What is the limit for photoautotrophic plankton growth rates?

Journal of Plankton Research

Volumn 39, Issue 1, 2017, Pages 13-22

  Flynn, Kevin J ^a   Raven, John A ^b,c  

^a SWANSEA UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Microalga; Phytoplankton; RuBisCO; Specific growth rate; Temperature

Indexed keywords

BIOGEOCHEMISTRY; ENZYME ACTIVITY; GROWTH RATE; MICROALGA; NUTRIENT LIMITATION; PHOTOAUTOTROPHY; PHYTOPLANKTON;

EID: 85014681019     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbw067     Document Type: Article

References (46)

1. Behrenfield, M. J. and Falkowski, P. G. (1997) A consumers guide to phytoplankton primary productivity models. Limnol. Oceanogr., 42, 1479-1491.
2. Bišová, K. and Zachleder, V. (2014) Cell-cycle regulation in green algae dividing by multiple fission. J. Exp. Bot., 65, 2585-2602 doi:10.1093/jxb/ert466.
3. Clark, D. R., Flynn, K. J. and Owens, N. J. P. (2002) The large capacity for dark nitrate-Assimilation in diatoms may overcome nitrate limitation of growth. New Phytol., 155, 101-108.
4. Cuhel, R. L., Ortner, P. B. and Lean, D. R. S. (1984) Night synthesis of protein by algae. Limnol. Oceanogr., 29, 701-744.
5. Davidi, D., Noor, E., Liebermeister., W., Bar-Even, A., Flamholz, A., Tummler, K., Goldenfeld, M., Shlomi, T. et al. (2016) Global characterization of in vivo enzyme catalytic rates and their correspondence to in vitro Kcat measurements. Proc. Natl. Acad. Sci. USA, 113, 3401-3406.
6. Droop, M. R. (1974) The nutrient status of algal cells in continuous culture. J. Mar. Biol. Assoc. U.K, 54, 825-855.
7. Ellis, R. J. (1979) Most abundant protein in the world. Trends Biochem. Sci., 4, 241-244.
8. Eppley, R. W. (1972) Temperature and phytoplankton growth in the sea. Fish. Bull., 70, 1063-1085.
9. Flynn, K. J. and Fasham, M. J. R. (2003) Operation of light-dark cycles within simple ecosystem models of primary production and the consequences of using phytoplankton models with different abilities to assimilate N in darkness. J. Plankton Res., 25, 83-92.
10. Flynn, K. J. and Hipkin, C. R. (1999) Interactions between iron, light, ammonium and nitrate; insights from the construction of a dynamic model of algal physiology. J. Phycol., 35, 1171-1190.
11. Flynn, K. J. and Martin-Jézéquel, V. (2000) Modelling Si-N limited growth of diatoms. J. Plankton Res., 22, 447-472.
12. Flynn, K. J., Clark, D. R. and Owens, N. J. P. (2002) Modelling suggests that optimization of dark nitrogen-Assimilation need not be a critical selective feature in phytoplankton. New Phytol., 155, 109-119.
13. Flynn, K. J., Raven, J. A., Rees, T. A. V., Finkel, Z., Quigg, A. and Beardall, J. (2010) Is the growth rate hypothesis applicable to microalgae? J. Phycol., 46, 1-12. DOI:10.1111/j.1529-8817.2009.00756.x.
14. Flynn, K. J., Stoecker, D. K., Mitra, A., Raven, J. A., Glibert, P. M., Hansen, P. J., Granéli, E. and Burkholder, J. M. (2013) Misuse of the phytoplankton-zooplankton dichotomy: The need to assign organisms as mixotrophs within plankton functional types. J. Plankton Res., 35, 3-11. doi:10.1093/plankt/fbs062.
15. Flynn, K. J., Clark, D. R., Mitra, A., Fabian, H., Hansen, P. J., Glibert, P. M., Wheeler, G. L., Stoecker, D. K. et al. (2015) Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession. Proc. R. Soc. B, 282, 20142604, http://dx. doi.org/10.1098/rspb.2014.2604.
16. Geider, R. J. and La Roche, J. (2005) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur. J. Phycol., 37, 1-17.
17. Gilstad, M. and Sakshaug, E. (1990) Growth rates of ten diatom species from the Barents Sea at different irradiances and day lengths. Mar. Ecol. Prog. Ser., 64, 169-173.
18. Halsey, K. H. and Jones, B. M. (2015) Phytoplankton strategies for photosynthetic energy allocation. Annu. Rev. Mar. Sci., 7, 265-297. doi:10.1146/annurev-marine-010814-015813.
19. Holt, M. G. and Smayda, T. J. (1974) The effect of daylength and light intensity on the growth rate of the marine diatom Detonula confervacea (Cleve) Gran. J. Phycol., 10, 231-237.
20. Hopkinson, B. M., Young, J. N., Tansik, A. L. and Binder, B. J. (2014) The minimal CO2-concentrating mechanism of Prochlorococcus spp. MED4 is effective and efficient. Plant Physiol., 166, 2205-2217.
21. Ichimi, K., Kawamura, T., Yamamoto, A., Tada, K. and Harrison, P. J. (2012) Extremely high growth rate of the small diatom Chaetoceros salsugineum isolated from an estuary in the eastern Seto inland sea, Japan. J. Phycol., 48, 1284-1288. DOI:10.1111/j.1529-8817.2012. 01185.x.
22. Kenny, P. and Flynn, K. J. (2014) In silico optimization for production of biomass and biofuel feedstocks from microalgae. J. Appl. Phycol., 27, 33-48. doi10.1007/s10811-014-0342-2.
23. Kruskopf, M. and Flynn, K. J. (2006) Chlorophyll content and fluorescence responses cannot be used to gauge reliably phytoplankton biomass, nutrient status or growth rate. New Phytol., 169, 525-536.
24. Laws, E. A. (2013) Evaluation of in situ phytoplankton growth rates: A synthesis of data from varied approaches. Annu. Rev. Mar. Sci., 5, 247-268. DOI:10.1146/annurev-marine-121211-172258.
25. Mitra, A., Flynn, K. J., Tillmann, U., Raven, J. A., Caron, D., Stoecker, D. K., Not, F., Hansen, P. J. et al. (2016) Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition; incorporation of diverse mixotrophic strategies. Protist, 167, 106-120, http://dx.doi.org/10.1016/j.protis.2016.01.003.
26. Mortain-Bertrand, A., Descolas-Gros, C. and Jupin, H. (1988) Patterns of dark inorganic carbon fixation in two species of diatoms: influence of light regime and regulator factors on diel variations. J. Plankton Res., 10, 199-217.
27. Molendijk, A. J., Van Egmond, P., Haringf, M. A., Klis, F. M. and van den Ende, H. (1992) Characterization of the cell cycle in synchronous cultures of Chlamydomonas eugametos in relation to gametogenesis. J. Gen. Microbiol., 138, 1941-1947.
28. Nelson, D. M. and Brand, L. E. (1979) Cell division periodicity in 13 species of marine phytoplankton on a light:dark cycle. J. Phycol., 15, 67-75.
29. Nicklisch, A., Shatwell, T. and Köhler, J. (2008) Analysis and modelling of the interactive effects of temperature and light on phytoplankton growth and relevance for the spring bloom. J. Plankton Res., 30, 75-91.
30. Raven, J. A. (2013a) Rubisco: still the most abundant protein in Earth? New Phytol., 198, 1-3.
31. Raven, J. A. (2013b) RNA function and phosphorus use by photosynthetic organisms. Frontiers Plant Sci., 4, 536.
32. Raven, J. A. (2015) Implications of mutation of organelle genomes for organelle function and evolution. J. Exp. Bot., 66, 5639-5650.
33. Raven, J. A. and Ralph, P. J. (2015) Enhanced biofuel production using optimality, pathway modification and waste minimization. J. Appl. Phycol., 27, 1-31. doi:10.1007/s10811-0140323-.
34. Raven, J. A., Beardall, J., Larkum, A. W. D. and Sánchez-Baracaldo, P. (2013) Interactions of photosynthesis with genome size and function. Phil. Trans. R. Soc. B, 368, 20120264.
35. Read, B. A. and Tabita, F. R. (1994) High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial RuBisCO containing "algal" residue modifications. Arch. Biochem. Biophys., 312, 210-218.
36. Reynolds, C. S., Harris, G. P. and Gouldney, D. N. (1985) Comparison of carbon-specific growth rates and rates of cellular increase of phytoplankton in large limnetic enclosures. J. Plankton Res., 7, 791-820.
37. Rost, B., Riebesell, U. and Söltemeyer, D. (2006) Carbon acquisition of marine phytoplankton: Effect of photoperiod length. Limnol. Oceanogr., 51, 12-20.
38. Shi, T., Bibby, T. S., Jiang, L., Irwin, A. J. and Falkowski, P. G. (2005) Protein interactions limit the rate of evolution of photosynthetic genes in cyanobacterial. Mol. Biol. Evol., 22, 2179-2189.
39. Smith, V. H. and McBride, R. C. (2015) Key ecological challenges in sustainable algal biofuels production. J. Plankton Res., 37, 671-682. doi:10.1093/plankt/fbv053.
40. Suggett, D. J., MacIntyre, H. L., Kana, T. M. and Geider, R. J. (2009) Comparing electron transport with gas exchange: parameterising exchange rates between alternative photosynthetic currencies for eukaryotic phytoplankton. Aquat. Microbial Ecol., 56, 147-162.
41. Tcherkez, G. G., Farquhar, G. D. and 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.
42. Thompson, P. A., Levasseur, M. E. and Harrison, P. J. (1989) Lightlimited growth on ammonium vs. nitrate: What is the advantage for marine phytoplankton? Limnol. Oceanogr., 34, 1014-1024.
43. Westberry, T., Behrenfeld, M. J., Siegel, D. A. and Boss, E. (2008) Carbon-based primary productivity modelling with vertically resolved photoacclimation. Glob. Biogeochem. Cycles, 22, GB2024, doi:10.1029/2007GB003078.
44. Young, J. N., Rickaby, R. E. M., Kapralov, M. V. and Filatov, D. A. (2012) Adaptive signals in algal Rubisco reveal a history of ancient carbon dioxide. Phil. Trans. R. Soc. B, 367, 483-492.
45. Young, J. N., Heureux, A. M. C., Sharwood, S. E., Rickaby, R. E. M., Morel, F. M. M. and Whitney, S. M. (2016) Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms. J. Exp. Bot., doi:10.1093/jxb/erw1633.
46. Zorz, J. K., Allanach, J. R., Murphy, C. D., Roodvoets, M. S., Campbell, D. A. and Cockshutt, A. M. (2015) The RUBISCO to photosystem II ratio limits the maximum photosynthetic rate in picocyanobacteria. Life, 5, 403-417. doi:10.3390/life5010403.