Microb Ecol (1988) 15:189-201

MICROBIAL ECOLOGY @ Springer-VerlagNew York Inc. 1988

Simultaneous Consumption of Bacteria and Dissolved Organic Matter by Tetrahymenapyriformis D a v i d Glaser* Harvard University, Museum of Comparative Zoology, 26 Oxford Street, Cambridge, Massachusetts 02138, USA Abstract. The addition o f ciliated protozoa to aquatic m i c r o c o s m s and bench-scale sewage treatment plants increases d e c o m p o s i t i o n rates. This is surprising, inasmuch as protozoa consume bacteria, which are the prim a r y decomposers. One possible mechanism o f the increase in d e c o m position rate is the direct c o n s u m p t i o n o f dissolved organic m a t t e r by protozoa that are feeding primarily on bacteria. This possibility was explored experimentally in two-stage continuous cultures, with glucose limiting Escherichia coli in the first stage and E. coli limiting Tetrahymena pyriformis in the second. Glycine and histidine were the test nutrients. The results o f adding t h e m to the second stages suggested that direct uptake by ciliates does not affect the dynamics o f dissob)ed a m i n o acids in pelagic e n v i r o n m e n t s or activated sludge plants. Ciliates might, however, affect the d))namics o f a m i n o acid pools in e n v i r o n m e n t s high in nutrients and ciliates, perhaps including some m i c r o e n v i r o n m e n t s near decomposing material or in benthic sediments. Direct uptake o f dissolved a m i n o acids by ciliates probably does not affect ciliate or bacterial populations substantially.

Introduction T h e addition o f p r o t o z o a to aquatic microcosms and bench-scale activatedsludge sewage t r e a t m e n t plants increases d e c o m p o s i t i o n rates [ 10, 15, 21, 36]. This result is surprising, inasmuch as protozoa c o n s u m e bacteria, which are the p r i m a r y decomposers. One possible m e c h a n i s m o f the increase in decomposition rate is the direct c o n s u m p t i o n o f dissolved organic matter (DOM) by p r o t o z o a that are feeding primarily on bacteria. Curds et al. [10] considered this possibility, and it has been d e m o n s t r a t e d to occur in r u m e n ciliates [5]. H o w e v e r , this hypothesis does not appear to have been tested experimentally with free-living aerobic p r o t o z o a [8]. In this study, the ability o f Tetrahymena pyriformis G L to consume D O M while feeding on bacteria was investigated. 7". pyriform& a freshwater ciliated

* Present address: Columbia University College of Physicians and Surgeons, Department of Microbiology, 701 W. 168th Street, New York, NY 10032.


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protozoan with world-wide distribution [ 12], can be grown on bacteria [31 ] or axenically in proteose peptone or a defined medium [28]. Uptake kinetics of amino acids and sugars in axenic suspensions of this species have been determined [22]. Therefore, it is physiologically possible for T. pyriformis to consume both bacteria and DOM. T. pyriformis is easy to culture, and much is known about its growth characteristics [9, 11, 22]. Two-stage continuous cultures were used to measure the consumption of dissolved amino acids by T. pyriformis growing primarily on Escherichia coli and to measure the population effects of this consumption (Fig. 1). The first stage of each culture contained bacteria, and the second stage, bacteria and protozoa. Sterile minimal medium with growth-limiting glucose flowed into the first stage, and the first-stage effluent flowed into the second stage. The test nutrient was added to the second stage. Nutrient consumption was measured by observing amino acid concentrations, and effects on populations were determined by comparing densities with and without the addition of amino acids. In one experiment, glycine (an amino acid not required by T. pyriformis) was added in a single pulse (Fig. la). In a second experiment, histidine (a required amino acid) was added continuously to one culture, while a second culture served as a control (Fig. lb). Materials and M e t h o d s

Experimental Organisms and Nutrients The culture o f T. pyriformis was obtained from A. G. Frederickson (Chemical Engineering Department, University of Minnesota, Minneapolis); it was derived from the stock culture used by Watson et al. [42]. Amino acids were chosen as test nutrients because potentially they could act as carbon and nitrogen sources. One essential amino acid (histidine [28]) and one nonessential amino acid (glycine) were used. These were added at high (millimolar) concentrations to increase the probability of protozoan consumption. E. eoli can support the growth o f T. pyriformis [27]. Strain EO2512, a K12 derivative, was obtained from Dale Oxender (Department of Biological Chemistry, University of Michigan, Ann Arbor).

Medium The medium was a modified version of the defined minimal medium of Tsuchiya et al. [41], prepared in 10 liter batches. Solution A contained KzHPO4, 31 g; KH2PO4, 19 g; NaMoO,. 2H20, 0.01 g; FeSO4.7H20, 0.01 g; EDTA, 0.004 g; (NH4)2SO4, 12.5 g; and distilled water, 9 liters. Solution B contained MgSO4' 7H20, 1.0 g; NaC1, 0.1 g; CaCl2, 0.2 g; and distilled water, 1 liter. The pH of solution A was adjusted to 7.0 with concentrated H2SO4- Both solutions were filtered through Whatman GF/C filters and autoclaved. They were combined with cool. A concentrated solution of glucose in distilled water, filtered through a sterile 0.22/~m millipore filter, was then added.

Apparatus Four glass culture vessels (Bellco Glass), modeled after Tsuchiya et al. [41] and Novick and Szilard [33], were used. They were assembled into two two-stage continuous cultures to avoid the oscil-

Consumption of Bacteria and DOM by Tetrahymena

Sterile I

/ t~


! 91

Pulse addition glycine





.... ~-~

la) Olycine


Fig. 1. Experimental design for two-stage continuous culture systems for the (a) glycine experiment and (b) histidine experiment. B, bacteria; P, protozoa; G, glycine; H, histidine.




with histldine





lations that can occur in single-stage predator-prey continuous cultures [3, 27]. Culture volume was 500 ml; the vessels were 25.5 cm-taU cylinders with rounded bottoms. Sterile, humidified air was bubbled in from below (500 ml rain -~) to aerate and mix the cultures. Dye studies showed that mixing was complete within a few seconds. Each culture vessel was enclosed in a glass water jacket. Water was pumped in series through a controlled-temperature bath and the four water jackets. Possible sources of contamination were wrapped in heating tape (Briskheat, Curtin Matheson Scientific) controlled with a variable-voltage transformer (Powerstat, Curtin Matheson Scientific). The flow rate into each first stage was controlled by gravity (range, 6.7-23 ml hour-~). Silicone tubing (length about 2 m; inside diameter 0.020 in; Manostat Corp.) slowed the rate to a drip, and it was regulated precisely by raising or lowering the carboy on a jack (Lab/Lift, Fisher Scientific Co.). The coefficient of variation o f the drip rate was about 4%. The flow out of the first stage into the second was controlled by siphon action. Occasionally, several milliliters dripped out at once and then there was no outflow for several minutes; this increased the population variation in the second stages. Average flow rate was measured by periodically weighing the outflow from the second stage and adding the amount sampled. Samples were removed with sterile pipettes and analyzed within 2 min.

Analytic Methods T. pyriformis was counted with a model ZfCoulter counter with a 100 gm aperture. When necessary, the cells were diluted in the same phosphate buffer as that in the medium. The lower threshold


D. Glaser

of the Coulter counter was set at 800 ~tm3. Mean cell size was estimated visually on the oscilloscope. Most measurements were to the nearest 400 ~tm 3. Bacterial population size in the first stage was measured as turbidity with a Perkin Elmer Model 552 spectrophotomctcr, and batch cultures were used to produce a standard curve that related optical density to grams dry weight of cells per liter. The number and size of bacterial cells were measured by staining with acridine orange [23] and observing with an Olympus model CH or an Olympus Vanox microscope adapted for epifluorescence. The cells were about 1 ocular micrometer unit wide, so only lengths were measured. Amino acid concentrations were measured with fluorescamine (Sigma Chemical Co.), a general fluorescent stain for primary amines [32], using a Turner model 110 fluorometer with excitation filter No. 405 and emissions filter No. 4. To assay for amino acids, 0.5 ml o f the culture or a dilution of it in phosphate buffer was added to 4.5 mt of borate buffer at pH 9.0, followed by 0.2 ml of fluorescamine (prepared as 20 mg in 100 ml of acetone), and fluorescence was measured. Prefiltering the sample did not affect the results of the measurement.

Experimental Design, Glycine Two two-stage continuous cultures were run at 30~ with 40/tg C ml -t of glucose in the sterile feed streams. The dilution rate was 0.046 hour-t; the maximal protozoan growth rate was 0.15 hour -t in batch culture under these conditions. To measure protozoan consumption ofglycine, a pulse o f sterile glycine in distilled water was added to each second stage at 116 hours, producing a concentration of 29 ug C ml -~ in the culture (Fig. la). To measure uptake by bacteria, a pulse was added to each first stage at 256 hours, producing 40 ug C ml -t. The consumption rate equaled the difference between the dilution rate and the rate o f decrease in the logarithm of the glycine concentration.

Experimental Design, Histidine Two two-stage continuous cultures were run at 26~ For each, a second sterile reservoir fed directly to the second stage. The reservoir feeding into the control culture contained the same phosphate buffer as in the medium; the reservoir feeding into the treatment culture contained buffer with histidine (Fig. lb). Cultures were started with 40/~g C ml -t o f glucose in the feed streams and dilution rates of 0.042 hour -). The maximal protozoan growth rate was 0.25 hour -~ in batch cultures under these conditions. The direct uptake of histidine was assayed as follows. The histidine concentration (H) in the treatment equaled the difference between the treatment and the control fluorescamine measurements. When H was significantly less than the concentration in the inflow, as determined by a t test, a maximum potential uptake rate was calculated, assuming all uptake was by the protozoa. To measure the effects of histidine, the steady state densities o f bacteria and protozoa in the treatment and control cultures were compared with t tests. Predictions of population differences were made with loop analysis [29], a method o f qualitative analysis for sets of linear differential equations. If protozoa used histidine, loop analysis predicted that the histidine treatment should have more protozoa and consequently fewer bacteria. The use of loop analysis presupposes that populations are near equilibrium. Here, a variable was assumed to be near equilibrium if the graphed trajectory showed no clear pattern of change over time, and if the regression coefficient of the variable against time was not significantly different from zero. Protozoan biovolume was considered more likely than numbers alone to respond to nutrient additions; in addition, protozoan densities in the second stages should have been linearly related to bacterial densities in the first stages, barring any effect of histidine. Therefore, a new variable was calculated by dividing protozoan biovolume (#m3(p)ml -t) by first-stage bacterial biomass (ttgC(B)ml-t):

C o n s u m p t i o n o f Bacteria a n d D O M by

P' =


~ m 3 (P) m l -~ in second stage #g C(B) m l -~ in first stage



Barring a n y effect o f histidine, P' s h o u l d be constant. Bacterial n u m b e r s were u s e d as a m e a s u r e o f d e n s i t y because in three c o m p a r i s o n s there were n o differences in cell lengths between t r e a t m e n t a n d control in first- or second-stage bacteria. A set o f four e x p e r i m e n t s was r u n over an 1800 h o u r period with breaks between experiments. T h e t i m e scales referred to below are relative to the start o f the first experiment, that is, 0 hours. E x p e r i m e n t 1 lasted 100 hours. At 105 hours, the control vessel was resterilized a n d reinoculated f r o m the t r e a t m e n t vessel; the t r e a t m e n t vessel was kept running. E x p e r i m e n t 2 lasted f r o m 170320 hours. To observe the effects o f growth rate on p r o t o z o a n feeding habits, at 320 h o u r s the dilution rates were t u r n e d d o w n to 0.0134 h o u r -~ in the t r e a t m e n t vessel a n d to 0.0143 h o u r -~ in the control. E x p e r i m e n t 3 lasted from 91 0 - 1 0 8 0 hours. T o m a g n i f y small effects, glucose was a d d e d to the reservoirs at 1210 hours, increasing the feed s t r e a m concentrations f r o m 40 to 200 #g C m l - ' . E x p e r i m e n t 4 lasted f r o m 1 4 4 0 - 1 7 6 0 hours.


Glycine Fluorescamine measurements in both stages indicated that amino acid concentrations before the addition of glycine were less than 0.5 ~tg C ml -I. Bacterial densities in the second stages were about 0.2 ~tg C ml-'. Immediately after the pulses, the glycine concentration was 40/~g C ml-' in the first stages and 29 ~tg C ml-' in the second stages. Thus, glycine was the most abundant carbon source for uptake by both populations. The log~irithm of glycine concentration was plotted (solid circles; Fig. 2) to compare the glycine disappearance rate with the dilution rate (solid lines). In all cases, glycine decreased faster than predicted by dilution alone (significant by t tests at P < 0.05); thus, some of the glycine was consumed in both stages. Assuming all uptake in the second stages was by protozoa, T. pyriformis took up 2.5 x 10 -3 #g C cell-I hour -~ [Up(Go); Equations 2 and 3, Table 1]. dG/dt = -DG

- Up(G)P

(-d[ln(G)]/dt) - D)G Up(G) = P

(2) (3)

However, that is probably overestimated in that the bacteria demonstrated their ability to use glycine in the first stages (Fig. 2). Multiplication of the firststage uptake rate [Us(Go) #g C cell -~ hour-', calculated by replacing P with B in equations 2 and 3] by the second-stage bacterial density (B2) indicates that the bacterial population was responsible for about 7% of the uptake [UB(G0)B2 = 0.035 zg C ml-' hour-'; Up(G0)P --- 0.48 ~tg C ml -~ hour-l; Table 1]. This is a minimum estimate, because bacterial uptake may have been increased by the protozoa in the second stage. Thus, T. pyriformis consumed at most 2.3 x 10 -5 #g C cell -1 hour-'. When glycine was added to the second stages, protozoan densities changed by less than 5% and bacterial densities by less than 50% (Fig. 2). Thus, although glycine was probably taken up by the protozoa, high concentrations ofglycine had negligible effects on the protozoan and bacterial populations.


D. Glaser



2.0 0.0 -2.0



PROTOZOA ceJls/ml x 1~ 4

2,0 0.0


Ld-~ -~o.0 z E

PROTOZOAN SIZE u ~ / c e i l x 10"3

4.0*********** ***5, 9

i 4.or~E



t Ig~lx~t~ ,..\;~gg:g

0.0 -2.0 4.0

BACTERIA colls/ml x



0.0 l.O


I 100

~ ,,I,

200 TIME (hours)

~' 300


400 0






-2.0 400

TIME (hourr

Fig. 2. Two-stage continuous cultures, pulse addition of glycine. Temperature 30~ Reservoir glucose concentration 40 ug C ml L Dilution rate 0.046 hour ~. For protozoa and bacteria, means and 95% confidence intervals are given. First stage bacterial density (~7), number of protozoa (D), protozoan size (*), number of second-stage bacteria (0), and In (glycine concentration) (@).

Histidine Figures 3(a), 4(a), and 5(a) contain the data from the treatment culture, and Figs. 3(b), 4(b) and 5(b) contain the data from the control culture. Histidine concentrations in the culture vessels were between 4 and 10 #g C ml-L Secondstage bacterial densities were a b o u t 0.2 tzg C ml -~. Thus, histidine was the most a b u n d a n t carbon source for p r o t o z o a n uptake. To test for equilibrium, regressions o f variables against time were calculated. Slopes for P' (Eq. 1) were o f borderline significance in experiment 2 for both cultures (t tests; 0.02 < P < 0.05), with values a b o u t 10% o f the dilution rate. All other slopes were not significantly different from zero. Therefore, equilibrium was assumed for all experiments. At 1080 hours, c o n t a m i n a n t s were observed in both cultures; the density o f

Consumption of Bacteria and DOM by Tetrahymena


Table 1. Glycine: data and calculations Culture Treatment


I st stage B~ (• 10 8) Go d(ln G)/dt Un(Go)

2.25 _+ 0.98" 2.45 _+ 0.24 40 40 -0.117 _+ 0.0115 -0.135 -4- 0.0182 1.36 x 10 8

2nd stage B2(• -6) P (• 10 4) Go d(ln G)/dt Up(Go)

2.61 + 0.75 3.10 + 0.86 1.9 + 0.04 1.9 _+ 0.04 28.8 28.8 -0.0606 _+ 0.0041 -0.0636 _+ 0.0048 2.5 • 10 5

_+95% confidence limits Variables: D = dilution rate = 0.046 hour t; B~= average bacterial density in the i~hstage (cells mI ~); P = average protozoan density (cells ml '); G = glycine concentration (tag C ml t); Go = glycine concentration immediately after pulse addition 0zg C ml ~); d(ln G)/ dt = decline slope of log of glycine concentration; Uu(G) = rate of glycine uptake by bacteria (ug C cell ~hour ~; replicates averaged); Up(G) = maximum possible rate of uptake of glycine by protozoa, based on Equation 3, not corrected for bacterial uptake (ug C cell ' hour-'; replicates averaged) the c o n t a m i n a n t s was h i g h e r in the c o n t r o l vessel t h a n i n the t r e a t m e n t vessel. T h i s m a d e n o a p p a r e n t difference to s t e a d y - s t a t e d e n s i t i e s (Fig. 4), so the c u l t u r e s were a l l o w e d to c o n t i n u e r u n n i n g . A t 1380 h o u r s , e a c h c u l t u r e was i n o c u l a t e d with 2 m l f r o m the o t h e r to h o m o g e n i z e the p o p u l a t i o n s . Bacterial d e n s i t i e s in e x p e r i m e n t 4 (Fig. 5) were n o t m e a s u r e d , b e c a u s e m u c h o f the b i o m a s s i n the t r e a t m e n t vessel was tied u p i n f i l a m e n t s , a n d the d e n s i t i e s o f p r o t o z o a i n b o t h were great e n o u g h to i n t e r f e r e w i t h b a c t e r i a l c o u n t s . I n three e x p e r i m e n t s (2, 3, a n d 4) there was a s i g n i f i c a n t r e d u c t i o n i n h i s t i d i n e . M a x i m u m p o t e n t i a l u p t a k e rates b y the p r o t o z o a were 0.10 • 10 -5 ( e x p e r i m e n t 2), 0.58 • 10 s ( e x p e r i m e n t 3), a n d 0 . 0 5 0 • 10 s/~g C cell ~h o u r ~( e x p e r i m e n t 4). T h u s , i n c r e a s i n g the d e n s i t y o f p r o t o z o a f r o m e x p e r i m e n t 3 to e x p e r i m e n t 4 d i d n o t lead to a p r o p o r t i o n a l decrease i n h i s t i d i n e . P' v a l u e s (Eq. 1) i n the t r e a t m e n t s were n o t s i g n i f i c a n t l y d i f f e r e n t f r o m c o n trols. I n e x p e r i m e n t 2, t h e b a c t e r i a l p o p u l a t i o n in the t r e a t m e n t was n o t sign i f i c a n t l y different f r o m the c o n t r o l . I n e x p e r i m e n t 1, t h e r e were fewer b a c t e r i a i n the t r e a t m e n t t h a n i n the c o n t r o l ; i n e x p e r i m e n t 3, t h e r e were m o r e . Both differences were o f b o r d e r l i n e s i g n i f i c a n c e (P ~ 0.05).


Direct Effects of Ciliates on Dynamics of Dissolved Amino Acids T h e s e e x p e r i m e n t s were d e s i g n e d to give the best p o s s i b l e c o n d i t i o n s for sim u l t a n e o u s c o n s u m p t i o n : T. pyriformis c a n live solely o n D O M ; a m i n o a c i d s


D, Glaser



2 7 0 FIRST





o~li*Imlx 164




v v vv


,:U k> U p ( G 0 ) P ; T a b l e 2]. T h i s suggests t h a t b a c t e r i a l u p t a k e in a c t i v a t e d - s l u d g e p l a n t s is m u c h greater than protozoan uptake.

Effects of Direct Uptake of Dissolved Amino Acids on Ciliate and Bacterial Populations G i v e n t h e s m a l l d i f f e r e n c e s o b s e r v e d a n d t h e high a m i n o a c i d c o n c e n t r a t i o n s u s e d , it s e e m s u n l i k e l y t h a t d i r e c t c o n s u m p t i o n o f g l y c i n e o r h i s t i d i n e b y c i l i a t e s w o u l d h a v e a s i g n i f i c a n t effect o n c i l i a t e o r b a c t e r i a l p o p u l a t i o n s in t h e field.

Other Possible Causes of the Positive Effect of Protozoa on Decomposition Rate T h i s s t u d y e x a m i n e d o n e p o s s i b l e m e c h a n i s m for p r o t o z o a n s t i m u l a t i o n o f b a c t e r i a l d e c o m p o s i t i o n . O t h e r m e c h a n i s m s i n c l u d e : (1) P r o t o z o a e x c r e t e n u t r i e n t s s u c h as n i t r o g e n a n d p h o s p h o r u s w h i c h a l l o w b a c t e r i a to u t i l i z e c a r b o n s o u r c e s m o r e fully [2, 4, 26]. (2) P r o t o z o a e x c r e t e lytic e n z y m e s [1 ]. (3) P r o t o z o a create microturbulence around bacteria, increasing nutrient and oxygen availa b i l i t y [15]. (4) I f t h e m a t e r i a l b e i n g d e c o m p o s e d is n o t a g r o w t h - l i m i t i n g nutrient, then under certain conditions, simply removing bacteria can increase t h e d e c o m p o s i t i o n r a t e [25]. (5) P r o t o z o a c o n s u m e b a c t e r i a l s p e c i e s w h i c h a r e d o m i n a n t b u t a r e inefficient n u t r i e n t c o n s u m e r s [20]. (6) P r o t o z o a p r o m o t e t h e g r o w t h o f b a c t e r i a b y c o n s u m i n g w a s t e p r o d u c t s such as a c e t a t e , b u t y r a t e , a n d e t h a n o l [12, 22]. I n light o f t h e r e s u l t s p r e s e n t e d here, o n e o r m o r e o f t h e s e m e c h a n i s m s is p r o b a b l y m o r e i m p o r t a n t t h a n d i r e c t c o n s u m p t i o n o f d i s s o l v e d organic matter by ciliated protozoa.


D. Glaser

Acknowledgments. Ralph Mitchell and Richard Lewontin provided laboratory space and help of various kinds throughout this project. Jim Maki and Norman Grossblatt read and commented on the manuscript. The efforts of all are appreciated.

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Consumption of Bacteria and DOM by Tetrahymena


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Simultaneous consumption of bacteria and dissolved organic matter byTetrahymena pyriformis.

The addition of ciliated protozoa to aquatic microcosms and bench-scale sewage treatment plants increases decomposition rates. This is surprising, ina...
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