Transparent exopolymer particles (TEP), phytoplankton and picocyanobacteria along a littoral-to-pelagic depth-gradient in a large subalpine lake

Submitted: 12 April 2021
Accepted: 15 May 2021
Published: 13 July 2021
Abstract Views: 920
PDF: 196
Supplementary: 53
HTML: 40
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

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.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

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: https://doi.org/10.1093/plankt/20.3.393
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: https://doi.org/10.1016/0967-0637(93)90129-Q
Ambrosetti W, Barbanti L, Sala N, 2003. Residence time and physical processes in lakes. J. Limnol. 62:s1.1. DOI: https://doi.org/10.4081/jlimnol.2003.s1.1
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: https://doi.org/10.1111/j.1462-2920.2007.01257.x
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: https://doi.org/10.5194/bg-13-3793-2016
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: https://doi.org/10.4081/jlimnol.2016.1374
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: https://doi.org/10.1007/s10750-010-0150-x
Bidle KD, 2015. The molecular ecophysiology of programmed cell death in marine phytoplankton. Annu. Rev. Mar. Sci. 7:341–375. DOI: https://doi.org/10.1146/annurev-marine-010213-135014
Bittar TB, Vieira AAH, 2010. Transparent exopolymer particles formation from capsules of Anabaena Spiroides (cyanobacteria) in culture1. J. Phycol. 46:243–247. DOI: https://doi.org/10.1111/j.1529-8817.2009.00802.x
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: https://doi.org/10.1093/femsec/fiw154
Callieri C, Bertoni R, Contesini M, Bertoni F, 2014. Lake level fluctuations boost toxic cyanobacterial “oligotrophic blooms.” PLoS One 9:e109526. DOI: https://doi.org/10.1371/journal.pone.0109526
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: https://doi.org/10.1080/20442041.2017.1294384
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: https://doi.org/10.1007/978-94-007-3855-3_8
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: https://doi.org/10.4081/jlimnol.2019.1907
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: https://doi.org/10.1093/plankt/fbi038
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: https://doi.org/10.1007/s00027-010-0147-6
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: https://doi.org/10.3354/ame01803
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: https://doi.org/10.1038/nature02453
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: https://doi.org/10.1073/pnas.1307701110
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: https://doi.org/10.1093/plankt/24.8.817
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: https://doi.org/10.1038/ismej.2010.145
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: https://doi.org/10.1007/8623_2015_139
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: https://doi.org/10.1016/S0304-4165(89)80016-9
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: https://doi.org/10.3354/ame014059
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: https://doi.org/10.1111/j.1462-2920.2006.00999.x
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: https://doi.org/10.4319/lo.1997.42.8.1651
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: https://doi.org/10.3354/ame015115
Grossart H-P, Simon M, 1998b. Bacterial colonization and microbial decomposition of limnetic organic aggregates (lake snow). Aquat. Microb. Ecol. 15:127–140. DOI: https://doi.org/10.3354/ame015127
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: https://doi.org/10.3354/ame047163
Iuculano F, Mazuecos IP, Reche I, Agustí S, 2017. Prochlorococcus as a Possible Source for Transparent Exopolymer Particles (TEP). Front. Microbiol. 8:709. DOI: https://doi.org/10.3389/fmicb.2017.00709
Kuznetsova A, Brockhoff PB, Christensen RHB, 2017. lmerTest Package: Tests in Linear Mixed Effects Models. J. Stat. Soft. 82:1–26. DOI: https://doi.org/10.18637/jss.v082.i13
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: https://doi.org/10.1080/02705060.2017.1391722
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: https://doi.org/10.1007/978-90-481-9268-7_13
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: https://doi.org/10.1007/s10750-012-1094-0
Nissimov JI, Bidle KD, 2017. Stress, death, and the biological glue of sinking matter. J. Phycol. 53:241–244. DOI: https://doi.org/10.1111/jpy.12506
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: https://doi.org/10.1007/s00248-010-9640-7
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: https://doi.org/10.1016/j.marchem.2009.06.004
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: https://doi.org/10.5194/bg-6-3071-2009
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: https://doi.org/10.1007/s10452-015-9550-3
Passow U, 2000. Formation of transparent exopolymer particles, TEP, from dissolved precursor material. Mar. Ecol. Prog. Ser. 192:1–11. DOI: https://doi.org/10.3354/meps192001
Passow U, 2002a. Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr. 55:287–333. DOI: https://doi.org/10.1016/S0079-6611(02)00138-6
Passow U, 2002b. Production of transparent exopolymer particles (TEP) by phyto- and bacterioplankton. Mar. Ecol. Prog. Ser. 236:1–12. DOI: https://doi.org/10.3354/meps236001
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: https://doi.org/10.3354/meps113185
Passow U, Alldredge AL, 1995. A dye‐binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol. Oceanogr. 40:1326–1335. DOI: https://doi.org/10.4319/lo.1995.40.7.1326
Passow U, Carlson CA, 2012. The biological pump in a high CO2 world. Mar. Ecol. Prog. Ser. 470:249–271. DOI: https://doi.org/10.3354/meps09985
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: https://doi.org/10.3354/meps104153
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: https://doi.org/10.3354/meps08840
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: https://doi.org/10.1016/j.dsr2.2006.03.009
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: https://doi.org/10.1093/plankt/23.5.515
R Core Team, 019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: https://www.R‐project.org/
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: https://doi.org/10.1007/s10750-018-3623-y
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: https://doi.org/10.1016/j.jglr.2020.01.017
Salmaso N, Mosello R, 2010. Limnological research in the deep southern subalpine lakes: synthesis, directions and perspectives. Adv. Oceanogr. Limnol. 1:5294. DOI: https://doi.org/10.4081/aiol.2010.5294
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: https://doi.org/10.1007/BF00024185
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: https://doi.org/10.3354/meps124227
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: https://doi.org/10.1126/science.201.4353.371
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: https://doi.org/10.3389/fmicb.2011.00229
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: https://doi.org/10.1016/S0967-0637(02)00015-8
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: https://doi.org/10.1007/s10750-015-2506-8
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: https://doi.org/10.3354/meps07830
Thornton DCO, 2004. Formation of transparent exopolymeric particles (TEP) from macroalgal detritus. Mar. Ecol. Prog. Ser. 282:1–12. DOI: https://doi.org/10.3354/meps282001
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: https://doi.org/10.1111/jpy.12470
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: https://doi.org/10.1016/j.marchem.2004.06.017
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: https://doi.org/10.1016/j.scitotenv.2019.06.524
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: https://doi.org/10.5194/bg-16-733-2019

How to Cite

Callieri, Cristiana, J. Salvador Hernández-Avilés, Ester M. Eckert, Michela Rogora, Gabriele Tartari, Tommaso Sforzi, Raffaella Sabatino, and Roberto Bertoni. 2021. “Transparent Exopolymer Particles (TEP), Phytoplankton and Picocyanobacteria Along a Littoral-to-Pelagic Depth-Gradient in a Large Subalpine Lake”. Journal of Limnology 80 (3). https://doi.org/10.4081/jlimnol.2021.2021.

List of Cited By :

Crossref logo