Abstract
The study of transparent exopolymer particles (TEP) in the Mediterranean Sea is particularly relevant as they can be promoters of mucilage events, a frequent phenomenon there. We assessed the influence of bacterioplankton on TEP distribution and dynamics across the west–east axis of the Mediterranean Sea. We performed an extensive study of TEP, dissolved carbohydrates, and their relationships with bacterial abundance and bacterial production (BP). A significant and positive relationship was observed between BP and TEP in the study region (r 2 = 0.51, p < 0.001). The direct release of TEP by bacteria was experimentally corroborated using regrowth cultures where increases in TEP tracked bacterial growth in abundance and production. These TEP increases were positively related to the increases in BP (r 2 = 0.78, p < 0.05). The consistency (similar slopes) of the regression lines between BP and TEP in natural conditions and between the increases of BP and TEP in the experiments underlines the relevant role of bacteria in the formation of TEP in this area.
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References
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 40:1131–1140
Azetsu-Scott K, Passow U (2004) Ascending marine particles: significance of transparent exopolymer particles (TEP) in the upper ocean. Limnol Oceanogr 49:741–748
Bar-Zeev E, Berman-Frank I, Stambler N, Vazquez-Dominguez E, Zohary T, Capuzzo E, Meeder E, Suggett DJ, Iluz D, Dishon G, Berman T (2009) Transparent exopolymer particles (TEP) link phytoplankton and bacterial production in the Gulf of Aqaba. Aquat Microb Ecol 56:217–225
Beauvais S, Pedrotti ML, Villa E, Lemée R (2003) Transparent exopolymer particle (TEP) dynamics in relation to trophic and hydrological conditions in the NW Mediterranean Sea. Mar Ecol Prog Ser 262:97–109
Berman T, Viner-Mozzini Y (2001) Abundance and characteristics of polysaccharide and proteinaceous particles in Lake Kinneret. Aquat Microb Ecol 24:255–264
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
Calleja ML, Duarte CM, Prairie YT, Agusti S, Herndl GJ (2009) Evidence for surface organic matter modulation of air–sea CO2 gas exchange. Biogeosciences 6:1105–1114
Calvo S, Barone R, Naselli-Flores L (1995) Observations on mucus aggregates along Sicilian coasts during 1991–1992. Sci Total Environ 165:23–31
Corzo A, Morillo JA, Rodriguez S (2000) Production of transparent exopolymer particles (TEP) in cultures of Chaetoceros calcitrans under nitrogen limitation. Aquat Microb Ecol 23:63–72
Costerton JW, Geesey GG, Cheng KJ (1978) How bacteria stick. Sci Am 238:86–95
Degobbis D (1989) Increased eutrophication of the Northern Adriatic Sea—2nd act. Mar Pollut Bull 20:452–457
del Giorgio P, Bird DF, Prairie YT, Planas D (1996) Flow cytometric determination of bacterial abundance in lake plankton with the green nucleic acid stain SYTO 13. Limnol Oceanogr 41:783–789
Ding YX, Chin WC, Rodriguez A, Hung CC, Santschi PH, Verdugo P (2008) Amphiphilic exopolymers from Sagittula stellata induce DOM self-assembly and formation of marine microgels. Mar Chem 112:11–19
Engel A, Passow U (2001) Carbon and nitrogen content of transparent exopolymer particles (TEP) in relation to their alcian blue adsorption. Mar Ecol Prog Ser 219:1–10
Gasol JM, Del Giorgio PA (2000) Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci Mar 64:197–224
Gasol JM, Moran XAG (1999) Effects of filtration on bacterial activity and picoplankton community structure as assessed by flow cytometry. Aquat Microb Ecol 16:251–264
Grossart HP, 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
Grossart HP, Simon M (2007) Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics. Aquat Microb Ecol 47:163–176
Guerrini F, Mazzotti A, Boni L, Pistocchi R (1998) Bacterial–algal interactions in polysaccharide production. Aquat Microb Ecol 15:247–253
Harlay J, De Bodt C, Engel A, Jansen S, d'Hoop Q, Piontek J, Van Oostende N, Groom S, Sabbe K, Chou L (2009) Abundance and size distribution of transparent exopolymer particles (TEP) in a coccolithophorid bloom in the northern Bay of Biscay. Deep-Sea Res Part I Oceanogr Res Pap 56:1251–1265
Hong Y, Smith WO, White AM (1997) Studies on transparent exopolymer particles (TEP) produced in the Ross Sea (Antarctica) and by Phaeocystis antarctica (Prymnesiophyceae). J Phycol 33:368–376
Hung CC, Guo LD, Santschi PH, Alvarado-Quiroz N, Haye JM (2003) Distributions of carbohydrate species in the Gulf of Mexico. Mar Chem 81:119–135
Johnson BD, Kepkay PE (1992) Colloid transport and bacterial utilization of oceanic Doc. Deep-Sea Res 39:855–869
Kirchman DL (1994) The uptake of inorganic nutrients by heterotrophic bacteria. Microb Ecol 28:255–271
Kirchman DL, Ducklow HW (1993) Estimating conversion factors for the thymidine and leucine methods for measuring bacterial production. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods on aquatic microbial ecology. Lewis, Boca Raton, pp 513–517
Logan BE, Passow U, Alldredge AL, Grossart HP, Simon M (1995) Rapid formation and sedimentation of large aggregates is predictable from coagulation rates (half-lives) of transparent exopolymer particles (TEP). Deep-Sea Res II 42:203–214
Mari X (2008) Does ocean acidification induce an upward flux of marine aggregates? Biogeosciences 5:1023–1031
Mari X, Beauvais S, Lemee R, Pedrotti ML (2001) Non-Redfield C:N ratio of transparent exopolymeric particles in the northwestern Mediterranean Sea. Limnol Oceanogr 46:1831–1836
Mari X, Kiorboe T (1996) Abundance, size distribution and bacterial colonization of transparent exopolymeric particles (TEP) during spring in the Kattegat. J Plankton Res 18:969–986
Mari X, Rassoulzadegan F, Brussaard CPD, Wassmann P (2005) Dynamics of transparent exopolymeric particles (TEP) production by Phaeocystis globosa under N- or P-limitation: a controlling factor of the retention/export balance. Harmful Algae 4:895–914
Mecozzi M, Acquistucci R, Di Noto V, Pietrantonio E, Amici M, Cardarilli D (2001) Characterization of mucilage aggregates in Adriatic and Tyrrhenian Sea: structure similarities between mucilage samples and the insoluble fractions of marine humic substance. Chemosphere 44:709–720
Momzikoff A, Brinis A, Dallot S, Gondry G, Saliot A, Lebaron P (2004) Field study of the chemical characterization of the upper ocean surface using various samplers. Limnol Oceanogr Meth 2:374–386
Myklestad S, Skanoy E, Hestmann S (1997) A sensitive and rapid method for analysis of dissolved mono- and polysaccharides in seawater. Mar Chem 56:279–286
Obernosterer I, Herndl GJ (1995) Phytoplankton extracellular release and bacterial-growth: dependence on the inorganic N:P ratio. Mar Ecol Prog Ser 116:247–257
Ortega-Retuerta E, Passow U, Duarte CM, Reche I (2009) Effects of ultraviolet B radiation on (not so) transparent exopolymer particles. Biogeosciences 6:3071–3080
Ortega-Retuerta E, Reche I, Pulido-Villena E, Agustí S, Duarte CM (2009) Uncoupled distributions of transparent exopolymer particles (TEP) and dissolved carbohydrates in the Southern Ocean. Mar Chem 115:59–65
Pakulski D, Benner R (1994) Abundance and distribution of carbohydrates in the ocean. Limnol Oceanogr 39:930–940
Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for sea water analysis. Pergamon, Oxford
Passow U (2000) Formation of transparent exopolymer particles, TEP, from dissolved precursor material. Mar Ecol Prog Ser 192:1–11
Passow U (2002) Production of transparent exopolymer particles (TEP) by phyto- and bacterioplankton. Mar Ecol Prog Ser 236:1–12
Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environments. Progr Oceanogr 55:287–333
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
Passow U, Alldredge AL (1995) A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol Oceanogr 40:1326–1335
Passow U, Shipe RF, Murray A, Pak DK, Brzezinski MA, Alldredge AL (2001) The origin of transparent exopolymer particles (TEP) and their role in the sedimentation of particulate matter. Cont Shelf Res 21:327–346
Prieto L, Navarro G, Cozar A, Echevarria F, Garcia CM (2006) Distribution of TEP in the euphotic and upper mesopelagic zones of the southern Iberian coasts. Deep-Sea Res II 53:1314–1328
Prieto L, Sommer F, Stibor HN, Koeve W (2001) Effects of planktonic copepods on transparent exopolymeric particles (TEP) abundance and size spectra. J Plankton Res 23:515–525
Radic T, Ivancic I, Fuks D, Radic J (2006) Marine bacterioplankton production of polysaccharidic and proteinaceous particles under different nutrient regimes. FEMS Microbiol Ecol 58:333–342
Riebesell U, Reigstad M, Wassmann P, Noji T, Passow U (1995) On the trophic fate of Phaeocystis pouchetii (Hariot). VI. Significance of Phaeocystis-derived mucus for vertical flux. Neth J Sea Res 33:193–203
Sala MM, Peters F, Gasol JM, Pedros-Alio C, Marrase C, Vaque D (2002) Seasonal and spatial variations in the nutrient limitation of bacterioplankton growth in the northwestern Mediterranean. Aquat Microb Ecol 27:47–56
Schuster S, Herndl GJ (1995) Formation and significance of transparent exopolymeric particles in the Northern Adriatic Sea. Mar Ecol Prog Ser 124:227–236
Shibata A, Kogure K, Koike I, Ohwada K (1997) Formation of submicron colloidal particles from marine bacteria by viral infection. Mar Ecol Prog Ser 155:303–307
Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51:201–213
Smith DC, Azam F (1992) A simple economical method for measuring bacterial protein synthesis rates in seawater using 3H leucine. Mar Microb Food Webs 6:107–114
Sprintall J, Roemmich D (1999) Characterizing the structure of the surface layer in the Pacific Ocean. J Geophys Res C Oceans 104:23297–23311
Stoderegger K, Herndl GJ (1998) Production and release of bacterial capsular material and its subsequent utilization by marine bacterioplankton. Limnol Oceanogr 43:877–884
Stoderegger KE, Herndl GJ (1999) Production of exopolymer particles by marine bacterioplankton under contrasting turbulence conditions. Mar Ecol Prog Ser 189:9–16
Sugimoto K, Fukuda H, Baki MA, Koike I (2007) Bacterial contributions to formation of transparent exopolymer particles (TEP) and seasonal trends in coastal waters of Sagami Bay, Jaoan. Aquat Microb Ecol 46:31–41
Tanaka T, Zohary T, Krom MD, Law CS, Pitta P, Psarra S, Rassoulzadegan F, Thingstad TF, Tselepides A, Woodward EMS, Flaten GAF, Skjoldal EF, Zodiatis G (2007) Microbial community structure and function in the Levantine Basin of the eastern Mediterranean. Deep-Sea Res Part I Oceanogr Res Pap 54:1721–1743
Thingstad TF, Rassoulzadegan F (1999) Conceptual models for the biogeochemical role of the photic zone microbial food web, with particular reference to the Mediterranean Sea. Progr Oceanogr 44:271–286
Thornton DCO (2004) Formation of transparent exopolymeric particles (TEP) from macroalgal detritus. Mar Ecol Prog Ser 282:1–12
Tranvik LJ, Sherr EB, Sherr BF (1993) Uptake and utilization of colloidal DOM by heterotrophic flagellates in seawater. Mar Ecol Prog Ser 92:301–309
Troussellier M, Courties C, Zettelmaier S (1995) Flow cytometric analysis of coastal lagoon bacterioplankton and picophytoplankton: fixation and storage effects. Estuar Coast Shelf Sci 40:621–633
Van Wambeke F, Christaki U, Giannakourou A, Moutin T, Souvemerzoglou K (2002) Longitudinal and vertical trends of bacterial limitation by phosphorus and carbon in the Mediterranean Sea. Microb Ecol 43:119–133
Van Wambeke F, Lefèvre D, Prieur L, Sempéré R, Bianchi M, Oubelkheir K, Bruyant F (2004) Distribution of microbial biomass, production, respiration, dissolved organic carbon and factors controlling bacterial production across a geostrophic front (Almeria-Oran, SW Mediterranean Sea). Mar Ecol Prog Ser 269:1–15
van Loosdrecht MCM, Lyklema J, Norde W, Zehnder AJB (1989) Bacterial adhesion: a physicochemical approach. Microb Ecol 17:1–15
Acknowledgements
We thank the captain and crew of R/V “García del Cid” and the Marine Technology Unit for their help in the sampling and experimental setup. We thank R. Santiago for the TOC and chl a analyses. We also acknowledge R.A. Reynolds for improving the English and the anonymous reviewers for the insightful comments to a previous version of this manuscript. This work was funded by the Spanish Ministry of Science and Technology (THRESHOLDS complementary action ref. CTM2005-24238-E to CMD and DISPAR CGL2005-00076 to IR). E.O.-R. was supported by fellowships from the Spanish Ministry of Science and Education and the University of Granada.
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Ortega-Retuerta, E., Duarte, C.M. & Reche, I. Significance of Bacterial Activity for the Distribution and Dynamics of Transparent Exopolymer Particles in the Mediterranean Sea. Microb Ecol 59, 808–818 (2010). https://doi.org/10.1007/s00248-010-9640-7
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DOI: https://doi.org/10.1007/s00248-010-9640-7