SENFT_ W. HERBERT. Dependence of light-saturated rates of algal

					Limnol. Oceanogr.,  23(4), 1978, 709-718
@ 1978, by the American    Society of Limnology     and Oceanography,     Inc.

Dependence       of light-saturated                                 rates of algal photosynthesis
on intracellular    concentrations                                  of phosphorus
W. Herbert           Senftl
Department         of Ecology     and Behavioral         Biology,       University   of Minnesota,   Minneapolis   55455

           Specific rates of photosynthesis      at saturating irradiances (PO,J by laboratory populations        of
        Chlorella   and Anabaena depend on intracellular            phosphorus (Q). A hyperbolic      model of the
        form Popt = PoptR (1 -&/Q)      is used to describe this relationship         for three measurements      of
        biomass (cell number, cell volume, and chlorophyll                a). Chlorophyll    a provides the most
        adequate fit to the model. When chlorophyll           a is used as the measure of population size, both
        the maximal specific rate of photosynthesis             (PO,:) and the subsistence cell quota (Ka) for
        Anabaena are much larger than for Chlorella.               The model provides a conceptual         basis for
        understanding    the relationship     between rates of photosynthesis       and intracellular  nutrients in
        populations   of planktonic    algae.

    Laboratory investigations         have shown                             difficult to measure (Jassby and Goldman
 that growth rates of algal populations          de-                         I975), even though they may be impor-
pend on cellular levels of limiting              nu-                        tant in determining          species dominance
trients. Mackereth (1953) observed that                                      and succession        (Porter 1973; O’Brien
the growth rate of the freshwater diatom                                     1974). This means that the relationship            of
Asterionella     .formosa is related to its in-                             growth to cellular nutrients must be re-
tracellular     phosphorus       level. Caperon                              examined in terms of a fundamental             pro-
 (1968) showed that the growth rate of the                                   cess that can be measured in situ in order
marine alga lsochrysis galbana could be                                     to analyze the effects of nutrients on nat-
hyperbolically       related to the inferred cel-                           ural populations.
lular nitrate pool size, and Droop (1968)                                       It seems highly probable that the de-
 observed a similar hyperbolic            relation-                         pendence of growth rates on intracellular
 ship between the growth rate of Mono-                                      nutrients     in laboratory      populations      re-
chrysis Zutheri and intracellular          concen-                          flects a more fundamental dependence of
trations     of vitamin      Bj2. Fuhs (1969)                               photosynthesis       on intracellular    nutrients.
proposed an exponential equation for the                                    A decrease       in photosynthesis           corre-
relationship        that he found between                                   sponding to a lowered growth rate asso-
growth rates of Cyclotella nana and Thal-                                   ciated with nutrient deficiency has been
assiosira $uviatilis        and cellular      phos-                         described by Healey (1973), Eppley and
phorus concentrations.        The relationships                             Renger (1974), and Pickett (1975). Since
between growth rate and intracellular                                       photosynthesis      supplies the energy stores
nutrient     concentrations     have also been                              and carbon skeletons used in growth, it
described by hyperbolic functions (Droop                                    is important to examine the relationship
 1973; Rhee 1973; Tilman and Kilham                                         between photosynthesis           and cellular nu-
 1976).                                                                     trients. Because rates of photosynthesis
    These relationships      were discerned by                              are easily measured in the field, these re-
analyzing      growth rates of algal popula-                                lationships,    unlike those for growth, can
tions in batch, continuous, or semicontin-                                  then be applied to natural populations.
uous culture. Growth is a net process in-                                       I have investigated       the photosynthetic
volving both production           and loss terms,                           characteristics       of a blue-green        and a
Under laboratory conditions,           population                           green alga in response to changes in in-
losses are well controlled. A lake, in con-                                 tracellular    phosphorus       and have found
trast, often has large loss factors that are                                major differences       in the photosynthetic
                                                                            responses of these algae to a fixed nutri-
  ’ Present address: Department                   of Biology,       Ball    tional status.
State University, Muncie, Indiana                 47306.                        I thank R. Megard for advice and en-
710                                            Senft

couragement. E. Gorham, J. Shapiro, D.              is the highest possible rate that a popu-
Tilman, and three anonymous reviewers               lation could attain; as the physiology            of
criticized   the manuscript,    J. Settles, J,      the population        approaches      an “ideal”
Balogh, and M. Balogh helped with lab-              state, Popt -+ PoptS.(In a similar manner,
oratory work. R. Thrift developed          the      P max + Pmax” as the algal cells become
simplex portion of the computer program.            nutrient saturated.) Both Popt and PoptSare
J. Wood and the Freshwater         Biological       measured, short term, specific rates of
Research Foundation       provided     labora-      photosynthesis       obtained under constant
tory space, computer facilities, and finan-         illumination     at a specified temperature.
cial support. A portion of this work was                It was assumed that the relationship
also supported       by ERDA        contract        between measured specific rates of pho-
E( 1 l-1)-1820 to R. Megard.                        tosynthesis at saturating irradiances (Popt)
                                                    and intracellular       concentrations      (Q) of
Theory                                              nutrients is analogous to the relationship
                                                    between growth and cellular nutrients.
     The specific rate of photosynthesis            at
                                                    As intracellular    concentrations     of the lim-
saturating light is an important physio-            iting nutrient increase, the rate of pho-
logical measure of the photosynthetic              ca-
                                                    tosynthesis approaches the nutrient-sat-
pability of phytoplankton.          It is referred   urated rate (Popts). Furthermore,              the
to as the maximal rate of photosynthesis,            intracellular   nutrient concentration       must
P max, in mathematical       equations used to       exceed a subsistence level (Ka) in order
describe and predict the photosynthesis-            for photosynthesis       to occur. The KQ value
light relationships     of algae (Smith 1936;        for gross photosynthesis         does not equal
Steele 1962; Vollenweider             1965; Jassby   the KQ value for growth since at zero
and Platt 1976). In those equations which            growth rate gross photosynthesis           (equal
incorporate photoinhibition,           the value of  to at least respiration)      still occurs. Two
P max is usually much larger than the mea-           equations relating light-saturated        rates of
sured light-saturated     rate of photosynthe-       photosynthesis     and levels of intracellular
sis because of the way in which photo-               nutrients, based on two previously            pub-
inhibition    is built into the mathematical         lished models of growth (Fuhs 1969;
expression. Vollenweider          (1965) and Fee      Droop 1968), are proposed:
 (1969) introduced the term P,,t, the opti-
 cal rate of photosynthesis,      to differentiate               popt = &,,9[1 _ 2-I(O-W&1],        (1)
the measured light-saturated            rate of pho-
 tosynthesis from the theoretical light-sat-            and
 urated rate, Pm,,. Popt and P,,, become                           f’wt = po,,“(1 - f&/Q).          (2)
 synonymous       in those equations that do
 not incorporate      photoinhibition         (Smith    These equations represent the first for-
  1936; Jassby and Platt 1976).                         mulations    of the relationship     of photo-
     These definitions     of PoPt and Pm,, do          synthesis to cellular nutrient levels.
 not imply any knowledge            about the nu-                                                          E
 tritional   state of the algal population.             Methods
 When dealing with the effects of nutrient
 limitation    on the magnitude of light-sat-              Axenic cultures of Anabaena cf. wis-
 urated rates of photosynthesis,            we need     consinense Prescott Univ. Nebraska col-
  more precise terminology              and I have      lection NU No. 41,~ md Chlorella           pyr-
  used the following     definitions       here. The    enoidosa     Chick (’ i-th Carolina       Biol.
  optimal specific rate of photosynthesis,              Supply Co. No. 15-L 470) were cultivated
 P Ogt,is the rate of photosynthesis         attained   in modified BGll          ,dla (Stanier et al.
  under saturating light conditions. It var-            1971). Stock culture        were kept under
  ies according to the physiological          state of continuous       fluorest :nt lighting    (0.30
  the algal population,      The nutrient-satu-         Ein. rnA2. h-l) in 250-ml flasks containing
  rated specific rate of photosynthesis,          Pop?, BGll with a 1.6 PM ?-PO4 concentration
                                          Intracellular       phosphorus                                    711

 and used to inoculate glass carboys con-                     equations     of Strickland     and Parsons
 taining 9 liters of 6.5 pM P-PO4 BGll                        (1965). Samples were filtered onto 0.45-p
 medium adjusted to pH 7.2. These batch                       glass-fiber filters, ground in 90% acetone,
 cultures were stirred with a magnetic                        and extracted for 10 min. Subsamples of
 stirrer and bubbled with sterile air at a                    algae were preserved with Lugol’s solu-
 flow rate of -0.1 liter.minBi                under con-      tion and counted on an inverted micro-
 tinuous white fluorescent                 light (==0.43      scope.
 Ein. rno2. h-l) at a temperature                of 23” rt       Concentrations    of phosphorus were de-
 1°C. The cultures were harvested 48-192                      termined    on filtered (0.45-p pore size)
 h after inoculation          and checked for con-            samples (Am. Public Health Assoc. 1971)
 tamination      by plating onto a bacto-agar                 with ascorbic acid as the reducing agent.
 medium. By choosing the time of harvest,                     Four analytical fractions of cellular phos-
 algal cells with various levels of cellular                  phorus were separated. Total cellular
 phosphorus could be obtained, since the                      phosphorus was assumed to equal partic-
 population was required to share a finite,                   ulate P, which was measured after diges-
 and eventually         limiting,     supply of P04.          tion with K2S208 in an autoclave for 45
 All other nutrients           were present in ex-            min (Menzel and Corwin 1965). Surplus
 cess.                                                        P, a measure of luxury phosphorus stored
    Rates of photosynthesis           and respiration         as cellular polyphosphates,     was extracted
 were estimated from changes in concen-                       according      to Fitzgerald     and Nelson
 trations of oxygen in transparent                    and     (1966) with 0.05 M Tris buffer (pH 7.7).
 opaque BOD bottles (300-ml capacity).                        The acid-soluble       phosphorus    fraction,
 Replicate transparent and opaque bottles                     which contains acid-soluble       7-min poly-
 were exposed to a range of light intensi-                    phosphates, ortho P, nucleotidic      labile P,
ties in an incubator similar to that de-                      and polyphosphate      A, was extracted with
 scribed by Fee (1973). In initial experi-                    10% TCA at 4°C for 45 min (Kanai et al.
 ments,       four       600-W         quartz-iodide           1965); the supernatant was then digested
photoflood       lamps were used as a light                   as in particulate P. Free inorganic phos-
source; in later experiments                  two of the      phorus in the cells-cellular-ortho          P-
 quartz-iodide        lamps were replaced by                  was measured by adding acid-washed,
 750-W self-ballasted                mercury        vapor     activated charcoal to the supernatant ob-
lamps. Both light sources provided                        a   tained from TCA-treated      samples and as-
range of light intensities great enough to                    saying immediately       for PO4 (Terry and
produce a complete photosynthesis-light                       Hooper 1970).
(P vs. I) relationship.             Spectral changes
associated with the different light sources
                                                              Rem1 ts
do not significantly            alter the photosyn-
thetic response of these algae (Senft et al.                      Relationships    between gross photosyn-
in prep.). Incubation           lasted for about 2 h          thesis and light for batch cultures of An-
at 23” -r- 1°C. 0 xygen in the BOD bottles                    abaena and Chlorella          are illustrated    in
was determined             titrimetrically        by the      Fig. 1. Both species show large variations
azide modification           of the Winkler proce-            in photosynthesis-light        curves as a func-
dure (Am. Public Health Assoc. 1971).                          tion of cellular phosphorus. Phosphorus
    Irradiance was measured with an un-                        nutrition   influences    the rates of photo-
derwater quantum sensor (Lambda Instr.                         synthesis     at saturating     irradiances.    In
Co.) fitted with a specially                   designed       Chlorella, the highest light-saturated         rate
spherical       collector        developed         by W.       measured is more than twice the lowest;
Combs. In general, the light intensity re-                     the highest light-saturated         rate in Ana-
ceived by any bottle in the incubator var-                    baena is more than three times the low-
ied by no more than 10% as it rotated                          est. The range of light saturation             for
through the light field.                                      Chlorella     is wide, 0.75-6.0 Ein. rne2. h-l,
    Concentrations         of chlorophyll         a were       much narrower (0.75-1.75 Ein. rnw2. h-‘)
determined         from the SCORKJNESCO                        for Anabaena.       Photosynthesis        in Ana-
712                                                                                            Senft

                                                                                                   plied by the user. The error function cho-
                                                           ANABAENA                                sen here was a least-squares fit of the
                                                                                                                      9 (Y
                                                                                                                              -   YtJ2,               (3)
                                                                                                   where the differences             between experi-
                                                                                                   mental (y) and predicted (yt) points are
                                                                                                   squared and summed for all points (n).
                                                                                                   Values of yt less than zero were set equal
%                                                                                                  to zero, since rates of gross photosynthe-
                   I      I          I       I       I          I               1          1       sis, unlike rates of growth, can never be
                                                                                                   negative. If values of yt are allowed to be
 k                                                                                                 negative, the theoretical           curve is forced
  s. 0.6
                                                          CHLORELLA                                through the datum point with the lowest
                                                                                                   cell quota (QmJ since yt + --OOif KQ >
  Li                                                                      Q=135
                                                                                                   Q min. Theoretical considerations             of sim-
  EO’                                                                     Q=74
                                                                                                   plex optimization         are detailed elsewhere
  z                                                                                                (Spendley et al. 1962; Nelder and Mead
 “0                                                                 x      Q=15                    1965; Deming and Morgan 1973; Morgan
 6                                                                                                 and Deming 1974; King et al. 1975). On
 2    0.2
                                                                           Q=3                     the basis of two criteria (visual compari-
                                                                                                   son and the magnitude of the error func-
                                                                                                   tion, Eq. 3), the hyperbolic model (Eq. 2)
            0      1      2
                                     3      4
                                                     I          I               I          I   J
                                                                                                   provides a better fit for all the observed
                                                                6               7          8   9
                  LIGHT         INTENSITY        ( Einrteinr-           m-‘-h       -’ I           relationships.       Further discussion here is
   Fig. 1. Photosynthesis-light    curves for batch                                                limited to this model.
cultures of Anabaena and Chlorella     with different                                                  Three measurements             of biomass (cell
cellular phosphorus levels, Q (nmoles P*pg Chl-‘),                                                 number, cell volume, and chlorophyll                a)
Vertical bars represent 95% confidence limits cal-                                                 were used to estimate population               levels
culated from pooled variance of light and dark bot-                                                in the cultures. Cell number (identified
tles. Curves are hand drawn.
                                                                                                   by asterisks) and cell volume (identified
                                                                                                   by primes) were chosen because they are
baena is inhibited       at high illumination,                                                     widely used estimates of algal densities
decreasing       to only 60% of the light-                                                         in laboratory populations.            Chlorophyll     a
saturated rate at intensities        of 6.0 Ein.                                                   was chosen for two reasons: it is an im-
m-2. h-1                                                                                           portant photosynthetic           pigment, and it is
    Equations 1 and 2 were evaluated by                                                            a practical measure of biomass for natural
using the photosynthetic          responses of                                                     phytoplankton          populations.    The concep-
Anabaena and ChZoreZZa to various levels                                                           tual model (Eq. 2) was tested separately
of intracellular    phosphorus. Popt was cho-                                                      using each of these parameters.
sen as the highest rate of gross photosyn-                                                             Optimal rates of gross photosynthesis                 .
thesis measured in a P vs. I curve, since                                                          and cellular phosphorus levels per indi-
the curves from the photosynthesis              in-                                                vidual alga are shown in Fig. 2. Both the
cubator always included            at least one                                                    minimal       cell quota, &*(lO+             pmoles
point in the light-saturated       region. Best-                                                    Pm individual-l)       and the maximum rate of
fit values for the two parameters (Pop? and                                                         photosynthesis,         Pop:*( low7 pmoles 0,.
KQ) of both models were found with a                                                                individual-l     - h-l) for Anabaena are much
computer program incorporating             a sim-                                                   larger than the values for Chlorella.
plex optimization      procedure. This meth-                                                        This might be expected since an indi-
od simultaneously        optimizes values for                                                       vidual Anabaena            is composed of sev-
the parameters of a theoretical         relation-                                                   eral cells (i.e. a filament) as opposed to
ship by minimizing       an error function sup-                                                    the single-celled         Chlorella . The experi-
                                                                              Intracellular                              phosphorus                                                                    713

                                                                           PS * = 2.37
        2.90 -
                                                                             K&= 0.68


                                                                          PS *
                                                                             op,   q    0.97

                                                                          K;=          0.07

                                 l          l
                                                                                                                                                                                   KQ=     2.9

                                I                I                         1                           I                       II                   I               I           I                      I         I
                0               1.2             2.4                       3.6                      4.8                         0                                               150                   200
                        PARTICULATE             Q*          (IO-B   pmoles P.             individual                 )                        PARTICULATE      6”       (nmolesP     Kg-Chl-’    )

    Fig. 2. Light-saturated   rates of gross photosyn-                                                                              Fig. 4.             As Fig. 2, for Pop? and KQ.
thesis vs. particulate phosphorus for Anabaena and
Chlorella.  Values of P,Pc* and KQ* are best-fit re-
sults from simplex optimization     of hyperbolic mod-
                                                                                                                          rate of gross photosynthesis,   Pop:’ (lo-l1
mental results for either species, how-                                                                                   pmoles Oz. prnm3* h-l), is lower for Ana-
ever, do not provide a close fit to the                                                                                   baena than for ChZoreZZa. Minimal         cell
model.                                                                                                                    quotas, I&‘( lo-l1 flmoles P~prn-~), are
   The relationship  is different if cell vol-                                                                            similar in the two species.
ume is used as the estimate of population                                                                                     The clearest expression of the relation-
size (Fig. 3). In this case, the maximal                                                                                  ship defined by Eq. 2 is provided when
                                                                                                                          chlorophyll    a is used to measure popu-
                                                                                                                          lation size (Fig. 4). This can be seen by
                                                                         ANABAENA                                         performing a linear transformation     of the
    19.4c                                                                                                      I          model. Equation 2 can be rewritten          in
                                                                                                                          the form

                                                                                                                                    p   opt     =      -
                                                                                                                                                    POPtS       (PoPtK2wQ).                                (4)

                                                                                                                          Plotting Popt vs. l/Q yields a straight line
                                                                                                                          with y-intercept     PoptS and x-intercept
                                                                                                                           l/&. Estimates of Pop? and Ke obtained
                                                                                                                          in this manner are only marginally        dif-
                                                                                                                          ferent from those of simplex optimiza-
                                                                                                                          tion. Values of the correlation coefficient,
                                                                           P&(         = 20.6
                                                                                                                          r, for Anabaena from the regression using
                                                                                                                          cell number, cell volume, and chloro-
                                                                                                                          phyll a as the measure of population size
                                                                                                                          are 0.66, 0.71, and 0.86. Chlorophyll        a
            0             1.2         2.4                         3.6                 4.8                      6.0        also provides     a better correlation     for
                      PARTICULATE      Q’                ( lo-”     gmoles         P. pmm3 )                              Chlorella   (r = 0.73) than either cell vol-
                    Fig. 3.     As Fig. 2, for P&’                         and I&‘.                                       ume (r = 6.71) or cell number (r = 0.56).
714                                                                                                             Senft

          0.70   t

    90                                                                         CHLORELLA
     $0.70       -


                                                                                      P&,       = 0.36

                                                                                      K0 = 1.5

                                   I               I                      I                           I
                 0                20              40                     60                          80         100                         l
                                 SURPLUS      Q        ( nmobs      P pg-Chl-’         )
                                                                                                                           I-         I             I             I               I
          Fig. 5.            As Fig. 4, but vs. surplus phosphorus.                                                        0         50           100            150            200
                                                                                                                                    PARTICULATE         Q   i nmoler   Chl-’   )
                                                                                                                         Fig. 7. Respiration rates as a function of partic-
   The estimates of Pop: (kmoles 02*pg                                                                                ulate phosphorus for Anabaena and ChZoreZZu.
Chl-l-h-l)   and KQ (nmoles P*pg Chl-l)
show large differences between species
(Fig. 4). Anabaena    has a much higher                                                                               fractions of the total particulate pool are
maximal rate of gross photosynthesis   than                                                                           examined. For surplus P (Fig. 5), Ana-
Chlorella. The minimal particulate P cell                                                                             baena has a higher maximal rate of pho-
quota for Chlorella   is much lower than                                                                              tosynthesis    and a higher minimal           cell
that for Anabaena.                                                                                                    quota than Chlorella.       In Chlorella,      the
   Values of Pop{ and KQ for these two spe-                                                                           estimates of the photosynthetic          parame-
cies show the same relationship       when                                                                            ters for acid-soluble     P compounds         and
                                                                                                                      cellular-ortho    P (Fig. 6) are almost iden-
                                                                                                                      tical with the estimates for surplus P
                                                                                                                      compounds (Fig. 5). This is not surpris-
                                                                                                                      ing since the analytical        separations      of
                                                                                                                      these fractions are not physiologically
          0 35
                                                                                                                      precise. In theory, the estimates of Popt
                                                                                                                      for a species obtained from plots of POPt
I                                                                                                                     vs. different phosphorus fractions should
                                                                                                                      be identical. The estimates of Pop: from
                             CELLULAR-ORTHO            Q         ( nmoks      P-pg Chl“               1
                                                                                                                      Figs. 4, 5, and 6 agree reasonably well
                                                                                                                      within both species. Although           the data
                                                                                                                      for surplus, acid-soluble,     and cellular-or-
    ~070-                                                                                                             tho P show a much closer agreement to
                                                                                                                      the theoretical model, values of particu-
      ^a                                                                                   .                          late P seem to provide an adequate mea-
     op                           .
           035       -                                                                                                sure of the nutritional    condition of these
                                                                                 k=            2.0
                                                                                                                         Rates of respiration     by the two algal
                         I             I           I                      I                           I               species show different        relationships      to
                                      20          40                     60                          80         100
                               ACID-SOLUBLE            Q     ( nm&s           Pepg Chl-’              )               intracellular   levels of phosphorus         (Fig.
    Fig. 6.                   As Fig. 4, but vs. acid-soluble                                             and cel-    7). Specific rates of respiration        (pmoles
lular-ortho                   phosphorus for Chlorella.                                                               02- pg Chl-l. h-l) of ChZoreZZa are unre-
                                      Intracellular    phosphorus                                       715

lated to cellular phosphorus. The regres-                 ADP, and to a lesser extent AMP, also
sion of respiration on cellular phosphorus                stimulate O2 evolution when added to the
in Anabaena is significant, however.                      chloroplasts. The increase in oxygen evo-
                                                          lution from the pea chloroplasts is a hy-
                                                          perbolic function of the amount of ATP
     These results show that photosynthesis                   For the work reported here, the com-
 in algal populations       is a function of cel- parison of photosynthetic                  responses de-
 lular phosphorus        nutrition.      The hyper-       pends on the unit used to measure pop-
 bolic form of this relationship,           similar to ulation size. When chlorophyll              a is used
 that of growth to cellular nutrition,            is not as a biomass estimate, Anabaena shows
 a foregone conclusion because there are a much higher specific rate of gross pho-
 many metabolic         processes involved            in tosynthesis and a much higher minimal
 growth other than photosynthesis                (respi-  concentration       of cellular      phosphorus
 ration, cell division, etc.). A limiting            nu- than Chlorella.      If, however, cell volume
 trient may control a process such as cell                is used as the biomass estimate, the op-
 division and so control the rate of growth.              posite situation holds. Since the amount
 These other processes may in turn regu-                  of chlorophyll    per unit biomass can fluc-
 late the photosynthetic             rate by some tuate widely              (Steele and Baird 1961,
 feedback mechanism.             Nor need an in- 1962; Kuenzler and Ketchum 1962; Ep-
 creased rate of photosynthesis              induce a pley and Renger 1974), rates of photosyn-
 parallel   increase in growth rate. End                  thesis are very dependent            on the chlo-
 products of photosynthesis              may simply       rophyll:biomass       ratio, Variations in this
 accumulate or leak out of the cell if the ratio can obscure the functional                          depen-
 proper nutrients       for protein synthesis,            dency of photosynthesis          on intracellular
 DNA replication,        or cell wall synthesis           concentrations     of nutrients.
 are lacking. We need to know more about                      Comparisons of photosynthetic           values
 the relationship    of cellular growth to cel- P opt ’ and KQ) with corresponding                   growth
 lular photosynthesis         in laboratory         cul-  parameters (j.~,,, an d KJ are not easily
tures.                                                    made. Several broad conclusions can be
     The mechanism responsible for the ob- reached, however. Regardless of the bio-
 served photosynthetic          responses of cells        mass measure used, the responses ofAn-
to increased phosphorus               levels is un- abaena and Chlorella               to a fixed level of
known. One plausible              mechanism         may cellular phosphorus do differ dramatical-
be a precursor-product             reaction. Phos- ly. This suggests that each algal species
phorus-containing          precursors          can be may have a characteristic Popt and KQ val-
maintained       at higher levels (yielding              ue, analogous to Rhee’s (1973) concept of
faster reaction rates) when Q is large;                  specific values for growth parameters.
such precursors might include the nu- Whether this difference is characteristic
cleotides, ATP, ADP, and AMP, and in- of green and blue-green algae remains to
organic polyphosphates.             Miyachi       et al. be seen. If such differences are the rule
(1964) have suggested that under photo-                  in natural systems, they would lend sup-
synthetic conditions polyphosphates                 “C”  port to the ideas of Grenney et al. (1974)
and “A” serve as intermediates                  in the and Tilman (1977) that the outcome of
transfer of phosphate to the phosphate-                  competition      between       two species de-
containing     compounds          synthesized.       At- pends on rates of both nutrient uptake
kinson (1968) proposed that the levels of and nutrient utilization.
AMP and ADP can influence the rate of                        The relationship      of gross photosynthe-
reactions involving       ATP synthesis. Rob- sis and cellular phosphorus shown here
inson and Wiskich (1976) have shown                      provides a basis for understanding               the
that the oxygen evolution of isolated pea role that nutrients play in the growth and
cholorplasts      is stimulated        from two to maintenance             of phytoplankton         popula-
twelve times by the addition                  of ATP.    tions. Previous studies on the constancy
716                                                                              Senft

                                                                                                                                           Cpl 10.71              [’       0 121

                                                                                                                                               KQ-    15 6

                                                                                                              A                                  I                             1
  k4   0         5                 10                  15                  20
                                                                                       P      0              30           60                    90                         120
 0                                                           -I                                       PARTICULATE       Q-’      (pg     Chl     .pmole           P-’      )
                 cl-’       ( mg C ‘mg       organic     N        )                      0”

                                                                                              I   1           I          I                       I                          I
                                                                                              0              50         100                     150                        200
       0        200                400                 600                 800
                                                                  -1                                  PARTICULATE   Q         ( nmoles       Chl-’        )
                        Q   ( pg   organic      N . mg       C         )

   Fig. 8. Photosynthesis     vs. organic nitrogen con-                                 Fig. 9. Optimal photosynthesis          vs. particulate
tent of’Phormidium     molle: A-linear   transformation                              phosphorus      for Halsted Bay, Lake Minnetonka,
of hyperbolic    model; B-hyperbolic       model. Value                               1974: A-linear     transformation    of hyperbolic    mod-
in brackets is 95% confidence limit for PoptS.                                       el; B-hyperbolic       model. Value in brackets is 95%
                                                                                     confidence limit of Popts. Optimal rates of photosyn-
                                                                                     thesis (P,,J were calculated       from photosynthesis-
                                                                                     depth curves of half-day incubations in situ.
of the photosynthesis:Chl:light          relation-
 ship have produced conflicting            results,
The data presented here clearly indicate                                             Brown’s (1973) data on oxygen evolution
that the photosynthetic         efficiency     of a                                  by Phormidium        molle, I found a hyper-
chlorophyll     unit is not constant, as as-                                         bolic relationship      similar to those dis-
sumed by Tett et al. (1975) in their anal-                                           cussed here (Fig. 8). Changes in the spe-
ysis of Chl:C ratios in marine phyto-                                                cific rates of gross photosynthesis      of algae
plankton,      but rather varies with the                                            during development          of a large phyto-
nutritional    state of the algal population.                                        plankton    bloom in Halsted Bay (Lake
Equation 2 represents an explicit formu-                                             Minnetonka)      corresponded to changes in
lation of the dependence of light-saturat-                                           the cellular phosphorus levels of the al-
ed rates of gross photosynthesis         on inter-                                   gae (Megard in prep.). This population,
nal nutrient          stores.    Mathematical                                        comprised predominantly            of Aphanixo-
representations       of photosynthesis-light                                        menon flos-aquae          (K. Baker unpub-
relationships     in phytoplankton      do not in-                                   lished), has a photosynthesis-nutrient
corporate     this functional       dependency                                       curve resembling       that of Anabaena (cf.
and so a new photosynthesis-light                ex-                                 Fig. 4 and 9B). It has a high nutrient-sat-
pression is needed (Senft in prep.).                                                 urated photosynthetic         rate and a high
    These results are not unique to the two                                          minimal cell quota (Fig. 9A). In this one
algae studied nor to phosphorus as a lim-                                            case, photosynthesis-nutrient           relation-
iting nutrient.     Keenan and Auer (1974)                                           ships found in the laboratory            for one
reported changes in the rate of photosyn-                                            blue-green     alga are in good agreement
thesis of Anabaena jlos-aquae             cells as                                   with those of a mixed blue-green popu-
levels of extractable         phosphorus        de-                                  lation in nature. Further interpretations
creased. When I replotted             Daley and                                      of natural phytoplankton       processes should
                                               Intracellular           phosphorus                                                    717

be possible as photosynthesis-nutrient                                 KANAI, R., S. AOKI, AND S. MIYACHI. 1965. Quan-
                                                                           titative separation of inorganic p0lyphoSpllates
relationships for different algal species                                   in Chlorella     cells. Plant Cell Physiol. 6: 467-
become known.                                                              473.
                                                                       KEENAN, J. D., AND M. T. AUER. 1974. The influ-
                                                                            ence of phosphorlls          luxury uptake on algal
References                                                                 bioassays. J. Water Pollut. Contr. Fed. 46: 532-
AMERICAN PUBLIC HEALTI~ ASSOCIATION. 1971.                             KING, P. G., S. N. DEMING, AND S. L. MORGAN.
    Standard methods for the examination                of water            1975. Difficulties      in the application         of simplex
    and wastewater,        13th cd.                                         optimization     to analytical chemistry. Anal. Lett.
ATKINSON, D. E. 1968. The energy charge of the                              8: 369-376.
    adenylate pool as a regulatory              parameter. Zn-         KUENZLER, E. J., AND B. II. KETCIUJ;~~. 1.962. Rate
    teraction with feedback modifiers. Biochemis-                           of phosphorus        uptake by Phaeodactylum                tri-
    try 7: 4030-4034.                                                      corn&urn.      Biol. Bull. 123: 134-145.
CAPERON, J. 1968. Population               growth response of          MACKERETH, F. J. 1953. Phosphorus utilization                     by
    Isochrysis     galbana to nitrate variation at lim-                    Asterionella     formosa. J. Exp. Bot. 4: 296-313.
    iting concentrations.          Ecology 49: 866-872.                MENZEL, D. W., AND N. CORWIN. 1965, The mca-
DALEY, R. J., AND S. R. BROWN. 1973. Chlorophyll,                           surement of total phosphorus in seawater based
    nitrogen,     and photosynthetic           patterns during              on the liberation      of organically bound fractions
    growth and senescence of two blue-green                      al-        by persulfate oxidation. Limnol. Oceanogr. 10:
     gae. J. Phycol. 9: 395-401.                                            280-282.
DEMING, S. N., AND S. L. MORGAN. 1973. Simplex                         MIYACIII, S., R. KANAI, S. MIIIAFU, S. MIYACIII,
    optimization      of variables in analytical chemis-                    AND S. AOKI. 1964. Metabolic roles of inorgan-
    try. Anal. Chem. 45: 278A-283A.                                         ic polyphosphates        in Cldorella       cells. Biochim.
DROOP, M. R. 1968, Vitamin B,, and marine ecol-                             Biophys. Acta 93: 625-634.
    ogy. 4. The kinetics of uptake, growth, and in-                    MORGAN, S. L., AND S. N. DEMING. 1974. Simplex
     hibition in Monochrysis            Zutheri. J. Mar. Biol.              optimization      of analytical        chemical methods.
     Assoc. U.K. 48: 689-733.                                               Anal. Chem. 46: 1170-1181.
-.         1973. Some thoughts on nutrient limitation                  NELDER, J. A., AND R. MEAD. 1965. A simplex
     in algae. J, Phycol. 9: 264-272.                                       method for function minimization.               Computer J.
EPPLEY, R. W., AND E. H. RENGER. 1974. Nitrogen                             7: 308-313.
    assimilation     of an oceanic diatom in nitrogen-                 O’BRIEN, W. J. 1974. The dynamics of nutrient lim-
     limited continuous culture. J. Phycol. 10: 1%                          itation of phytoplankton          algae: A model recon-
     23.                                                                    sidered. Ecology 55: 135-141.
FEE, E. J. 1969. A numerical model for the esti-                       PLCKETT, J. M. 1975, Growth of Chlorella                    in a ni-
     mation of photosynthetic            production,    integrat-           trate-limited      chemostat.         Plant Physiol.       55:
     cd over time and depth, in natural water. Lim-                         223-225.
     nol. Oceanogr. 14: 906-911.                                       PORTER, K. G. 1973. Selective grazing and diffcr-
-.          1973. A numerical model for determining                         ential digestion of algae by zooplankton.                   Na-
     integral primary production            and its application             ture 244: 179-180.
     to Lake Michigan.           J. Fish. Res. Bd. Can. 30:            RIIEE, G-Y. 1973. A continuous                 culture study of
      1447-1468.                                                            phosphate uptake, growth rate, and polyphos-
FITZGERALD, G. P., AND T. C. NELSON. 1966. Ex-                              phate in Scenedesmus sp. J. Phycol. 9: 494-
     tractive and enzymatic analysis for limiting                 or        506.
     surplus phosphorus in algae. J. Phycol. 2: 32-                    ROBINSON, S. P,, AND J. T. WISKICII. 1976. Stim-
     37.                                                                    ulation of carbon dioxide fixation in isolated
FUHS, G. W. 1969. Phosphorus content and rate of                            pea chloroplasts       by catalytic amounts of ade-
     growth in the diatoms Cyclotella                 nana and              nine nucleotides.       Plant Physiol. 58: 156-162.
    Thalassiosira     jluviatilis.     J. Phycol. 5: 312-321.          SMITH, E. L. 1936. Photosynthesis                  in relation to
GRENNEY, W. J., D. A. BELLA, AND H. C. CURL,                                 light and carbon dioxide. Proc. Natl. Acad. Sci.
     JR. 1974. Effects of intracellular          nutrient pools              22: 504-511.
     on growth dynamics of phytoplankton,                J. Water      SPENDLEY, W., G. R. HEXT, AND F. R. HIM-
     Pollut. Contr. Fed. 46: 1751-1760.                                      SWORTH. 1962. Sequential application                   of sim-
HEALEY, F. P. 1973. Inorganic nutrient uptake and                            plex designs in optimization             and evolutionary
     deficiency in algae. Crit. Rev. Microbial.             3: 69-           operation. Technometrics             4: 441-461.
      113.                                                             STANIER, R. Y., R. JUNISAWA, M. MANDEL, AND G.
JASSBY, A. D., AND C. R. GOLDMAN. 1975. LOSS                                 COHEN-BAZIRE.          1971. Purification          and prop-
     rates from a phytoplankton              community.       Lim-           erties of unicellular       blue-green         algae {order
     nol. Oceanogr. 19: 618-627.                                             Chroococcales).       Bacterial.       Rev. 34: 171-205.
-,         AND T. PLATT. 1976. Mathematical                     for-   STEELE, J. II. 1962. Environmental                control of pho-
     mulation of the relationship          between photosyn-                 tosynthesis    in the sea. Limnol. Oceanogr. 7:
     thesis and light for phytoplankton.                 Limnol.             137-I 50.
     Oceanogr. 2 1: 540-547.                                           -,         AND I. E. BAIRD. 1961.. Relations between
718                                                      Senft

     primary production,      chlorophyll   and particu-      TILMAN, D. 1977. Resource competition        between
     late carbon. Limnol. Oceangr. 6: 67-68.                      planktonic algae: An experimental     and theoret-
-,AND--.                 1962. Carbon-chlorophyll       re-       ical approach. Ecology 38: 338-348.
     lations in cultures. Limnol. Oceangr. 7: 101-            -3       AND S. KILHAM. 1976. Phosphate and sili-
      102.                                                        cate growth and uptake kinetics of the diatoms
STRICKLAND, J. D., AND T. R. PARSONS. 1965. A                     Asterionella   formosa and Cyclotella    meneghi-
     manual of seawater analysis. Bull. Fish. Res.                niana in batch and semicontinuous       culture. J.
     Bd. Can. 125.                                                Phycol. 12: 375-383.
TERRY, K. R., AND A. B. HOOPER. 1970. Polyphos-               VOLLENWEIDER, R. A. 1965. Calculation       models of
     phate and orthophosphate       content of Nitrosom-          photosynthesis-depth     curves and some impli-
     onus europaea as a function of growth. J. Bac-               cations regarding day rate estimates in primary
     teriol. 103: 199-206.                                        production    measurements.    Mem. 1st. Ital. Id-
TETT, P., J. C. COTTRELL, P. 0. TREW, AND B. J.                   robiol. 18(suppl.):   425-457.
     WOOD. 1975. Phosphorus quota and the chlo-
     rophyll:carbon    ratio in marine phytoplankton.                         Submitted: 2 February           1977
     Limnol. Oceanogr. 20: 587-603.                                          Accepted: 14 November            1977

Shared By: