Phosphate utilization by an oceanic diatom in phosphorus‐limited chemostat culture and in the oligotrophic waters of the central North Pacific1

Thalassiosira pseudonana from the oligotrophic waters of the central North Pacific Ocean was grown in phosphorus-limited chemostat culture. When the chemical composition of the cells, expressed as ratios, was compared with that of nitrogen-limited cultures, several of these ratios varied in excess of a factor of five between the two systems. Among these, which emerged as diagnostic indicators of phosphorus-starvation vs. nitrogen-deficiency, were the C : P, N : P, P : Chl a and Chl a : ATP ratios. The physiological responses of a population were determined by its preconditioning history. The minimum cellular phosphorus content, go, varied with the degree of phosphorus starvation. The rate of phosphate uptake at a saturating concentration of phosphate by phosphorus-limited cultures of T. pseudonana exceeded the rates of uptake by nonphosphorus-limited cultures by an order of magnitude; the K, for phosphate uptake was not a function of phosphorus deficiency. Phytoplankton in phosphorus-starved chemostat cultures on medium made with central North Pacific Ocean water did not USC naturally occurring dissolved organic phosphorus despite the presence of cell-surface alkaline phosphatase. Phosphate uptake by natural phytoplankton assemblages in the central North Pacific was measured with JaP. Uptake rates in the field were not significantly affected by light intensity. No circadian periodicity in uptake rates was detected in natural phytoplankton or algae cultured on a light/dark cycle. In the midninetcenth century von Licbig formulated the principle that the maximum population size or maximum yield of plant material was controlled by a single factor, such as “a” limiting nutrient. Brandt (cite&! in Gran 1912) observed that this principle also applied to the regulation of phytoplankton organic production by soluble nutrients. Under specified conditions in a batch culture in the laboratory, which can be considered as analogous to the agronomist’s cxpcrimcntal plot, a maximum population density of algae can easily be reached. 1 This research was supported by National Science Foundation grant GA-31167X, R. W. Eppley, Principal Investigator. Portions of this research were also supported by a National Science Foundation graduate fellowship and by the Women’s International Fishing Association. Ship time was supported by the National Science Foundation block-funded ship-time grant to the Scripps Institution of Oceanography for “Biological work at sea” and the National Scicnco Foundation Alpha Helix program. Contribution from Scripps Institution of Oceanography. ’ Present address : Department of Oceanography, University of Washington, Seattle 98195. Howcvcr, in the ocean maximal phytoplankton biomass or numbers of cells are generally not observed, because factors such as grazing (McAllister et al. 1960) and mixing ( Riley 1942) constantly remove a portion of the po,pulation. Consequently the rates at which the phytoplankton grow become important, as does a knowledge of the mechanisms controlling these rates. A more recent interpretation of Liebig’s law of the minimum cxtcnds this classi& concept to include the regulation or control of phytoplankton growth rate by “the” limiting nutrient (see O’Brien 1972). In the ocean nitrogen has been considcrcd to limit phytoplankton growth rate. However, in the central gyre of the North Pacific, studies of the physiology of the phytoplankton suggested that two nutrients might potentially limit phytoplankton growth rate: phosphate and nitrogen. Conccntrations of both were extremely low in these waters; inorganic phosphate was often undctcc table ( Armstrong 1972). Alkaline phosphatase localized outside the cell membrane is indicative of phosphorus deficiency LIMNOLOGY AND OCEANOGRAPIIY 88 JANUARY 1976, V. 21( 1) Phosphate utilization 89 (Torriani 1960); this enzyme was occasionally detected associated with the phytoplankton of the mixed layer in the central North Pacific, suggesting that these phytoplankton wcrc at times phosphorus-starved (Perry 1972). 0 ne nutrient enrichment expcriment in these waters, based on the 14C incorporation tcchniquc of Goldman (1960), required the addition of both phosphorus and nitrogen to obtain a growth response above that of the unenriched controls (Epplcy ct al. 1973). The experiments rcportcd here were dcsigned primarily to find trends useful for diagnosing the nutritional status of phytoplankton in the field-specifically the phytoplankton of the central gyre of the North Pacific Ocean. The chemostat proved to be well suited to the study of phosphorus limitation of marine phytoplankton at several levels of P starvation. Field experiments on phosphate utilization by natural phytoplankton in the central North Pacific were done with 33P as a tracer . I wish to thank R. W. Eppley for the use of his chemostat facilities and for advice and discussions. I wish also to thank M. M. Mullin for reading the manuscript and for assistance at sea, J, Beers and E. Renger are acknowledged for their shipboard assistance, J. Jordan for purifying clone 66-A of Thalassiosira pseudonana, J, Sharp for access to unpublished particulate carbon and nitrogen data, E. Vcnrick for USC of unpublished chlorophyll a data, and F. Azam for many discussions.