The Relationship between Energy-dependent Phagocytosis and the Rate of Oxygen Consumption in Tetrahymena

Abstract

The induction of high rates of food vacuole formation in Tetrahymena pyr$ormis increased the rate of respiration in exponentially growing cells by 17% and in starving cells by yo. The increased rate of oxygen uptake was caused by phagocytosis itself, as shown by comparing the rates of respiration of a Tetrahymena mutant exposed to particles at the permissive or restrictive temperatures for food vacuole formation. During cell division, heat-synchronized cells in rich, particle-supplemented medium showed a significant decrease in the rate of respiration. Furthermore, dimethyl sulphoxide, in concentrations sufficient to block food vacuole formation, suppressed the rate of respiration to a level similar to that of starved cells. Cytochalasin B, however, did not reduce the rate of oxygen uptake despite the inability of the cells to complete the formation of food vacuoles during treatment; a possible explanation for this finding is discussed. There was a strong correlation between formation of food vacuoles and a high metabolic rate in Tetrahymena. I N T R O D U C T I O NIn nature, the ciliate Tetrahymena pyriformis is a suspension feeder; particulate material is carried by means of the oral cilia to the cytostome where food vacuoles are formed. The ease of cultivation and rapid growth rate of this organism make it especially suitable for the experimental study of phagocytosis.Since formation of food vacuoles in Tetrahymena is dependent on environmental conditions (Nilsson, 1972(Nilsson, , 1976, variations in these conditions offer possibilities for exploring the relationship between cellular metabolism and food vacuole formation. The ingestion of particles depends on oxidative phosphorylation (Chapman-Andresen & Nilsson, 1968) ; hence it is relevant to investigate how much energy Tetrahymena expends on phagocytosis.The present investigation provides an estimate of the amount of energy spent in the process of forming food vacuoles in exponentially growing and starving cells. (Borden et al., 1973) and Tetrnhymena thermophila NP1 were grown axenically in a 2% (w/v) proteose peptone (PP) medium enriched with 0.1 % (w/v) liver extract and salts (Plesner et al., 1964). Cells fixed in 2 % (v/v) glutaraldehyde were counted using either a calibrated counting chamber or a Coulter counter, model ZB; no significant difference in cell number was found between the two methods. Normally, 100 ml cultures were grown in 450 ml Fernbach flasks at 28 "C and aerated with filtered air at approximately 0-5 1 min-I. Under these conditions earlystationary phase was reached at a density of about 2 x lo5 cells ml-l. In most experiments a density of 0-5 x lo5 to 1-5 x lo5 cells ml-l was used. For studies involving starved cells, an exponential phase culture was METHODS Organisms and growth conditions. Tetrahymena pyriformis GLS

The SHAM-sensitive Alternative Oxidase in Tetrahymena pyriformis: Activity as a Function of Growth State and Chloramphenicol Treatment

“…The results with respect to general levels of respiration and inhibitor sensitivity for exponentially growing and stationary phase cells are in good agreement with previously published data (Ruben & Hooper, 1978;Lloyd et al, 1980;Skriver & Nilsson, 1978).…”

Pulsed-resource dynamics increase the asymmetry of antagonistic coevolution between a predatory protist and a prey bacterium

“…This feeding strategy could be, however, maladaptive in a nonliving culture medium, where pinocytosis might ensure the most efficient protozoan growth. Thus, increased allocation to energy‐demanding phagocytosis, in terms of increased metabolic rate (Burmeister, 1971; Skriver & Nilsson, 1978), could have led to wasteful energy usage and, thus, reduced the predator biomass yield in a nonliving predator culture medium. Even though this kind of growth cost is unlikely to constrain predator coevolution in prey resource media, it demonstrates that adaptation to one resource environment can reduce protist fitness in other environment (Ketola et al.…”

On cell organelles in Tetrahymena. With special reference to mitochondria and peroxisomes

“…After 1 h in this concentration, the mitochondria and peroxisomes have changed into their dense type (Figure l la), typical of starved and stationary phase cells; furthermore, lipid droplets, glycogen particles, autophagic vacuoles, and various nucleolar changes are found (94,95). Apart from the variable nucleolar changes, these effects resemble those observed during starvation; however, additional changes such as helical patterns of polyribosomes (95) and the appearance of fibrous bundles in the nucleus (99) may be ascribed to a specific action of DMSO, whereas the former effects reflect a decrease in the rates of cell proliferation (94), oxygen consumption (128), and synthesis of RNA (94) and protein (99). The cells recover from the 1-h treatment; however, although the rate of RNA synthesis has returned to the control level 1 h after removal of DMSO (94), only mitochondria have reversed into the light type after 3 h (Figure 1 I b), the peroxisomes remain dense.…”