Fottea 2023, 23(2):201-207 | DOI: 10.5507/fot.2022.020
High abundances and negligible grazing during winter by the mixotrophic chrysophyte Dinobryon
- 1 Pennsylvania State University Schuylkill, Department of Biology, Schuylkill Haven, PA 17972, USA; *Corresponding author e-mail: sbp20@psu.edu
- 2 Temple University, Department of Biology, Philadelphia, PA 19122, USA
Grazing on bacteria by planktonic organisms is a channel for the biological transfer of organic matter through the aquatic food web. Much attention has been given to the importance of heterotrophic nanoflagellates and ciliates as primary grazers of bacteria. However, the prevalence of phagotrophy by phytoplankton across many environments emphasizes a need to include mixotrophy in studies of the protistan food web. Few studies have addressed the seasonal dynamics nor grazing activity of mixotrophs in freshwater environments, especially those that extend below surface waters. The goal of this work was to examine temporal patterns in mixotroph abundance and taxon-specific bacterivory, with a focus on Dinobryon. Results shown here support our general predictions of increased bacterivory by Dinobryon where a low light and nutrient environment may promote grazing. Dinobryon spp. were numerically dominant members of the community under-ice in winter, possibly as a result of their ability to supplement photosynthesis with phagotrophy of bacteria in conditions of reduced irradiance and day length. However, daily grazing rate and associated impact on the bacterial community during winter were not substantial. These results highlight the importance of including winter sampling when an active community of phagotrophic phytoflagellates may play a major role in ecosystem functioning. Results underscore the importance of including measurements of grazing activity with mixotroph occurrences, as high abundance of Dinobryon did not align with high rates of bacterivory.
Keywords: bacterivory, Dinobryon, flagellate, mixotrophy, phagotrophy, seasonal succession
Received: September 21, 2022; Revised: November 6, 2022; Accepted: December 13, 2022; Prepublished online: August 2, 2023; Published: October 25, 2023 Show citation
References
- Anderson, R.; Jurgens, K. & Hansen, P.J. (2017): Mixotrophic phytoflagellate bacterivory field measurements strongly biased by standard approaches: a case study. - Frontiers in Microbiology 8: 1398. DOI: 10.3389/fmicb.2017.01398
Go to original source...
- Azam, F.; Fenchel, T.; Field, J. G.; Gray, J. S., Meyerreil, L. A. & Thingstad, F. (1983): The ecological role of water-column microbes in the sea. - Marine Ecology Progress Series 10: 257-263.
Go to original source...
- Bell, E.M. & Laybourn-Parry, J. (2003): Mixotrophy in the Antarctic phytoflagellate, Pyramimonas gelidicola (Chlorophyta: Prasinophyceae). - Journal of Phycology 39: 644-649.
Go to original source...
- Berninger, U.G.; Caron, D.A. & Sanders, R.W. (1992): Mixotrophic algae in 3 ice-covered lakes of the Pocano Mountains, USA. - Freshwater Biology 28: 263-272.
Go to original source...
- Bird, D.F. & Kalff, J. (1987): Algal phagotrophy: Regulating factors and importance relative to photosynthesis in Dinobryon (Chryphyceae). - Limnology and Oceanography 32: 277-284.
Go to original source...
- Butts, E. & Carrick, H.J. (2017): Phytoplankton seasonality along a trophic gradient of temperate lakes: convergence in taxonomic compostion during winter ice-cover. - Northeastern Naturalist 24: B167-B187.
Go to original source...
- Caron, D.A.; Sanders, R.W.; Lim, E.L.; Marrase; C.; Amaral, L.A.; Whitney, S.; Aoki, R.B. & Porter, K.G. (1993): Light-dependent phagotrophy in the fresh-water mixotrophic chrysophyte Dinobryon cylindricum. - Microbial Ecology 25: 93-111.
Go to original source...
- Charvet, S.; Vincent, W.F. & Lovejoy, C. (2012): Chrysophytes and other protists in High Arctic lakes: molecular gene surveys, pigment signatures and microscopy. - Polar Biology 35: 733-748.
Go to original source...
- Domaizon, I.; Viboud, S. & Fontvieille, D. (2003): Taxon-specific and seasonal variations in flagellates grazing on heterotrophic bacteria in the oligotrophic Lake Annecy - importance of mixotrophy. - FEMS Microbiology Ecology 46: 317-329.
Go to original source...
- Ehrenberg, C.G. (1834): Dritter Beitrag zur Erkenntniss grosser Organisation in der Richtung des kleinsten Raumes. - Abhandlungen der Königlichen Akademie der Wissenschaften 1833: 145-336.
- Fischer, R.; Giebel, H.A.; Hillebrand, H. & Ptacnik, R. (2017): Importance of mixotrophic bacterivory can be predicted by light and loss rates. - Oikos 126: 713-722.
Go to original source...
- Gasol, J.M.; Garciacantizano, J.; Massana, R.; Guerrero, R. & Pedrosalio, C. (1993): Physiological ecology of a metalimnetic cryptomonas population - relationships to light, sulfide and nutrients. - Journal of Plankton Research 15: 255-275.
Go to original source...
- Gerea, M.; Queimalinos, C. & Unrein, F. (2019): Grazing impact and prey selectivity of picoplanktonic cells by mixotrophic flagellates in oligotrophic lakes. - Hydrobiologia 831: 5-21.
Go to original source...
- Grosbois, G.; Mariash, H.; Schneider, T. & Rautio, M. (2017): Under-ice availability of phytoplankton lipids is key to freshwater zooplankton winter survival. - Scientific Reports 7: 11543. DOI: 10.1038/s41598-017-10956-0
Go to original source...
- Hampton, S.E.; Moore, M.V.; Ozersky, T.; Stanley, E.H.; Polashenski, C.M. & Galloway, A.W.E. (2015): Heating up a cold subject: prospects for under-ice plankton research in lakes. - Journal of Plankton Research 37: 277-284.
Go to original source...
- Hansson, T.H.; Grossart, H.P.; del Giorgio, P.A.; St-Gelais, N.F. & Beisner, B.E. (2019): Environmental drivers of mixotrophs in boreal lakes. - Limnology and Oceanography 64: 1688-1705.
Go to original source...
- Heinze, A.W.; Truesdale, C.L.; DeVaul, S.B.; Swinden, J. & Sanders, R.W. (2013): Role of temperature in growth, feeding, and vertical distribution of the mixotrophic chrysophyte Dinobryon. - Aquatic Microbial Ecology 71: 155-163.
Go to original source...
- Hitchman, R.B. & Jones, H.L.J. (2000): The role of mixotrophic protists in the population dynamics of the microbial food web in a small artificial pond. - Freshwater Biology 43: 231-241.
Go to original source...
- Holen, D.A. (1999): Effects of prey abundance and light intensity on the mixotrophic chrysophyte Poterioochromonas malhamensis from a mesotrophic lake. - Freshwater Biology 42: 445-455.
Go to original source...
- Holen, D.A. & Boraas, M.E. (1995): Mixotrophy in Chrysophytes. - In: Sandgren, C.D.; Smol, J.P. & Kristiansen, J. (eds): Chrysophyte Algae: Ecology, Phylogeny and Development. - pp. 119-140, Cambridge University Press.
Go to original source...
- Jost, C.; Lawrence, C.A.; Campolongo, F.; van de Bund, W.; Hill, S. & DeAngelis, D.L. (2004): The effects of mixotrophy on the stability and dynamics of a simple planktonic food web model. - Theoretical Population Biology 66: 37-51.
Go to original source...
- Knoll, L.B.; Morgan, A.; Vanni, M.J.; Leach, T.H.; Williamson, T.J. & Brentrup, J.A. (2016): Quantifying pelagic phosphorus regeneration using three methods in lakes of varying productivity. - Inland Waters 6: 509-522.
Go to original source...
- Lie, A.A.Y.; Liu, Z.F.; Terrado, R.; Tatters, A.O.; Heidelberg, K.B. & Caron, D.A. (2017): Effect of light and prey availability on gene expression of the mixotrophic chrysophyte, Ochromonas sp. - BMC Genomics 18.
Go to original source...
- Millette, N. C.; da Costa, M.; Mora, J. W. & Gast, R. J. (2021): Temporal and spatial variability of phytoplankton and mixotrophs in a temperate estuary. - Marine Ecology Progress Series 677: 17-31.
Go to original source...
- Palsson, C. & Graneli, W. (2003): Diurnal and seasonal variations in grazing by bacterivorous mixotrophs in an oligotrophic clearwater lake. - Archiv Für Hydrobiologie 157: 289-307.
Go to original source...
- Princiotta, S.D. & Sanders, R.W. (2017): Heterotrophic and mixotrophic nanoflagellates in a mesotrophic lake: Abundance and grazing impacts across season and depth. - Limnology and Oceanography 62: 632-644.
Go to original source...
- Princiotta, S.D.; Smith, B.T. & Sanders, R.W. (2016): Temperature-dependent phagotrophy and phototrophy in a mixotrophic chrysophyte. - Journal of Phycology 52: 432-440.
Go to original source...
- Ptacnik, R.; Gomes, A.; Royer, S.J.; Berger, S.A.; Calbet, A.; Nejstgaard, J.C.; Gasol, J.M.; Isari, S.; Moorthi, S.D.; Ptacnikova, R.; Striebel, M.; Sazhin, A.F.; Tsagaraki, T.M.; Zervoudaki, S.; Altoja, K.; Dimitriou, P.D.; Laas, P.; Gazihan, A.; Martinez, R.A.; Schabhuttl, S.; Santi, I.; Sousoni, D. & Pitta, P. (2016): A light-induced shortcut in the planktonic microbial loop. - Scientific Reports 6: 29286. DOI: 10.1038/srep29286
Go to original source...
- Ram, A.S.P.; Palesse, S.; Colombet, J.; Sabart, M.; Perriere, F. & Sime-Ngando, T. (2013): Variable viral and grazer control of prokaryotic growth efficiency in temperate freshwater lakes (French Massif Central). - Microbial Ecology 66: 906-916.
Go to original source...
- Sander, R.W. (1991): Mixotrophic protists in marine and freshwater ecosystems. - Journal of Protozoology 38: 76-81.
Go to original source...
- Sanders, R.W.; Porter, K.G.; Bennett, S.J. & Debiase, A. E. (1989): Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a fresh-water planktonic community. - Limnology and Oceanography 34: 673-687.
Go to original source...
- Sherr, B.F.; Sherr, E.B. & Fallon, R.D. (1987): Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. - Applied and Environmental Microbiology 53: 958-965.
Go to original source...
- Sherr, E.B. & Sherr, B.F. (1994): Bacterivory and herbivory - key roles of phagotrophic protists in pelagic food webs. - Microbial Ecology 28: 223-235.
Go to original source...
- Stoecker, D.K. & Lavrentyev, P.J. (2018): Mixotrophic plankton in the polar seas: a pan-Arctic review. - Frontiers in Marine Science 5: 292. DOI: 10.3389/fmars.2018.00292
Go to original source...
- Thingstad, T.F.; Havskum, H.; Garde, K. & Riemann, B. (1996): On the strategy of "eating your competitor'': A mathematical analysis of algal mixotrophy. - Ecology 77: 2108-2118.
Go to original source...
- Unrein, F.; Gasol, J.M. & Massana, R. (2010): Dinobryon faculiferum (Chrysophyta) in coastal Mediterranean seawater: presence and grazing impact on bacteria. - Journal of Plankton Research 32: 559-564.
Go to original source...
- van Hannen, E.J.; Veninga, M.; Bloem, J.; Gons, H.J. & Laanbroek, H.J. (1999): Genetic changes in the bacterial community structure associated with protistan grazers. - Archiv Für Hydrobiologie 145: 25-38.
Go to original source...
- Vick-Majors, T.J.; Priscu, J.C. & Amaral-Zettler, L.A. (2014): Modular community structure suggests metabolic plasticity during the transition to polar night in ice-covered Antarctic lakes. - ISME Journal 8: 778-789.
Go to original source...
- Wilken, S.; Choi, C.J. & Worden, A.Z. (2020): Contrasting mixotrophic lifestyles reveal different ecological niches in two closely related marine protists. - Journal of Phycology 56: 52-67.
Go to original source...