Do mixotrophs grow as photoheterotrophs? Photophysiological acclimation of the chrysophyte ochromonas danica after feeding

New Phytologist

Volumn 204, Issue 4, 2014, Pages 882-889

  Wilken, Susanne ^a,c   Schuurmans, J Merijn ^a,b   Matthijs, Hans C P ^b  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c MONTEREY BAY AQUARIUM RESEARCH INSTITUTE   (United States)

Author keywords

Autotrophy; Carbon fixation; Heterotrophy; Mixotrophy; Ochromonas danica; Photoheterotrophy; Photosystem; Rubisco

Indexed keywords

CHRYSOPHYCEAE; OCHROMONAS DANICA;

CARBON; CHLOROPHYLL; CHLOROPHYLL A; PHOTOSYSTEM I; PHOTOSYSTEM II; PIGMENT; RIBULOSEBISPHOSPHATE CARBOXYLASE;

ACCLIMATIZATION; AUTOTROPHY; BIOMASS; COMPARATIVE STUDY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OCHROMONAS; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; PHYSIOLOGY;

ACCLIMATIZATION; AUTOTROPHIC PROCESSES; BIOMASS; CARBON; CHLOROPHYLL; OCHROMONAS; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; PIGMENTS, BIOLOGICAL; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 84911995892     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12975     Document Type: Article

References (47)

1. Adolf JE, Stoecker DK, Harding LW. 2006. The balance of autotrophy and heterotrophy during mixotrophic growth of Karlodinium micrum (Dinophyceae). Journal of Plankton Research 28: 737-751.
2. Allen AE, LaRoche J, Maheswari U, Lommer M, Schauer N, Lopez PJ, Finazzi G, Fernie AR, Bowler C. 2008. Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proceedings of the National Academy of Sciences, USA 105: 10438-10443.
3. Béjà O, Spudich EN, Spudich JL, Leclerc M, DeLong EF. 2001. Proteorhodopsin phototrophy in the ocean. Nature 411: 786-789.
4. Bernát G, Waschewski N, Rögner M. 2009. Towards efficient hydrogen production: the impact of antenna size and external factors on electron transport dynamics in Synechocystis PCC6803. Photosynthesis Research 99: 205-216.
5. Berninger UG, Caron DA, Sanders RW. 1992. Mixotrophic algae in three ice-covered lakes of the Pocano Mountains, USA. Freshwater Biology 28: 263-272.
6. Bird DF, Kalff J. 1989. Phagotrophic sustenance of a metalimnetic phytoplankton peak. Limnology and Oceanography 34: 155-162.
7. Caron DA, Porter KG, Sanders RW. 1990. Carbon, nitrogen, and phosphorus budgets for the mixotrophic phytoflagellate Poterioochromonas malhamensis (Chrysophyceae) during bacterial ingestion. Limnology and Oceanography 35: 433-443.
8. Compeau G, Alachi BJ, Platsouka E, Levy SB. 1988. Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Applied and Environmental Microbiology 54: 2432-2438.
9. Flöder S, Hansen T, Ptacnik R. 2006. Energy-dependent bacterivory in Ochromonas minima: a strategy promoting the use of substitutable resources and survival at insufficient light supply. Protist 157: 291-302.
10. Flynn KJ, Stoecker DK, Mitra A, Raven JA, Glibert PM, Hansen PJ, Graneli E, Burkholder JM. 2013. Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. Journal of Plankton Research 35: 3-11.
11. 13C natural abundance of autotrophic and mycoheterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytologist 160: 209-223.
12. Gibbs PB, Biggins J. 1989. Regulation of the distribution of excitation energy in Ochromonas danica, an organism containing a chlorophyll-A/C/carotenoid light harvesting antenna. Photosynthesis Research 21: 81-91.
13. Gómez-Conarnau L, Gonzáles JM, Coll-Lladó M, Gourdon P, Pascher T, Neutze R, Pedrós-Alió C, Pinhassi J. 2007. Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445: 210-213.
14. Hartmann M, Grob C, Scanlan DJ, Martin AP, Burkill PH, Zubkov MV. 2011. Comparison of phosphate uptake rates by the smallest plastidic and aplastidic protists in the North Atlantic subtropical gyre. FEMS Microbiology Ecology 78: 327-335.
15. Hartmann M, Grob C, Tarran GA, Martin AP, Burkill PH, Scanlan DJ, Zubkov MV. 2012. Mixotrophic basis of Atlantic oligotrophic ecosystems. Proceedings of the National Academy of Sciences, USA 109: 5756-5760.
16. Jansson M, Blomqvist P, Jonsson A, Bergström AK. 1996. Nutrient limitation of bacterioplankton, autotrophic and mixotrophic phytoplankton, and heterotrophic nanoflagellates in Lake Örträsket. Limnology and Oceanography 41: 1552-1559.
17. Johnson MD. 2011. The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynthesis Research 107: 117-132.
18. Jones H. 1997. A classification of mixotrophic protists based on their behaviour. Freshwater Biology 37: 35-43.
19. Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblizek M, Rathgeber C, Falkowski PG. 2001. Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292: 2492-2495.
20. Kovacs L, Wiessner W, Kis M, Nagy F, Mende D, Demeter S. 2000. Short- and long-term redox regulation of photosynthetic light energy distribution and photosystem stoichiometry by acetate metabolism in the green alga, Chlamydobotrys stellata. Photosynthesis Research 65: 231-247.
21. Kröger M, Müller-Langer F. 2011. Impact of heterotrophic and mixotrophic growth of microalgae on the production of future biofuels. Biofuels 2: 145-151.
22. Laemmli UK. 1970. Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227: 680-685.
23. Maberly SC, Ball LA, Raven JA, Sültemeyer D. 2009. Inorganic carbon acquisition by chrysophytes. Journal of Phycology 45: 1052-1061.
24. Menden-Deuer S, Lessard EJ. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45: 569-579.
25. Merrett MJ. 1976. Enzyme levels in relation to obligate phototrophy in Chlamydobotrys. Plant Physiology 58: 179-181.
26. Olrik K. 1998. Ecology of mixotrophic flagellates with special reference to Chrysophyceae in Danish lakes. Hydrobiologia 370: 329-338.
27. Pålsson C, Daniel C. 2004. Effects of prey abundance and light intensity on nutrition of a mixotrophic flagellate and its competitive relationship with an obligate heterotroph. Aquatic Microbial Ecology 36: 247-256.
28. Peltier G, Cournac L. 2002. Chlororespiration. Annual Review of Plant Biology 53: 523-550.
29. +-ATP synthases from yeast and from chloroplast. Proceedings of the National Academy of Sciences, USA 109: 11150-11155.
30. Pringsheim EG. 1958. Über Mixotrophie bei Flagellaten. Planta 52: 405-430.
31. Raven JA. 1997. Phagotrophy in phototrophs. Limnology and Oceanography 42: 198-205.
32. Rothhaupt KO. 1996a. Laboratory experiments with a mixotrophic chrysophyte and obligately phagotrophic and phototrophic competitors. Ecology 77: 716-724.
33. Rothhaupt KO. 1996b. Utilization of substitutable carbon and phosphorus sources by the mixotrophic chrysophyte Ochromonas sp. Ecology 77: 706-715.
34. Sanders RW, Porter KG, Caron DA. 1990. Relationship between phototrophy and phagotrophy in the mixotrophic chrysophyte Poterioochromonas malhamensis. Microbial Ecology 19: 97-109.
35. Scheibe R. 2004. Malate valves to balance cellular energy supply. Physiologia Plantarum 120: 21-26.
36. Selosse MA, Roy M. 2009. Green plants that feed on fungi: facts and questions about mixotrophy. Trends in Plant Science 14: 64-70.
37. Stoecker DK. 1998. Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. European Journal of Protistology 34: 281-290.
38. Tcherkez G, Boex-Fontvieille E, Mahe A, Hodges M. 2012. Respiratory carbon fluxes in leaves. Current Opinion in Plant Biology 15: 308-314.
39. Tittel J, Bissinger V, Zippel B, Gaedke U, Bell E, Lorke A, Kamjunke N. 2003. Mixotrophs combine resource use to outcompete specialists: implications for aquatic food webs. Proceedings of the National Academy of Sciences, USA 100: 12776-12781.
40. Unrein F, Massana R, Alonso-Saez L, Gasol JM. 2007. Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnology and Oceanography 52: 456-469.
41. Wan MX, Liu P, Xia JL, Rosenberg JN, Oyler GA, Betenbaugh MJ, Nie ZY, Qiu GZ. 2011. The effect of mixotrophy on microalgal growth, lipid content, and expression levels of three pathway genes in Chlorella sorokiniana. Applied Microbiology and Biotechnology 91: 835-844.
42. Weis D, Brown AH. 1959. Kinetic relationships between photosynthesis and respiration in the algal flagellate Ochromonas malhamensis. Plant Physiology 34: 235-239.
43. Wiessner W, French CS. 1970. The forms of native chlorophyll in Chlamydobotris stellata and their changes during adaptation from photoheterotrophic to autotrophic growth. Planta 94: 78-90.
44. Wilken S, Huisman J, Naus-Wiezer S, van Donk E. 2013. Mixotrophic organisms become more heterotrophic with rising temperature. Ecology Letters 16: 225-233.
45. Zehr JP, Bench SR, Carter BJ, Hewson I, Niazi F, Shi T, Tripp HJ, Affourtit JP. 2008. Globally distributed uncultivated oceanic N(2)-fixing cyanobacteria lack oxygenic photosystem II. Science 322: 1110-1112.
46. Zubkov MV. 2009. Photoheterotrophy in marine prokaryotes. Journal of Plankton Research 31: 933-938.
47. Zubkov MV, Tarran GA. 2008. High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455: 224-226.