The interaction between ammonium and nitrate uptake in phytoplankton

A basic tenet of nitrogen utilization in phytoplankton is that ammoniuln inhibits nitrate uptake. Consequently, it is generally believed that little or no nitrate uptake occurs at ammonium concentrations above ca 1 yM. A thorough review of field studies shows that the reduction of nitrate uptake rate in the presence of ammonium is rarely so severe, and that it is a highly variable phenomenon. To simplify quantification of the interaction between nitrate and ammonium uptake, it is proposed that it be divided into an indirect interaction, preference, and a direct effect, inhibition. In order to determine preference and inhibition it is necessary to measure uptake of each inorganic nitrogen source alone and in the presence of increasing concentrations of the other nitrogen source. Preference for ammonium uptake is manifested primarily in a higher V,,,,, and lower K, for ammonium uptake than for nitrate uptake and is accentuated by low light and low nitrogen availability. However, although ammonium is the preferred nitrogen source for uptake, growth rates on nitrate usually equal or exceed those on ammonium. Inhibition of nitrate uptake by ammonium is much more variable, but when separated from preference is less extreme. I t is also enhanced by low light, but unlike preference, i t is greater when phytoplankton are N sufficient. Species differences are apparent for both preference and inhibition, but there are only enough data for preference to determine how it varies among algal groups. Finally, there are reports of low concentrations of ammonium stimulating nitrate uptake and of nitrate inhibiting ammonium uptake. Such unexpected interactions along with variations in preference and inhibition with species composition and environmental conditions may account for the variability observed in field studies and will not be explainable or predictable until more is known about the underlying biochemical mechanisms. Even though it is not possible at present to model nitrate uptake accurately because of uncertainty about the interaction between ammonluln and nitrate uptake, it is quite evident that the simplistic view that nitrate uptake is reduced to zero if ammonium exceeds 1 1iM would often result in large underestimates of nitrate uptake and new production. INTRODUCTION Itis generally believed that the rateof nitrate uptake by phytoplankton is severely reduced by the presence of ammonium. This effect is referred to either as 'inhibition' of nitrate uptake by ammonium or 'preference' for ammonium, and in its most extreme form it is believed to result in no nitrate uptake above a threshold ammonium concentration of ca 1 PM. Evidence for the negative effect of ammonium on nitrate utilization arises from 3 sources: (1) early laboratory studies of nitrate utilization in freshwater green algae (reviewed in Morris 1974), (2 ) early field studies in marine ecosystems (Table l ) , and (3) theoretical considerations of the relative energy requirements for the utilization of nitrate and ammonium, due to the number of electrons required to reduce nitrate to ammonium (Losado & Guerrero 1979, Syrett 1981). In many of these early studies it was assumed that nitrate uptake (transport into the cell) and reduction were so tightly coupled that uptake of nitrate must be inhibited by ammonium because the enzyme nitrate reductase is strongly inhibited. It is now known that nitrate uptake and reduction are frequently uncoupled during transient conditions in marine phytoplankton (DeManche e t al. 1979, Dortch et al. 1979, Collos 1982) and that nitrogen uptake and assimilation are so complex that it is difficult to explain the interaction between nitrate and ammonium uptake by one simple mechanism. O Inter-Research/Printed in F. R. Germany 017 1-8630/90/0061/0183/$ 03.00 T ab le 1 . E vl cl en ce f or t he n eg at lv e ef fe ct o f a m m o n ~ u ~ n o n n it ra te u p ta k e in t he f ~ e ld . A ll r at lo s ar e th e ra n g e of v al u es o b se rv ed o r ex tr ap o la te d f or 1 1 tM a m m o n iu m , th e pu ta tl ve t hr es ho lc l fo r in h ~ b lt lo n . If n ec es sa ry , d at a w er e re pl ot te d a s a fu nc ti on o f am m o n iu m c o n ce n tr at lo n , a ft er e x tr ac t~ o n fr om t ab le s an d f ~ g u re s In o rl gi na l re fe re n ce . T h e re la ti o n sh ~ p b et w ee n a r at 10 a nc l a n in cr ea se I n th e NM : co nc en tr at io n 1s d e sc r~ b e d b y : N V , no v ar ia ti on ; L , l in ea r d ec re as e; N L , n o n -l in ea r d ec re as e; 1 , u n ab le t o d et er m in e. V r ef er s to e it h er t he s p ec ~ fl c r at e of u p ta k e (h -' ) or r at e of tr an sp or t (y m ol I' h -' ) of a pa rt ic ul ar N c o m p o u n d . A re a C a r~ h h ra n S ea E su bt ro pi ca l P ac ~ fl c 0. 05 -0 . 9 4 N V S co tl a S ea -A n ta rc t~ ca 0 . 0 1 4 ::7 N V