1. Phytoplankton Growth, Nutrients, and Temperature
Introduction to Biological Oceanography 2004 John Cullen (Storm-Stayed)

2. Required Reading:
McCarthy, J. J. (1981). The kinetics of nutrient utilization. In: Platt, T. (ed) Physiological Bases of Phytoplankton Ecology. p

3. What we should have learned so far
marine.rutgers.edu/opp/

4. Phytoplankton provide food energy for marine food webs and strongly influence chemical cycles in the sea
Coscinodiscus waelesii
Phytopia CD-ROM
Bigelow Laboratory

5. The measurement of light tells us much about the ocean, including distributions of phytoplankton and influences on their growth
marine.rutgers.edu/opp/

6. The major causes of variations in primary productivity are related to light and nutrients
marine.rutgers.edu/opp/

7. Because phytoplankton need light for photosynthesis and nutrients to support growth
100
200
300
400
500
600
900
1200 P B
(mol O 2
mol Chl -1 h )
Irradiance (µmol m-2 s-1)
net
gross
respiration
carbohydrates
Photosynthesis
Lipids
Protein
nucleid acids

8. Light + Nutrients  Growth  Consumption
The Growth and Chemical Composition of
Phytoplankton is a Major Driver of
Ocean Chemistry
Light + Nutrients  Growth  Consumption
Nutrients  Decomposition
Bottom

9. Chemical Composition of Phytoplankton (protein is a major constituent)
Like the form of nutrient for growth, the chemical composition of phytoplankton can vary

10. Generalized reactions for growth on nitrate and ammonium
Stoichiometry depends on N source and chemical composition of phytoplankton
Generalized reactions for growth on nitrate and ammonium
Understand and remember the definition and significance of the photosynthetic quotient, PQ

11. Growth on CO2 and the Macronutrients N and P
It is convenient (and often necessary) to consider the growth and decomposition of an “average” phytoplankter. Redfield (Redfield, Ketchum and Richards 1963) showed strong and profound relationships between dissolved elements that were consistent with the growth and decomposition of phytoplankton:
C:N:P ~ 106:16:1 - Termed the Redfield Ratios
Nitrate and phosphate to proteins, phospholipids, nucleotides, etc. …the implicit PQ is 1.30

12. Micronutrients (Trace Elements)
e.g.,
Cu, Zn, Ni, Co, Fe, Mo, Mn, B, Na, Cl
Generally, these are required to act as cofactors in enzymes (Ferredoxin [Fe], Flavodoxin [Mn], Carbonic Anhydrase [Zn])
Iron is well recognized as being in short supply over large parts of the ocean. It is particularly important in Nitrogen Fixation. Copper, Zinc and Nickel have also been implicated in influencing the growth of open-ocean phytoplankton. Trace element interactions are complex, and incompletely understood.

13. One of our jobs is to describe how light, nutrients, and temperature influence the photosynthesis, growth, and chemical composition of phytoplankton. Quite a job!

14. Temperature
Eppley, R. W Temperature and phytoplankton growth in the sea. Fish. Bull. 70:
When light and nutrients are not limiting, growth rate is a function of temperature. No one species grows at all the temperatures found in the oceans. Nonetheless, it seems that one general function can provide some indication of the maximum potential growth rate of phytoplankton as a function of temperature. Some species do quite well even though they do not reach the maximum. Perhaps they minimize losses or maximize the utilization of nutrients.

15. Temperature Effects in the Ocean
Eppley
1972
Banse, K Zooplankton: Pivotal role in the control of ocean production. ICES J. mar. Sci. 52:
The growth-rate-vs-temperature relationship described by Eppley has been used as a benchmark for quantifying the degree to which growth rates were below maximal. Hazardous indeed!

16. Nutrients and Growth
Growth of phytoplankton depletes nutrients consistent with their chemical composition
Growth cannot continue when nutrients run out
When one nutrient is depleted first, unbalanced growth can proceed
We need to know how growth conditions and nutrient limitation affect chemical composition and growth rates of phytoplankton

17. Effects of Nutrient Concentration: Michaelis-Menten Kinetics
N: Nitrate (NO3-), ammonium (NH4+), urea (CO[NH2]2)
Nitrate predominates in the deep ocean, and is delivered to surface waters by mixing and upwelling. Ammonium and urea are regenerated nutrients. Ammonium is converted to nitrate by nitrification, largely in the deep ocean.
also Phosphate, Silicate, Trace elements
It makes sense that the efficiency and capacity of nutrient uptake can have a strong influence on competitive success
Dugdale, R. C Nutrient limitation in the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12:
McCarthy, J. J The kinetics of nutrient utilization, p. 83–102. In T. Platt [ed.], Physiological Bases of Phytoplankton Ecology.

18. also Phosphate, Silicate, Trace elements
N: Nitrate (NO3-), ammonium (NH4+), urea (CO[NH2]2)
Nitrate predominates in the deep ocean, and is delivered to surface waters by mixing and upwelling. Ammonium and urea are regenerated nutrients. Ammonium is converted to nitrate by nitrification, largely in the deep ocean.
also Phosphate, Silicate, Trace elements
It makes sense that the efficiency and capacity of nutrient uptake can have a strong influence on competitive success
Dugdale, R. C Nutrient limitation in the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12:
McCarthy, J. J The kinetics of nutrient utilization, p. 83–102. In T. Platt [ed.], Physiological Bases of Phytoplankton Ecology.

19. also Phosphate, Silicate, Trace elements
Nutrient-uptake
kinetics and
ecological/evolutionary
selection
It was subsequently demonstrated that phytoplankton isolated from oligotrophic environments had lower Ks values than phytoplankton from eutrophic environments (consistent with prediction based on ecological theory)
N: Nitrate (NO3-), ammonium (NH4+), urea (CO[NH2]2)
Nitrate predominates in the deep ocean, and is delivered to surface waters by mixing and upwelling. Ammonium and urea are regenerated nutrients. Ammonium is converted to nitrate by nitrification, largely in the deep ocean.
also Phosphate, Silicate, Trace elements
It makes sense that the efficiency and capacity of nutrient uptake can have a strong influence on competitive success
Dugdale, R. C Nutrient limitation in the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12:
McCarthy, J. J The kinetics of nutrient utilization, p. 83–102. In T. Platt [ed.], Physiological Bases of Phytoplankton Ecology.

20. also Phosphate, Silicate, Trace elements
However:
Nutrient uptake experiments are generally performed under unnatural conditions.
Procedure for measuring nitrate uptake kinetics: a culture is grown on nitrite (easy to measure) until the point of depletion, then subsamples are supplemented with different concentrations of nitrate; the initial rate of uptake is then determined and described as a function of initial concentration.
The complication arises because the phytoplankton are in unbalanced growth, adjusting physiologically to changing conditions as the experiment is performed.
(In the field, nitrate and ammonium assimilation is
measured with 15N tracers)
N: Nitrate (NO3-), ammonium (NH4+), urea (CO[NH2]2)
Nitrate predominates in the deep ocean, and is delivered to surface waters by mixing and upwelling. Ammonium and urea are regenerated nutrients. Ammonium is converted to nitrate by nitrification, largely in the deep ocean.
also Phosphate, Silicate, Trace elements
It makes sense that the efficiency and capacity of nutrient uptake can have a strong influence on competitive success
Dugdale, R. C Nutrient limitation in the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12:
McCarthy, J. J The kinetics of nutrient utilization, p. 83–102. In T. Platt [ed.], Physiological Bases of Phytoplankton Ecology.

21. Nutrient kinetics for growth (rather than for uptake) are more difficult to determine: experiments involve growth in chemostat culture
Ks < 0.1 µg-at L-1
The kinetic model for growth as a function of nutrient concentration is different than that for uptake. At almost all growth rates, nutrient concentration can be below the limit of detection. Still, it is generally believed that the function is hyperbolic, as suggested by better methods for measuring nitrate:
Garside, C., and H. E. Glover Chemiluminescent measurements of nitrate kinetics: I. Thalassiosira pseudonana (clone 3H) and neritic assemblages. J. Plankton Res. 13 Suppl.: 5-19.

22. The chemostat work produced another type of nutritional pattern that was easier to measure: Cell Quota
The kinetic model for growth as a function of nutrient concentration is different than that for uptake. At almost all growth rates, nutrient concentration can be below the limit of detection. Still, it is generally believed that the function is hyperbolic, as suggested by better methods for measuring nitrate:
Garside, C., and H. E. Glover Chemiluminescent measurements of nitrate kinetics: I. Thalassiosira pseudonana (clone 3H) and neritic assemblages. J. Plankton Res. 13 Suppl.: 5-19.
from Droop, in McCarthy, 1981
Algal growth could be described as a function of internal stores of a limiting nutrient.

23. Consequently, chemical composition responds to growth conditions
N-Limited <——> N-sufficient
The chemical composition of phytoplankton is very responsive to growth conditions. Here, nitrogen content is lower when growth rate is limited by the supply of N (carbohydrates are accumulated).

24. A consequence of variable cell quota (e. g
A consequence of variable cell quota (e.g., N cell-1) is that even if nutrient uptake per cell (nmol N cell-1 h-1) is constant as a function of nutrient limitation, the maximum specific rate of nutrient uptake (Vm; µg-at N (µg-at cell N)-1 h-1) will increase with nitrogen limitation.
The kinetic model for growth as a function of nutrient concentration is different than that for uptake. At almost all growth rates, nutrient concentration can be below the limit of detection. Still, it is generally believed that the function is hyperbolic, as suggested by better methods for measuring nitrate:
Garside, C., and H. E. Glover Chemiluminescent measurements of nitrate kinetics: I. Thalassiosira pseudonana (clone 3H) and neritic assemblages. J. Plankton Res. 13 Suppl.: 5-19.
from McCarthy, 1981

25. Two reasons for “luxury uptake”
Enhanced uptake per
cell under nutrient
limitation
Reduced Cell Quota
at lower growth rates
see Morel, F. M. M Kinetics of nutrient uptake and growth in phytoplankton. J. Phycol. 22:

26. Kinetics of uptake vs for growth are not the same
Ks for growth < 0.1 µg-at L-1
Uptake Growth

27. Photoacclimation affects chemical composition
High Light
Low Light L E P L P S S E
This is balanced growth
Geider, R. J., H. L. MacIntyre, and T. M. Kana A dynamic model of photoadaptation in phytoplankton. Limnol. Oceanogr. 41: 1-15.
P = Photosynthate
E = Enzymes
Sizes of arrows are proportional to flux:
Sizes of boxes  pool size  growth rate
S = Storage
L = Light Harvesting
after Geider et al. 1996

28. Photoacclimation and P vs E

29. Chemical composition responds to growth conditions
N-Limited <——> N-sufficient
The chemical composition of phytoplankton is very responsive to growth conditions. Here, nitrogen content is lower when growth rate is limited by the supply of N (carbohydrates are accumulated).

30. Chemical composition responds to growth conditions
N-Limited <——> N-sufficient
Carbon content is also higher when irradiance is higher.
How does chemical composition change?

31. Source (light absorption) exceeds sink (synthesis of proteins)
Unbalanced growth
High —> Low
Low —> High L E P L P S S E
Low —> High:
Source (light absorption) exceeds sink (synthesis of proteins)
High —> Low:
Sink exceed source
Measures of relative storage such as carbohydrate:protein, C:chlorophyll and C:N are high under conditions of relatively low nutrient supply, low temperature, or high irradiance (source exceeds sink). Models (e.g. by RJ Geider and colleagues) now capture the essence of this regulation, predicting acclimated chemical composition and changes during unbalanced growth.
Pigment synthesis inhibited
Synthesis of enzymes cannot
accelerate quickly
Photosynthate goes to storage
Pigment synthesis continues
Synthesis of enzymes slows
because supply is reduced
Stored carbon is mobilized into
free sugars
see Geider et al. 1996

32. Unbalanced Growth
When nitrogen ran out (day 6), photosynthesis continued, but C was stored as starch. Growth was unbalanced, and much different than “Redfield”. When N was supplied, starch was used, protein was synthesized, and Redfield was restored.
When we measure growth in the field, we do not generally know if balanced growth is occurring.

33. Chemical composition responds to growth conditions
A central tendency is toward Redfield:
C:N = 6.6 by atoms
C:Chl of about 50
Higher light, N or P limitation:
C:Chl goes up
Further reading: Geider, R.J. (1987). Light and temperature dependence of the carbon to chlorophyll a ratio in microalgae and cyanobacteria: implications for physiology and growth of phytoplankton. New Phytol. 106:1-34.

34. Chemical composition responds to growth conditions
Lower temperature is like higher light
N limitation:
C:N goes up
P limitation:
C:P goes up
Further reading: Goldman, J.C. (1980). Physiological processes, nutrient availability, and concept of relative growth rate in marine phytoplankton ecology. In: Falkowski P.G., (ed.) Primary Productivity in the Sea. Plenum, New York, pp

35. Summary
Phytoplankton are microscopic organisms that provide food for life in the sea.
They do this by growing (cell division). This requires
Light
CO2
major nutrients (N, P, and Si for some), and
micronutrients (including Fe)
The growth process is fueled by
Photosynthesis and Nutrient Assimilation

36. Summary Phytoplankton cells are composed of
Protein (cellular structure and enzymes: contains N)
Carbohydrate (energy storage)
Lipids (energy storage, membranes)
…and other stuff
The relative proportions of these constituents change between taxa and with physiological state or nutrient limitation. That alters the stoichiometry of nutrient assimilation and growth. This stoichiometry strongly influences biogeochemical cycles in the sea.