiche qualitative], p. 77–84 In: CNR IRSA (ed.), Ricerche sull’evoluzione del Lago Maggiore. Aspetti Limnologici. Programma Triennale 2016‐2018. Campagna 2018 e Rapporto Triennale 2016-­‐2018].[Book in Italian]. Commissione Internazionale per la protezione delle acque italo‐svizzere.

Callieri C, Corno G, Contesini M, Fontaneto D, Bertoni R, 2017. Transparent exopolymer particles (TEP) are driven by chlorophyll a and mainly confined to the euphotic zone in a deep subalpine lake. Inland Waters 7:118–127. DOI:

Callieri C, Cronberg G, Stockner JG, 2012. Freshwater picocyanobacteria: Single cells, microcolonies and colonial forms, p. 229-269 In: Whitton BA (ed.), Ecology of cyanobacteria II: Their diversity in space and time. Dordrecht: Springer. DOI:

Callieri C, Sathicq MB, Cabello-Yeves PJ, Eckert EM, Hernández-­‐Avilés JS, 2019b. TEP production under oxidative stress of the picocyanobacterium Synechococcus. J. Limnol. 78:1907. DOI:

CNR IRSA Verbania, 2020. [Ricerche sull’evoluzione del Lago Maggiore. Aspetti limnologici. Programma triennale 2019-2021. Campagna 2019].[Book in Italian]. Commissione Internazionale per la protezione delle acque italo‐svizzere: 110 pp.

Corzo A, Rodríguez‐Gálvez S, Lubian L, Sangrá P, Martínez A, Morillo JA, 2005. Spatial distribution of transparent exopolymer particles in the Bransfield Strait, Antarctica. J. Plankton Res. 27:635–646. DOI:

de Vicente I, Ortega‐Retuerta E, Mazuecos IP, Pace ML, Cole JJ, Reche I, 2010. Variation in transparent exopolymer particles in relation to biological and chemical factors in two contrasting lake districts. Aquat. Sci. 72:443–453. DOI:

Deng W, Cruz BN, Neuer S, 2016. Effects of nutrient limitation on cell growth, TEP production and aggregate formation of marine Synechococcus. Aquat. Microb. Ecol. 78:39–49. DOI:

Engel A, Thoms S, Riebesell U, Rochelle-­‐Newall E, Zondervan I, 2004. Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. Nature 428:929–932. DOI:

Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N, Karl DM, Li WKW, Lomas MW, Veneziano D, Vera CS, Vrugt JA, et al., 2013. Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. PNAS 110:9824–9829. DOI:

Fox J, Weisberg S, 2019. An R Companion to Applied Regression. Los Angeles: SAGE; 577 pp.

García CM, Prieto L, Vargas M, Echevarría F, García-Lafuente J, Ruiz J, Rubín JP, 2002. Hydrodynamics and the spatial distribution of plankton and TEP in the Gulf of Cádiz (SW Iberian Peninsula). J. Plankton Res. 24:817–833. DOI:

Gärdes A, Iversen MH, Grossart H‐P, Passow U, Ullrich MS, 2011. Diatom-associated bacteria are required for aggregation of Thalassiosira weissflogii. ISME J. 5:436–445. DOI:

Gasol JM, Morán XAG, 2015. Flow cytometric determination of microbial abundances and its use to obtain indices of community structure and relative activity, p. 159–187. In: McGenity TJ, KN Timmis, and B Nogales (eds.), Hydrocarbon and lipid microbiology protocols. Berlin: Springer. DOI:

Genty B, Briantais J-M, Baker NR, 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA - Gen. Subjects 990:87–92. DOI:

Grossart H-P, Berman T, Simon M, Pohlmann K, 1998. Occurrence and microbial dynamics of macroscopic organic aggregates (lake snow) in Lake Kinneret, Israel, in fall. Aquat. Microb. Ecol. 14:59–67. DOI:

Grossart H-P, Czub G, Simon M, 2006. Algae–bacteria interactions and their effects on aggregation and organic matter flux in the sea. Environ. Microbiol. 8:1074–1084. DOI:

Grossart H-P, Simon M, Logan BE, 1997. 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. DOI:

Grossart H-P, Simon M, 1998a. Significance of limnetic organic aggregates (lake snow) for the sinking flux of particulate organic matter in a large lake. Aquat. Microb. Ecol. 15:115–125. DOI:

Grossart H-P, Simon M, 1998b. Bacterial colonization and microbial decomposition of limnetic organic aggregates (lake snow). Aquat. Microb. Ecol. 15:127–140. DOI:

Grossart H-P, Simon M, 2007. Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics. Aquat. Microb. Ecol. 47:163–176. DOI:

Iuculano F, Mazuecos IP, Reche I, Agustí S, 2017. Prochlorococcus as a Possible Source for Transparent Exopolymer Particles (TEP). Front. Microbiol. 8:709. DOI:

Kuznetsova A, Brockhoff PB, Christensen RHB, 2017. lmerTest Package: Tests in Linear Mixed Effects Models. J. Stat. Soft. 82:1–26. DOI:

Liu L, Huang Q, Qin B, 2018. Characteristics and roles of Microcystis extracellular polymeric substances (EPS) in cyanobacterial blooms: a short review. J. Freshwater Ecol. 33:183–193. DOI:

Masojídek J, Vonshak A, Torzillo G, 2010. Chlorophyll Fluorescence Applications in Microalgal Mass Cultures, p. 277–292 In: DJ Suggett, O Prášil, and MA Borowitzka (eds.), Chlorophyll a fluorescence in aquatic sciences: Methods and applications. Dordrecht: Springer. DOI:

Morabito G, Oggioni A, Austoni M, 2012. Resource ratio and human impact: how diatom assemblages in Lake Maggiore responded to oligotrophication and climatic variability. Hydrobiologia. 698:47-­‐60. DOI:

Nissimov JI, Bidle KD, 2017. Stress, death, and the biological glue of sinking matter. J. Phycol. 53:241–244. DOI:

Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H, 2019. Vegan: Community Ecology Package. R package version 2.5‐6.

Ortega‐Retuerta E, Duarte CM, Reche I, 2010. Significance of bacterial activity for the distribution and dynamics of transparent exopolymer particles in the Mediterranean Sea. Microb. Ecol. 59:808–818. DOI:

Ortega-Retuerta E, Reche I, Pulido‐Villena E, Agustí S, Duarte CM, 2009a. Uncoupled distributions of transparent exopolymer particles (TEP) and dissolved carbohydrates in the Southern ocean. Mar. Chem. 115:59–65. DOI:

Ortega-Retuerta E, Passow U, Duarte CM, Reche I, 2009b. Effects of ultraviolet B radiation on (not so) transparent exopolymer particles. Biogeosciences 6:3071‐3080. DOI:

Pannard A, Pédromo J, Bormans M, Briand E, Claquim P, Lagadeuc Y, 2016. Production of exopolymers (EPS) by cyanobacteria: impact on the carbon‐to-nutrient ratio of the particulate organic matter. Aquat. Ecol. 50:29–44. DOI:

Passow U, 2000. Formation of transparent exopolymer particles, TEP, from dissolved precursor material. Mar. Ecol. Prog. Ser. 192:1–11. DOI:

Passow U, 2002a. Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr. 55:287–333. DOI:

Passow U, 2002b. Production of transparent exopolymer particles (TEP) by phyto- and bacterioplankton. Mar. Ecol. Prog. Ser. 236:1–12. DOI:

Passow U, Alldredge AL, 1994. Distribution, size and bacterial colonization of transparent exopolymer particles (TEP) in the ocean. Mar. Ecol. Prog. Ser. 113:185–198. DOI:

Passow U, Alldredge AL, 1995. A dye‐binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol. Oceanogr. 40:1326–1335. DOI:

Passow U, Carlson CA, 2012. The biological pump in a high CO2 world. Mar. Ecol. Prog. Ser. 470:249–271. DOI:

Passow U, Wassmann P, 1994. On the trophic fate of Phaeocystis pouchetii (Hariot): IV. The formation of marine snow by P. pouchetii. Mar. Ecol. Prog. Ser. 104:153–161. DOI:

Pedrotti ML, Peters F, Beauvais S, Vidal M, Egge J, Jacobsen A, Marrasé C, 2010. Effects of nutrients and turbulence on the production of transparent exopolymer particles: a mesocosm study. Mar. Ecol. Prog. Ser. 419:57–69. DOI:

Prieto L, Navarro G, Cózar A, Echevarría F, García CM, 2006. Distribution of TEP in the euphotic and upper mesopelagic zones of the southern Iberian coasts. Deep Sea Res. Part II Top. Stud. Oceanogr. 53:1314–1328. DOI:

Prieto L, Sommer F, Stibor H, Koeve W, 2001. Effects of Planktonic Copepods on Transparent Exopolymeric Particles (TEP) Abundance and Size Spectra. J. Plankton Res. 23:515–525. DOI:

R Core Team, 019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: https://www.R‐

Rogora M, Buzzi F, Dresti C, Leoni B, Lepori F, Mosello R, Patelli M, Salmaso N, 2018. Climatic effects on vertical mixing and deep-water oxygen content in the subalpine lakes in Italy. Hydrobiologia 824:33–50. DOI:

Rogora M, Giacomotti P, Mosello R, Orrù A, Tartari GA, 2019. [Evoluzione stagionale e a lungo termine delle caratteristiche chimiche del Lago Maggiore e bilancio dei nutrienti a lago (azoto e fosforo)], p. 31–54 In: CNR IRSA. Sede di Verbania (ed.), [Ricerche sull’evoluzione del Lago Maggiore. Aspetti limnologici. Programma triennale 2016 – 2018. Campagna 2018 e rapporto triennale 2016‐18].[Book in Italian]. Commissione Internazionale per la protezione delle acque italo-svizzere.

Salmaso N, Buzzi F, Capelli C, Cerasino L, Leoni B, Lepori F, Rogora M, 2020. Responses to local and global stressors in the large southern perialpine lakes: Present status and challenges for research and management. J. Great Lakes Res. 46:752–766. DOI:

Salmaso N, Mosello R, 2010. Limnological research in the deep southern subalpine lakes: synthesis, directions and perspectives. Adv. Oceanogr. Limnol. 1:5294. DOI:

Schreiber U, Schliwa U, Bilger W, 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10:51–62. DOI:

Schuster S, Herndl G, 1995. Formation and significance of transparent exopolymeric particles in the northern Adriatic Sea. Mar. Ecol. Prog. Ser. 124:227–236. DOI:

Silver MW, Shanks AL, Trent JD, 1978. Marine snow: Microplankton habitat and source of small- scale patchiness in pelagic populations. Science 201:371–373. DOI:

Sohm JA, Edwards BR, Wilson BG, Webb EA, 2011. Constitutive Extracellular Polysaccharide (EPS) production by specific isolates of Crocosphaera watsonii. Front. Microbiol. 2:229. DOI:

Sosik HM, Olson RJ, 2002. Phytoplankton and iron limitation of photosynthetic efficiency in the Southern Ocean during late summer. Deep Sea Res. Part I Oceanogr. Res. Pap. 49:1195-1216. DOI:

Stefani F, Salerno F, Copetti D, Rabuffetti D, Guidetti L, Torri G, Naggi A, Iacomini M, Morabito G, Guzzella L, 2016. Endogenous origin of foams in lakes: a long-term analysis for Lake Maggiore (northern Italy). Hydrobiologia 767:249–265. DOI:

Suggett DJ, Moore CM, Hickman AE, Geider RJ, 2009. Interpretation of fast repetition rate (FRR) fluorescence: signatures of phytoplankton community structure versus physiological state. Mar. Ecol. Prog. Ser. 376:1-19. DOI:

Thornton DCO, 2004. Formation of transparent exopolymeric particles (TEP) from macroalgal detritus. Mar. Ecol. Prog. Ser. 282:1–12. DOI:

Thornton DCO, Chen J, 2017. 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. DOI:

Verdugo P, Alldredge AL, Azam F, Kirchman DL, Passow U, Santschi PH, 2004. The oceanic gel phase: a bridge in the DOM–POM continuum. Mar. Chem. 92:67-85. DOI:

Zamanillo M, Ortega‐Retuerta E, Nunes S, Estrada M, Sala MM, Royer S‐J, López‐Sandoval DC, Emelianov M, Vaqué D, Marrasé C, Simó R, 2019a. Distribution of transparent exopolymer particles (TEP) in distinct regions of the Southern Ocean. Sci. Total Environ. 691:736–748. DOI:

Zamanillo M, Ortega-Retuerta E, Nunes S, Rodríguez‐Ros P, Dall’Osto M, Estrada M, Montserrat Sala M, Simó R, 2019b. Main drivers of transparent exopolymer particle distribution across the surface Atlantic Ocean. Biogeosciences 16:733-749. DOI:

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TEP horizontal distribution, picocyanobacteria and phytoplankton distribution, Lake Maggiore, littoral-pelagic samples
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How to Cite
Callieri C, Hernández-Avilés JS, Eckert EM, Rogora M, Tartari G, Sforzi T, Sabatino R, Bertoni R. Transparent Exopolymer Particles (TEP), phytoplankton and picocyanobacteria a littoral-to-pelagic depth-gradient in a large subalpine lake. J Limnol [Internet]. 2021 Jul. 13 [cited 2021 Jul. 28];. Available from:

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