Skip to main content
Log in

Effect of Temperature on the Release of Transparent Exopolymer Particles (TEP) and Aggregation by Marine Diatoms (Thalassiosira weissflogii and Skeletonema marinoi)

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

The presence of diatoms is accompanied by the production of a large amount of extracellular polymeric substances, which are mainly composed of carbohydrates. Transparent exopolymer particles (TEP) are a large class of extracellular polymeric substances with high stickiness that promotes the formation of aggregates and marine snow, which affects marine bio-carbon pump efficiency. The purpose of this research was to determine how temperature increases affect the allocation of cellular carbohydrates and the formation and aggregation of TEP. The results showed that the responses of two different diatom species (Thalassiosira weissflogii and Skeletonema marinoi) differed according to temperature. The cell density and chlorophyll a concentration of the former were not significantly correlated with temperature, while those of the latter were significantly decreased with increasing temperature. This indicates that the two species of diatom may have different heat tolerance ranges. A temperature increase will promote significant formation of TEP by both types of diatoms, including aggregation of S. marinoi as the temperature rises, meaning that the high temperature will produce an aggregate with a larger particle size and thus may increase the sedimentation rate of organic carbon. Moreover, the TEP aggregation of T. weissflogii did not increase; therefore, its particle size was smaller, and so it may remain on the sea surface at high temperatures for longer periods. These influences have a profound impact on the biogeochemical cycling of carbon.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alldredge, A. L., Passow, U., and Logan, B. E., 1993. The abundance and significance of a class of large, transparent organic particles in the ocean. Deep-Sea Research Part I — Oceanographic Research Papers, 40: 1131–1140.

    Article  Google Scholar 

  • Arar, E. J., and Collins, G. B., 1997. Method 445.0. In vitro determination of chlorophyll a and pheophytin a in marine and freshwater algae by fluorescence. Environmental Protection Agency, Cincinnati, Ohio, 1–20.

    Google Scholar 

  • Armbrust, E. V., and Galindo, H. M., 2001. Rapid evolution of a sexual reproduction gene in centric diatoms of the genus Thalassiosira. Applied Environmental Microbiology, 67: 3501–3513.

    Article  Google Scholar 

  • Barofsky, A., Simonelli, P., Vidoudez, C., Troedsson, C., Nejstgaard, J. C., Jakobsen, H. H., and Pohnert, G., 2010. Growth phase of the diatom Skeletonema marinoi influences the metabolic profile of the cells and the selective feeding of the copepod Calanus spp. Journal of Plankton Research, 32: 263–272.

    Article  Google Scholar 

  • Bhaskar, P. V., and Bhosle, N. B., 2005. Microbial extracellular polymeric substances in marine biogeochemical processes. Current Science, 88: 45–53.

    Google Scholar 

  • Bittar, T. B., Uta, P., Liti, H., Bidle, K. D., and Harvey, E. L., 2018. An updated method for the calibration of transparent exopolymer particle measurements. Limnology and Oceanography Methods, 16: 621–628.

    Article  Google Scholar 

  • Bresnan, E., Hay, S., Hughes, S. L., Fraser, S., Rasmussen, J., Webster, L., Slesser, G., Dunn, J., and Heath, M. R., 2009. Seasonal and interannual variation in the phytoplankton community in the north east of Scotland. Journal of Sea Research, 61(1–2): 17–25.

    Article  Google Scholar 

  • Chin, W. C., Orellana, M. W., and Verdugo, P., 1998. Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature, 391: 568–571.

    Article  Google Scholar 

  • Cisternas-Novoa, C., Lee, C., Tang, T., de Jesus, R., and Engel, A., 2019. Effects of higher CO2 and temperature on exopolymer particle content and physical properties of marine aggregates. Frontiers in Marine Science, 5: 500.

    Article  Google Scholar 

  • Claquin, P., Probert, I., Lefebvre, S., and Veron, B., 2008. Effects of temperature on photosynthetic parameters and TEP production in eight species of marine microalgae. Aquatic Microbial Ecology, 51: 1–11.

    Article  Google Scholar 

  • Corzo, A., Morillo, J. A., and Rodriguez, S., 2000. Production of transparent exopolymer particles (TEP) in cultures of Chaetoceros calcitrans under nitrogen limitation. Aquatic Microbial Ecology, 23: 63–72.

    Article  Google Scholar 

  • Crocker, K. M., 1993. Diatom aggregation and dimethylsulfide production in phytoplankton blooms. PhD thesis. University of California, Santa Barbara, California.

  • Crocker, K. M., and Passow, U., 1995. Differential aggregation of diatoms. Marine Ecology Progress Series, 117: 249–257.

    Article  Google Scholar 

  • Degerlund, M., and Eilertsen, H., 2010. Main species characteristics of phytoplankton spring blooms in NE Atlantic and Arctic waters (68–80°N). Estuaries and Coasts, 33: 242–269.

    Article  Google Scholar 

  • Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., and Smith, F., 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28: 350–356.

    Article  Google Scholar 

  • Engel, A., 2000. The role of transparent exopolymer particles (TEP) in the increase in apparent particles stickiness (α) during the decline of a diatom bloom. Journal of Plankton Research, 22: 485–497.

    Article  Google Scholar 

  • Engel, A., 2009. Determination of marine gel particles. In: Practical Guidelines for the Analysis of Seawater. Oliver, W., ed., CRC Press, Taylor and Francis Group, Boca Raton, Florida, 57–71.

    Google Scholar 

  • Engel, A., Händel, N., Wohlers, J., Lunau, M., Petergrossart, H., Sommer, U., and Riebesell, U., 2011. Effects of sea surface warming on the production and composition of dissolved organic matter during phytoplankton blooms, results from a mesocosm study. Journal of Plankton Research, 33: 357–372.

    Article  Google Scholar 

  • Franklin, D. J., Airs, R. L., Fernandes, M., Bell, T. G., Bongaerts, R. J., Berges, J. A., and Malin, G., 2012. Identification of senescence and death in Emiliania huxleyi and Thalassiosira pseudonana: Cell staining, chlorophyll alterations, and dimethylsulfoniopropionate (DMSP) metabolism. Limnology and Oceanography, 57: 305–317.

    Article  Google Scholar 

  • Fukao, T., Kimoto, K., and Kotani, Y., 2010. Production of transparent exopolymer particles by four diatom species. Fisheries Science, 76(5): 755–760.

    Article  Google Scholar 

  • Fukao, T., Kimoto, K., and Kotani, Y., 2012. Effect of temperature on cell growth and production of transparent exopolymer particles by the diatom Coscinodiscus granii isolated from marine mucilage. Journal of Applied Phycology, 24: 181–186.

    Article  Google Scholar 

  • Grossart, H. P., Czub, G., and Simon, M., 2006. Algae-bacteria interactions and their effects on aggregation and organic matter flux in the sea. Environmental Microbiology, 8(6): 1074–1084.

    Article  Google Scholar 

  • Guillard, R. R. L., and Sieracki, M. S., 2005. Chapter 16. Counting cells in cultures with the light microscope. In: Algal Culturing Techniques. Andersen, R. A., ed., Academic Press, Boston, Massachusetts, 251–289.

    Google Scholar 

  • Hoagland, K. D., Rosowski, J. R., Gretz, M. R., and Roemer, S. C., 1993. Diatom extracellular polymeric substances, function, fine-structure, chemistry, and physiology. Journal of Phycology, 29: 537–566.

    Article  Google Scholar 

  • Hobbie, J. E., Daley, R., and Jasper, S., 1977. Use of uuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology, 33(5): 948–951.

    Article  Google Scholar 

  • IPCC, 2013. Climate change: The physical science basis. Summary for policy makers. contribution of working group I to the fourth assessment report of the intergovernmental panel for climate change. IPCC Secretariat, Geneva, 21.

    Google Scholar 

  • Kaeriyama, H., Katsuki, E., Otsubo, M., Yamada, M., Ichimi, K., Tada, K., and Harrison, J. P., 2011. Effects of temperature and irradiance on growth of strains belonging to seven Skeletonema species isolated from Dokai Bay, southern Japan. European Journal of Phycology, 46(2): 113–124.

    Article  Google Scholar 

  • Kent, M. L., Whyte, J. N. C., and Latrace, C., 1995. Gill lesions and mortality in seawater pen-reared Atlantic salmon Salmo salar associated with a dense bloom of Skeletonema costatum and Thalassiosira species. Diseases of Aquatic Organisms, 22: 77–81.

    Article  Google Scholar 

  • Keys, M., Tilstone, G., Findlay, H. S., Widdicombe, C. E., and Lawson, T., 2018. Effects of elevated CO2 and temperature on phytoplankton community biomass, species composition and photosynthesis during an experimentally induced autumn bloom in the western English Channel. Biogeosciences, 15(10): 3203–3222.

    Article  Google Scholar 

  • Kiørboe, T., and Hansen, J. L. S., 1993. Phytoplankton aggregate formation, observations of patterns and mechanisms of cell sticking and the significance of exopolymeric material. Journal of Plankton Research, 15: 993–1018.

    Article  Google Scholar 

  • Kiørboe, T., Lundsgaard, C., Olesen, M., and Hansen, J. L. S., 1994. Aggregation and sedimentation processes during a spring phytoplankton bloom: A field experiment to test coagulation theory. Journal of Marine Research, 52(2): 297–323.

    Article  Google Scholar 

  • Kiørboe, T., Tiselius, P., Mitchell-Innes, B., Hansen, J. L. S., Visser, A. W., and Mari, X., 1998. Intensive aggregate formation with low vertical flux during an upwelling-induced diatom bloom. Limnology Oceanography, 43(1): 104–116.

    Article  Google Scholar 

  • Kirby, R. R., Beaugrand, G., Lindley, J. A., Richardson, A. J., Edwards, M., and Reid, P., 2007. Climate effects and benthic-pelagic coupling in the North Sea. Marine Ecology Progress Series, 330: 31–38.

    Article  Google Scholar 

  • Lewandowska, A., and Sommer, U., 2010. Climate change and the spring bloom: A mesocosm study on the influence of light and temperature on phytoplankton and mesozooplankton. Marine Ecology Progress Series, 405: 101–111.

    Article  Google Scholar 

  • Logan, B. E., Grossart, H. P., and Simon, M., 1994. Direct observation of phytoplankton, TEP and aggregates on polycarbonate filters using brightfield microscopy. Journal of Plankton Research, 16: 1811–1815.

    Article  Google Scholar 

  • Mari, X., Passow, U., Migon, C., Burd, A. B., and Legendre, L., 2017. Transparent exopolymer particles: Effects on carbon cycling in the ocean. Progress in Oceanography, 151: 13–37.

    Article  Google Scholar 

  • Passow, U., 2002a. Formation of transparent exopolymer particles, TEP from dissolved precursor material. Marine Ecology Progress Series, 192: 1–11.

    Article  Google Scholar 

  • Passow, U., 2002b. Transparent exopolymer particles (TEP) in aquatic environments. Progress in Oceanography, 55: 287–333.

    Article  Google Scholar 

  • Passow, U., 2002c. Production of transparent exopolymer particles (TEP) by phyto- and bacterioplankton. Marine Ecology Progress Series, 236: 1–12.

    Article  Google Scholar 

  • Passow, U., and Alldredge, A. L., 1995. Aggregation of a diatom bloom in a mesocosm: The role of transparent exopolymer particles (TEP). Deep-Sea Research Part II, 42: 99–109.

    Article  Google Scholar 

  • Passow, U., and Laws, E. A., 2015. Ocean acidification as one of multiple stressors: Growth response of Thalassiosira weissflogii (diatom) under temperature and light stress. Marine Ecology Progress, 541: 75–90.

    Article  Google Scholar 

  • Passow, U., Alldredge, A. L., and Logan, B. E., 1994. The role of particulate carbohydrate exudates in the flocculation of diatom blooms. Deep Sea Research Part I — Oceanographic Research Papers, 41(2): 335–357.

    Article  Google Scholar 

  • Rzadkowolski, C. E., and Thornton, D. C. O., 2012. Using laser scattering to identify diatoms and conduct aggregation experiments. European Journal of Phycology, 47: 30–41.

    Article  Google Scholar 

  • Sarmento, H., Montoya, J. M., Vázquez-Domínguez, E., Vaqué, D., and Gasol, J. M., 2010. Warming effects on marine microbial food web processes: How far can we go when it comes to predictions? Philosophical Transactions of the Royal Society, 365: 2137–2149.

    Article  Google Scholar 

  • Sarno, D., Kooistra, W. H. C. F., Medlin, L. K., Percopo, I., and Zingone, A., 2005. Diversity in the genus Skeletonema (Bacillariophyceae). II. An assessment of the taxonomy of S. costatum-like species with the description of four new species. Journal of Phycology, 41: 151–176.

    Article  Google Scholar 

  • Smith, D. J., and Underwood, G. J. C., 1998. Exopolymer production by intertidal epipelic diatoms. Limnology and Oceanography, 43(7): 1578–1591.

    Article  Google Scholar 

  • Sorhannus, U., Ortiz, J. D., Wolf, M., and Fox, M. G., 2010. Microevolution and speciation in Thalassiosira weissflogii (Bacillariophyta). Protist, 161: 237–249.

    Article  Google Scholar 

  • Spungin, D., Belkin, N., Foster, R., Stenegren, M., Caputo, A., Pujo-Pay, M., Leblond, N., Dupouy, C., Bonnet, S., and Berman-Frank, I., 2018. Programmed cell death in diazotrophs and the fate of organic matter in the western tropical South Pacific Ocean during the OUTPACE cruise. Biogeosciences, 15(12): 3893–3908.

    Article  Google Scholar 

  • Thornton, D. C. O., 2002. Diatom aggregation in the sea: Mechanisms and ecological implications. European Journal of Phycology, 37: 149–161.

    Article  Google Scholar 

  • Thornton, D. C. O., and Chen, J., 2017. Exopolymer production as a function of cell permeability and death in a diatom (Thalassiosira weissflogii) and a cyanobacterium (Synechococcus elongatus). Journal of Phycology, 53(2): 245–260.

    Article  Google Scholar 

  • Thornton, D. C. O., and Thake, B., 1998. Effect of temperature on the aggregation of Skeletonema costatum (Bacillariophyceae) and the implication for carbon flux in coastal waters. Marine Ecology Progress Series, 174: 223–231.

    Article  Google Scholar 

  • Underwood, G. J. C., and Paterson, D. M., 2003. The importance of extracellular carbohydrate production by marine epipelic diatoms. Advances in Botanical Research, 40: 183–240.

    Article  Google Scholar 

  • Underwood, G. J. C., Boulcott, M., Raines, C. A., and Waldron, K., 2004. Environmental effects on exopolymer production by marine benthic diatoms: Dynamics, changes in composition, and pathways of production. Journal of Phycology, 40: 293–304.

    Article  Google Scholar 

  • Underwood, G. J. C., Paterson, D. M., and Parkes, R. J., 1995. The measurement of microbial carbohydrate exopolymers from intertidal sediments. Limnology Oceanography, 40: 1243–1253.

    Article  Google Scholar 

  • Veldhuis, M. J. W., Kraay, G. W., and Timmermans, K. R., 2001. Cell death in phytoplankton: Correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. European Journal of Phycology, 36: 167–177.

    Article  Google Scholar 

  • Verdugo, P., Alldredge, A. L., Azam, F., Kirchman, D., Passow, U., and Santschi, P., 2004. The oceanic gel phase: A bridge in the DOM-POM continuum. Marine Chemistry, 92: 67–85.

    Article  Google Scholar 

  • Wolfstein, K. L., and Stal, J., 2002. Production of extracellular polymeric substances (EPS) by benthic diatoms: Effect of irradiance and temperature. Marine Ecology Progress Series, 236: 13–22.

    Article  Google Scholar 

  • Zlotnik, I., and Dubinsky, Z., 1989. The effect of light and temperature on DOC excretion by phytoplankton. Limnology and Oceanography, 34: 831–839.

    Article  Google Scholar 

Download references

Acknowledgements

This work is supported by the National Natural Science Foundation of China (No. 31500411), the Guangxi Zhuang Autonomous Region International Platform Project (No. 2019AC17008), the Guangxi Beihai Science and Technology Research Focus (Nos. 201995048 202082021 and 2019D05), the U. S. National Science Foundation (No. OCE 0726369), the Special Fund for Asian Regional Cooperation ‘2019 China-ASEAN Marine Science and Technology Cooperation Seminar Project’, the China Asia-Pacific Economic Cooperation (APEC) Cooperation Fund Project ‘APEC Typical Regional Coral Reef Ecosystem Comprehensive Assessment Technology and Management Cooperation Research’ and the ‘Bilateral and Multilateral International Cooperation’ Project of the Central Financial Allocation Program in 2019 and 2020.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kangli Guo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, J., Guo, K., Thornton, D.C.O. et al. Effect of Temperature on the Release of Transparent Exopolymer Particles (TEP) and Aggregation by Marine Diatoms (Thalassiosira weissflogii and Skeletonema marinoi). J. Ocean Univ. China 20, 56–66 (2021). https://doi.org/10.1007/s11802-021-4528-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-021-4528-3

Key words

Navigation