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

Required Reading: McCarthy, J. J. (1981). The kinetics of nutrient utilization. In: Platt, T. (ed) Physiological Bases of Phytoplankton Ecology. p. 83-102.

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

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

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

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

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 http://staff.jccc.net/pdecell/biochemistry/carbohyd.html Lipids Protein nucleid acids http://www.agen.ufl.edu/~chyn/age2062/lect/lect_02/

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

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

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

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

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.

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

Temperature Eppley, R. W. 1972. Temperature and phytoplankton growth in the sea. Fish. Bull. 70: 1063-1085. 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.

Temperature Effects in the Ocean Eppley 1972 Banse, K. 1995. Zooplankton: Pivotal role in the control of ocean production. ICES J. mar. Sci. 52: 265-277. 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!

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

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. 1967. Nutrient limitation in the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12: 685-695. McCarthy, J. J. 1981. The kinetics of nutrient utilization, p. 83–102. In T. Platt [ed.], Physiological Bases of Phytoplankton Ecology.

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. 1967. Nutrient limitation in the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12: 685-695. McCarthy, J. J. 1981. The kinetics of nutrient utilization, p. 83–102. In T. Platt [ed.], Physiological Bases of Phytoplankton Ecology.

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. 1967. Nutrient limitation in the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12: 685-695. McCarthy, J. J. 1981. The kinetics of nutrient utilization, p. 83–102. In T. Platt [ed.], Physiological Bases of Phytoplankton Ecology.

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. 1967. Nutrient limitation in the sea: dynamics, identification, and significance. Limnol. Oceanogr. 12: 685-695. McCarthy, J. J. 1981. The kinetics of nutrient utilization, p. 83–102. In T. Platt [ed.], Physiological Bases of Phytoplankton Ecology.

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. 1991. Chemiluminescent measurements of nitrate kinetics: I. Thalassiosira pseudonana (clone 3H) and neritic assemblages. J. Plankton Res. 13 Suppl.: 5-19.

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. 1991. 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.

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).

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. 1991. Chemiluminescent measurements of nitrate kinetics: I. Thalassiosira pseudonana (clone 3H) and neritic assemblages. J. Plankton Res. 13 Suppl.: 5-19. from McCarthy, 1981

Two reasons for “luxury uptake” Enhanced uptake per cell under nutrient limitation Reduced Cell Quota at lower growth rates see Morel, F. M. M. 1987. Kinetics of nutrient uptake and growth in phytoplankton. J. Phycol. 22: 1037-1050.

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

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. 1996. 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

Photoacclimation and P vs E

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).

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

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

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.

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.

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. 179-194.

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

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.