Mixotrophic organisms become more heterotrophic with rising temperature

Ecology Letters

Volumn 16, Issue 2, 2013, Pages 225-233

  Wilken, Susanne ^a,b   Huisman, Jef ^a   Naus Wiezer, Suzanne ^a   Van Donk, Ellen ^a,c  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Autotrophy; Global warming; Heterotrophy; Metabolic theory; Microbial loop; Mixotrophy; Photosynthesis; Plankton communities

Indexed keywords

AUTOTROPHY; BACTERIUM; BROWN ALGA; CARBON CYCLE; CHLOROPHYLL; ELECTRON; FOOD WEB; FUNCTIONAL ROLE; GLOBAL WARMING; GRAZING; GROWTH RATE; HETEROTROPHY; HIGH TEMPERATURE; HYPOTHESIS TESTING; MICROBIAL LOOP; MIXOTROPHY; NUTRITION; PHOTOSYNTHESIS; TEMPERATURE EFFECT;

ARTICLE; AUTOTROPHY; GROWTH, DEVELOPMENT AND AGING; HETEROTROPHY; OCHROMONAS; PHOTOSYNTHESIS; PHYSIOLOGY; POPULATION DYNAMICS; TEMPERATURE;

AUTOTROPHIC PROCESSES; HETEROTROPHIC PROCESSES; OCHROMONAS; PHOTOSYNTHESIS; POPULATION DYNAMICS; TEMPERATURE;

BACTERIA (MICROORGANISMS); CHRYSOPHYCEAE; OCHROMONAS;

EID: 84872621533     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12033     Document Type: Article

References (50)

1. Allen, A.P., Gillooly, J.F. & Brown, J.H. (2005). Linking the global carbon cycle to individual metabolism. Funct. Ecol., 19, 202-213.
2. Andersson, A., Falk, S., Samuelsson, G. & Hagström, Å. (1989). Nutritional characteristics of a mixotrophic nanoflagellate, Ochromonas sp. Microb. Ecol., 17, 251-262.
3. Bennett, S.J., Sanders, R.W. & Porter, K.G. (1990). Heterotrophic, autotrophic, and mixotrophic nanoflagellates: seasonal abundances and bacterivory in a eutrophic lake. Limnol. Oceanogr., 35, 1821-1832.
4. Bernacchi, C.J., Singsaas, E.L., Pimentel, C., Portis, A.R. & Long, S.P. (2001). Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell Environ., 24, 253-259.
5. Blackman, F.F. (1905). Optima and limiting factors. Ann. Bot., 19, 281-296.
6. Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M. & West, G.B. (2004). Toward a metabolic theory of ecology. Ecology, 85, 1771-1789.
7. Burkholder, J.A.M., Glibert, P.M. & Skelton, H.M. (2008). Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae, 8, 77-93.
8. Caron, D.A., Goldman, J.C. & Dennett, M.R. (1986). Effect of temperature on growth, respiration, and nutrient regeneration by an omnivorous microflagellate. Appl. Environ. Microbiol., 52, 1340-1347.
9. Choi, J.W. & Peters, F. (1992). Effects of temperature on two psychrophilic ecotypes of a heterotrophic nanoflagellate, Paraphysomonas imperforata. Appl. Environ. Microbiol., 58, 593-599.
10. Coles, J.F. & Jones, R.C. (2000). Effect of temperature on photosynthesis-light response and growth of four phytoplankton species isolated from a tidal freshwater river. J. Phycol., 36, 7-16.
11. Compeau, G., Alachi, B.J., Platsouka, E. & Levy, S.B. (1988). Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Appl. Environ. Microbiol., 54, 2432-2438.
12. Diehl, S. & Feissel, M. (2000). Effects of enrichment on three-level food chains with omnivory. Am. Nat., 155, 200-218.
13. Englund, G., Öhlund, G., Hein, C.L. & Diehl, S. (2011). Temperature dependence of the functional response. Ecol. Lett., 14, 914-921.
14. Eppley, R.W. (1972). Temperature and phytoplankton growth in the sea. Fish. Bull., 70, 1063-1085.
15. Estep, K.W., Davis, P.G., Keller, M.D. & Sieburth, J.McN. (1986). How important are oceanic algal nanoflagellates in bacterivory? Limnol. Oceanogr., 31, 646-650.
16. Falkowski, P.G. & Raven, J.A. (2007). Aquatic Photosynthesis, 2nd edn. Princeton University Press, Princeton, NJ, USA.
17. Flynn, K.J., Stoecker, D.K., Mitra, A., Raven, J.A., Glibert, P.M., Hansen, P.J. et al. (2012). Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J. Plankton Res., DOI:10.1093/plankt/fbs062.
18. Gillooly, J.F., Brown, J.H., West, G.B., Savage, V.M. & Charnov, E.L. (2001). Effects of size and temperature on metabolic rate. Science, 293, 2248-2251.
19. Hansen, P.J. (2011). The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J. Eukaryot. Microbiol., 58, 203-214.
20. Hartmann, M., Grob, C., Tarran, G.A., Martin, A.P., Burkill, P.H., Scanlan, D.J. et al. (2012). Mixotrophic basis of Atlantic oligotrophic ecosystems. Proc. Natl Acad. Sci. USA, 109, 5756-5760.
21. Heinbokel, J.F. (1978). Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar. Biol., 47, 177-189.
22. Hoppe, H.G., Gocke, K., Koppe, R. & Begler, C. (2002). Bacterial growth and primary production along a north-south transect of the Atlantic ocean. Nature, 416, 168-171.
23. Jansson, M., Blomqvist, P., Jonsson, A. & Bergström, A.K. (1996). Nutrient limitation of bacterioplankton, autotrophic and mixotrophic phytoplankton, and heterotrophic nanoflagellates in Lake Örträsket. Limnol. Oceanogr., 41, 1552-1559.
24. Jöhnk, K.D., Huisman, J., Sharples, J., Sommeijer, B., Visser, P.M. & Stroom, J.M. (2008). Summer heatwaves promote blooms of harmful cyanobacteria. Glob. Change Biol., 14, 495-512.
25. Johnson, M.D. (2011). The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynthesis Res., 107, 117-132.
26. Johnson, M.D. & Stoecker, D.K. (2005). Role of feeding in growth and photophysiology of Myrionecta rubra. Aquat. Microb. Ecol., 39, 303-312.
27. Jones, H. (1997). A classification of mixotrophic protists based on their behaviour. Freshwat. Biol., 37, 35-43.
28. 2 specificity of ribulose 1, 5-bisphosphate carboxylase/oxygenase: dependence on ribulosebisphosphate concentration, pH and temperature. Planta, 161, 308-313.
29. Kratina, P., Greig, H.S., Thompson, P.L., Carvalho-Pereira, T.S.A. & Shurin, J.B. (2012). Warming modifies trophic cascades and eutrophication in experimental freshwater communities. Ecology, 93, 1421-1430.
30. Lopez-Urrutia, A., San Martin, E., Harris, R.P. & Irigoien, X. (2006). Scaling the metabolic balance of the oceans. Proc. Natl Acad. Sci. USA, 103, 8739-8744.
31. Maberly, S.C., Ball, L.A., Raven, J.A. & Sueltemeyer, D. (2009). Inorganic carbon acquisition by chrysophytes. J. Phycol., 45, 1052-1061.
32. Maxwell, K. & Johnson, G.N. (2000). Chlorophyll fluorescence: a practical guide. J. Exp. Bot., 51, 659-668.
33. O'Connor, M.I., Piehler, M.F., Leech, D.M., Anton, A. & Bruno, J.F. (2009). Warming and resource availability shift food web structure and metabolism. PLoS Biol., 7, e1000178. doi:10.1371/journal.pbio.1000178.
34. Paerl, H.W. & Huisman, J. (2008). Blooms like it hot. Science, 320, 57-58.
35. Platt, T., Gallegos, C.L. & Harrison, W.G. (1980). Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res., 38, 687-701.
36. Polis, G.A. & Holt, R.D. (1992). Intraguild predation: the dynamics of complex trophic interactions. Trends Ecol. Evol., 7, 151-154.
37. Rose, J.M. & Caron, D.A. (2007). Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters. Limnol. Oceanogr., 52, 886-895.
38. Sanders, R.W., Berninger, U.G., Lim, E.L., Kemp, P.F. & Caron, D.A. (2000). Heterotrophic and mixotrophic nanoplankton predation on picoplankton in the Sargasso Sea and on Georges Bank. Mar. Ecol. Prog. Ser., 192, 103-118.
39. Sanders, R.W., Caron, D.A., Davidson, J.M., Dennett, M.R. & Moran, D.M. (2001). Nutrient acquisition and population growth of a mixotrophic alga in axenic and bacterized cultures. Microb. Ecol., 42, 513-523.
40. Savage, V.M., Gillooly, J.F., Brown, J.H., West, G.B. & Charnov, E.L. (2004). Effects of body size and temperature on population growth. Am. Nat., 163, 429-441.
41. Selosse, M.A. & Roy, M. (2009). Green plants that feed on fungi: facts and questions about mixotrophy. Trends Plant Sci., 14, 64-70.
42. Stoecker, D.K. (1998). Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur. J. Protistol., 34, 281-290.
43. Stoecker, D.K. & Michaels, A.E. (1991). Respiration, photosynthesis and carbon metabolism in planktonic ciliates. Mar. Biol., 108, 441-447.
44. Tcherkez, G.G.B., Farquhar, G.D. & Andrews, T.J. (2006). Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc. Natl Acad. Sci. USA, 103, 7246-7251.
45. Van Donk, E., Cerbin, S., Wilken, S., Helmsing, N.R., Ptacnik, R. & Verschoor, A.M. (2009). The effect of a mixotrophic chrysophyte on toxic and colony-forming cyanobacteria. Freshwat. Biol., 54, 1843-1855.
46. Vasseur, D.A. & McCann, K.S. (2005). A mechanistic approach for modeling temperature-dependent consumer-resource dynamics. Am. Nat., 166, 184-198.
47. Wilken, S., Wiezer, S., Huisman, J. & Van Donk, E. (2010). Microcystins do not provide anti-herbivore defence against mixotrophic flagellates. Aquat. Microb. Ecol., 59, 207-216.
48. Wohlers, J., Engel, A., Zöllner, E., Breithaupt, P., Jürgens, K., Hoppe, H.G. et al. (2009). Changes in biogenic carbon flow in response to sea surface warming. Proc. Natl Acad. Sci. USA, 106, 7067-7072.
49. Yvon-Durocher, G., Jones, J.I., Trimmer, M., Woodward, G. & Montoya, J.M. (2010). Warming alters the metabolic balance of ecosystems. Philos. Trans. R. Soc. B-Biol. Sci., 365, 2117-2126.
50. Zubkov, M.V. & Tarran, G.A. (2008). High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature, 455, 224-226.