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Respiration rates in heterotrophic, free-living protozoa

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Abstract

Published estimates of protozoan respiratory rates are reviewed with the object of clarifying their value in ecological studies. The data show a surprisingly large variance when similarly sized cells or individual species are compared. This is attributed to the range of physiological states in the cells concerned. The concept of basal metabolism has little meaning in protozoa. During balanced growth, energy metabolism is nearly linearly proportional to the growth rate constant; at the initiation of starvation, metabolic rate rapidly declines. Motility requires an insignificant fraction of the energy budget of protozoans. For growing cells, metabolic rate is approximately proportional to weight0.75 and the data fall nearly exactly on a curve extrapolated from that describing the respiration rates of poikilotherm metazoans as a function of body weight. It is conceivable that protozoan species exist with lower maximum potential growth and metabolic rates than those predicted from cell volume and the equations derived from the available data. However, the lack of information concerning the state of the cells studied prevents verification of this idea. Laboratory measurements of protozoan respiratory rates have no predictive value for protozoa in nature other than delimiting a potential range. For small protozoans, this range may, on an individual basis, represent a factor of 50.

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References

  1. Baker EGS, Baumberger JP (1941) The respiratory rate and the cytochrome content of a ciliate protozoan (Tetrahymena gelei). J Cell Comp Physiol 17:285–303

    Google Scholar 

  2. Baldock BM, Baker JH, Sleigh MA (1980) Laboratory growth rates of six species of freshwater gymnamoebia. Oecologia (Berl) 47:156–159

    Google Scholar 

  3. Baldock BM, Rogerson A, Berger J (1982) Further studies on respiratory rates of freshwater amoebae (Rhizopoda, Gymnamoebia). Microb Ecol 8:55–60

    Google Scholar 

  4. Band RN, Mohrlok S (1969) The respiratory metabolism ofAcanthamoeba rhysodes during encystation. J Gen Microbiol 59:351–358

    Google Scholar 

  5. Beauchop T, Elsden SR (1960) The growth of micro-organisms in relation to their energy supply. J Gen Microbiol 23:457–469

    Google Scholar 

  6. Boell EJ, Woodruff LL (1941) Respiratory metabolism of mating types inParamecium calkinsi. J Exp Zool 87:385–402

    Google Scholar 

  7. Brachet J (1955) Recherches sur les interactions biochimiques entre le noyau et le cytoplasme chez les organismes unicellulaires. I.Amoeba proteus. Biochim Biophys Acta 18:247–268

    PubMed  Google Scholar 

  8. Buetow DE (1961) Variation of the respiration of protozoan cells with length of centrifuging. Anal Biochem 2:242–247

    Google Scholar 

  9. Byers TJ, Rudick VL, Rudick MJ (1969) Cell size, macromolecule composition, nuclear number, oxygen consumption and cyst formation during two growth phases in unagitated cultures ofAcanthamoebae castellanii. J Protozool 16: 693–699

    PubMed  Google Scholar 

  10. Calow P (1977) Conversion efficiencies in heterotrophic organisms. Biol Rev 52: 385–409

    Google Scholar 

  11. Cameron IL, Jeter JR (1970) Synchronization of the cell cycle ofTetrahymena by starvation and refeeding. J Protozool 17:429–433

    PubMed  Google Scholar 

  12. Chen M-L (1970) Effect of energy source on growth and respiration ofTetrahymena pyriformis. Bull Inst Zool, Academia Sinica 9: 1–5

    Google Scholar 

  13. Claff CL, Tahmisian TN (1949) Cartesian diver technique. J Biol Chem 179: 577–583

    Google Scholar 

  14. Conner RL, Cline SG (1967) Some factors governing respiration, glucose metabolism and iodoacetate sensitivity inTetrahymena pyriformis. J Protozool 14:22–26

    Google Scholar 

  15. Crowell MF (1928) Protozoa in an apple tree. Proc Pa Acad Sci 2: 102

    Google Scholar 

  16. Cunningham B, Kirk PL (1942) The oxygen consumption of single cells inParamecium caudatum as measured by a capillary respirometer. J Cell Comp Physiol 20: 119–134

    Google Scholar 

  17. Curds CR, Cockburn A (1968) Studies on the growth and feeding ofTetrahymena pyriformis in axenic and monoxenic culture. J Gen Microbiol 54: 343–358

    PubMed  Google Scholar 

  18. von Dach H (1942) Respiration of a colorless flagellateAstasia klebsii. Biol Bull Mar Biol Lab, Woods Hole 82: 356–371

    Google Scholar 

  19. Danforth WF, Wilson BW (1961) The endogenous metabolism ofEuglena gracilis. J Gen Microbiol 24: 95–105

    PubMed  Google Scholar 

  20. Emerson R (1930) Measurements of the metabolism of two protozoans. J Gen Physiol 13: 153–158

    Google Scholar 

  21. Fenchel T (1968) The ecology of marine microbenthos III. The reproductive potential of ciliates. Ophelia 5: 123–136

    Google Scholar 

  22. Fenchel T (1974) Intrinsic rate of natural increase: the relationship with body size. Oecologia (Berl) 14: 317–326

    Google Scholar 

  23. Fenchel T (1980) Suspension feeding in ciliated protozoa: functional response and particle size selection. Microb Ecol 6: 1–11

    Google Scholar 

  24. Fenchel T (1982) Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar Ecol Prog Ser 8: 225–231

    Google Scholar 

  25. Fenchel T (1982) Ecology of heterotrophic microflagellates. III. Adaptations to heterogenous environments. Mar Ecol Prog Ser 9: 25–33

    Google Scholar 

  26. Finlay BJ (1977) The dependence of reproductive rate on cell size and temperature in freshwater ciliated protozoa. Oecologia (Berl) 30: 75–81

    Google Scholar 

  27. Finlay BJ, Uhlig G (1981) Calorific and carbon values of marine and freshwater protozoa. Helgoländer Meeresunters 34: 401–412

    Google Scholar 

  28. Finlay BJ, Span A, Ochsenbein-Gattlen C (1983) Influence of physiological state on indices of respiration rate in protozoa. Comp Biochem Physiol 74A:211–219

    Google Scholar 

  29. Hall RL (1938) The oxygen consumption ofColpidium campylum. Biol Bull Mar Biol Lab, Woods Hole 75:395–408

    Google Scholar 

  30. Hamburger K (1975) Respiratory rate through the growth-division cycle ofAcanthamobae sp. C R Trav Lab Carlsberg 40:175–185

    Google Scholar 

  31. Hamburger K, Zeuthen E (1957) Synchronous divisions inTetrahymena pyriformis as studied in an inorganic medium. Exp Cell Res 13:443–453

    PubMed  Google Scholar 

  32. Hamburger K, Zeuthen E (1971) Respiratory responses to dissolved food of starved, normal and division-synchronizedTetrahymena cells. C R Trav Lab Carlsberg 38:145–161

    PubMed  Google Scholar 

  33. Hemmingsen AM (1950) The relation of standard (basal) energy metabolism to total fresh weight of living organisms. Rep Steno Mem Hosp, Copenhagen 4: 1–58

    Google Scholar 

  34. Hemmingsen AM (1960) Energy metabolism as related to body size and respiratory surfaces and its evolution. Rep Steno Mem Hosp, Copenhagen 9:1–110

    Google Scholar 

  35. Hiramoto Y (1974) Mechanics of ciliary movement. In: Sleigh MA (ed) Cilia and flagella, Academic Press, London and New York, pp 177–196

    Google Scholar 

  36. Holter H, Zeuthen E (1949) Metabolism and reduced weight in starvingChaos chaos. C R Trav Lab Carlsberg 26:277–296

    Google Scholar 

  37. Holz GG (1954) The oxidative metabolism of a cryptomonad flagellateChilomonas paramecium. J Protozool 1: 114–120

    Google Scholar 

  38. Howland RB, Bernstein A (1931) A method for determining the oxygen consumption of a single cell. J Gen Physiol 43:339–348

    Google Scholar 

  39. Hunter FR, Lee JW (1962) On the metabolism ofAstasia longa (Jahn). J Protozool 9:74–78

    Google Scholar 

  40. Hutchens JO (1941) The effect of the age of the culture on the rate of oxygen consumption and the respiratory quotient ofChilomonas paramecium. J Cell Comp Physiol 17:321–332

    Google Scholar 

  41. Hutchens JO, Podolsky B, Morales MF (1948) Studies on the kinetics and energetics of carbon and nitrogen metabolism ofChilomonas paramecium. J Cell Comp Physiol 32:117–141

    Google Scholar 

  42. Ikeda T (1979) Respiration rates of copepod larvae and a ciliate of a tropical sea. J Oceanogr Soc Japan 35:1–8

    Google Scholar 

  43. James TW, Read CP (1957) The effect of incubation temperature on the cell size ofTetrahymena pyriformis. Exp Cell Res 13:510–516

    PubMed  Google Scholar 

  44. Johnson BF (1962) Influence of temperature on the respiration and metabolic effectiveness ofChilomonas. Exp Cell Res 28:419–423

    Google Scholar 

  45. Kalisz B (1973) Stimulation of respiration inAmoebae proteus by inducers of pinocytosis. Folia Biol 21:169–172

    Google Scholar 

  46. Khlebovich TV (1974) Rate of respiration in ciliates of different sizes. Tsitologiya 16:103–110

    Google Scholar 

  47. Klekowski RZ (1981) Ecology of aquatic organisms. 3. Animals. Size dependance of metabolism on protozoans. Verh Int Verein Theor Angew Limnol 21:1498–1502

    Google Scholar 

  48. Korohoda W, Kalisz B (1970) Correlation of respiratory and motile activities inAmoebae proteus. Folia Biol, Krakow 18:137–143

    Google Scholar 

  49. Laybourn J (1975) Respiratory energy losses inStentor coeruleus Ehrenberg (Ciliophora). Oecologia (Berl) 21: 273–278

    Google Scholar 

  50. Laybourn J (1976) Respiratory losses inPodophrya fixa Müller in relation to temperature and nutritional status. J Gen Microbiol 96:203–208

    Google Scholar 

  51. Laybourn J (1977) Respiratory energy losses in the protozoan predatorDidinium nasutum Müller (Ciliophora). Oecologia (Berl) 27:305–309

    Google Scholar 

  52. Laybourn J, Finlay BJ (1976) Respiratory energy losses related to cell weight and temperature in ciliated protozoa. Oecologia (Berl) 24:349–355

    Google Scholar 

  53. Laybourn-Parry J, Baldock B, Kingmill-Robinson C (1980) Respiratory studies on two small freshwater amoebae. Microb Ecol 6:209–216

    Google Scholar 

  54. Lee CC, Fenchel T (1972) Studies on ciliates associated with sea ice from Antarctica. II. Temperature responses and tolerances in ciliates from Antarctic, temperate and tropical habitats. Arch Protistenk 114:237–244

    Google Scholar 

  55. Lee JL, Muller WA (1973) Trophic dynamics and niches of salt marsh Foraminifera. Am Zool 13:215–223

    Google Scholar 

  56. Lloyd D, Phillips CA, Statham M (1978) Oscillations of respiration, adenine nucleotid levels and heat evolution in synchronous cultures ofTetrahymena pyriformis ST prepared by continuous-flow selection. J Gen Microbiol 106:19–26

    Google Scholar 

  57. Løvlie A (1963) Growth in mass and respiration rate during the cell cycle ofTetrahymena pyriformis. C R Trav Lab Carlsberg 33:377–413

    PubMed  Google Scholar 

  58. Lwoff A (1934) Sur la respiration du cilieGlaucoma piriformis. C R Soc Biol 115:237–241

    Google Scholar 

  59. McCashland BW, Kronschnabel JM (1962) Exogenous factors affecting respiration inTetrahymena pyriformis. J Protozool 9:276–279

    Google Scholar 

  60. Mast SO, Pace DM, Mast LM (1936) The effect of sulfur on the rate of respiration and on the respiratory quotient inChilomonas paramecium. J Cell Comp Physiol 8:125–140

    Google Scholar 

  61. Neff RJ, Neff RH, Taylor RE (1958) The nutrition and metabolism of a soil Amoebae,Acanthamoebae sp. Physiol Zool 31:73–91

    Google Scholar 

  62. Ormsbee RA (1942) The normal growth and respiration ofTetrahymena geleii. Biol Bull Mar Biol Lab, Woods Hole 82:423–437

    Google Scholar 

  63. Pace DM, Belda WH (1944) The effect of food content and temperature on respiration inPelomyxa carolinensis Wilson. Biol Bull Mar Biol Lab, Woods Hole 86:146–153

    Google Scholar 

  64. Pace DM, Kimura KK (1944) The effect of temperature on respiration inParamecium aurelia andParamecium caudatum. J Cell Comp Physiol 24:173–183

    Google Scholar 

  65. Pace DM, Kimura TE (1946) Relation between metabolic activity and cyanide inhibition inPelomyxa carolinensis Wilson. Exp Biol Med 62:223–227

    Google Scholar 

  66. Pace DM, Lyman LD (1947) Oxygen consumption and carbon dioxide elimination inTetrahymena geleii Furgason. Biol Bull Mar Biol Lab, Woods Hole 92:210–216

    Google Scholar 

  67. Pace DM, Frost BL (1952) The effects of ethyl alcohol on growth and respiration inPelomyxa carolinensis. Biol Bull Mar Biol Lab, Woods Hole 103:97–103

    Google Scholar 

  68. Pace DM, McCashland BW (1951) Effects of low concentration of cyanide on growth and respiration inPelomyxa carolinensis-Wilson (18424). Proc Soc Exp Biol Med 76:165–168

    PubMed  Google Scholar 

  69. Padilla GM, James TW (1960) Synchronization of cell division inAstasia longa on a chemically defined medium. Exp Cell Res 20:401–415

    PubMed  Google Scholar 

  70. Paine WJ (1970) Energy yields and growth of heterotrophs. Ann Rev Microbiol 24:17–52

    Google Scholar 

  71. Parker JG (1976) Cultural characteristics of the marine ciliated protozoa,Uronema marinum Dujardin. J Exp Mar Biol Ecol 24:213–226

    Google Scholar 

  72. Pigon A (1954) Respiration and cytochrome oxidase content in certain Infusoria. Bull Acad Pol Sci Cl II Sér (Biol) 11:131–134

    Google Scholar 

  73. Pigon A (1959) Respiration ofColpoda cucullus during active life and encystment. J Protozool 6:303–308

    Google Scholar 

  74. Pitts RF (1932) Effect of cyanide on respiration of the protozoanColpidium campylum. Proc Soc Exp Biol Med 29:542–544

    Google Scholar 

  75. Proper G, Garver JC (1966) Mass culture of the ProtozoaColpoda steinii. Biotechnol Bioeng 8:287–296

    Google Scholar 

  76. Purcell EM (1977) Life at low Reynolds number. Am J Physiol 45:3–11

    Google Scholar 

  77. Reich K (1948) Studies on the respiration of an Amoeba,Mayorella palestinensis. Physiol Zool 21:390–412

    Google Scholar 

  78. Rogerson A (1981) The ecological energetics ofAmoeba proteus (Protozoa). Hydrobiologia 85:117–128

    Google Scholar 

  79. Rubin HA, Lee JJ (1976) Informational energy flow as an aspect of ecological efficiency of marine ciliates. J Theor Biol 62:69–91

    PubMed  Google Scholar 

  80. Ryley JF (1952) Studies on the metabolism of Protozoa. 3. Metabolism of the ciliateTetrahymena pyriformis (Glaucoma piriformis). Biochem J 52:483–492

    PubMed  Google Scholar 

  81. Scholander PF, Claff CL, Sveinsson SL (1952) Respiratory studies of single cells. I. Methods. Biol Bull Mar Biol Lab, Woods Hole 102:157–198

    Google Scholar 

  82. Schwab D, Hofer HW (1979) Metabolism in the ProtozoanAllogromia lacticollaris Arnold. Z Mikrosk-Anat Forsch 93:715–727

    PubMed  Google Scholar 

  83. Simonesen DH, van Wagtendonk WJ (1952) Respiratory studies onParamecium aurelia variety 4, killers and sensitives. Biochim Biophys Acta 9:515–527

    PubMed  Google Scholar 

  84. Sleigh MA, Blake JR (1977) Methods of ciliary propulsion and their limitations. In: Pedley TJ (ed) Scale effects in animal locomotion. Academic Press, London, pp 243–256

    Google Scholar 

  85. Specht H (1935) Aerobic respiration inSpirostomum ambiguum and the production of ammonia. J Cell Comp Physiol 5: 319–333

    Google Scholar 

  86. Stewart JM (1964) The measurements of oxygen consumption in paramecia of different ages. J Protozool 11 Suppl Abs 119:39–40

    Google Scholar 

  87. Stouthamer AH (1977) Energetic aspects of the growth of micro-organisms. In: Haddock BA, Hamilton WA (eds) Microbial energetics. Cambridge University Press, Cambridge, pp 285–315

    Google Scholar 

  88. Taylor WD (1978) Growth responses of ciliate protozoa to the abundance of their bacterial prey. Microb Ecol 4:207–214

    Google Scholar 

  89. Taylor WD, Berger J (1976) Growth ofColpidium campylum in monoxenic batch culture. Can J Zool 54:392–398

    Google Scholar 

  90. Taylor WD, Berger J (1976) Growth responses of cohabiting ciliate protozoa to various prey bacteria. Can J Zool 54:1111–1114

    Google Scholar 

  91. Trinci APJ, Thurston CF (1976) Transition to the non-growing state in eukaryotic microorganisms. In: Gray TRG, Postgate JR (eds) The survival of vegetative microbes. Cambridge University Press, Cambridge, pp 55–79

    Google Scholar 

  92. Veldkamp H, Jannasch HW (1972) Mixed culture studies with the chemostat. J Appl Chem Biotechnol 22:105–123

    Google Scholar 

  93. Vernberg WB, Coull BC (1974) Respiration of an interstitial ciliate and benthic energy relationships. Oecologia (Berl) 16:259–264

    Google Scholar 

  94. van de Vijver G (1966) Studies on the metabolism ofTetrahymena pyriformis GL. I. Influence of substrates on the respiratory rate. Enzymologia 31:363–381

    PubMed  Google Scholar 

  95. Vinberg GG (ed) (1971) Symbols, units and conversion factors in studies of fresh water productivity. London, International Biological Programme p 23

    Google Scholar 

  96. Whitely A (1960) Interactions of nucleus and cytoplasm in controlling respiratory patterns in regeneratingStentor coeruleus. C R Trav Lab Carlsberg 32:49–62

    PubMed  Google Scholar 

  97. Wilson BW (1963) The oxidative assimilation of acetate byAstasia longa and the regulation of cell respiration. J Cell Comp Physiol 62:49–56

    Google Scholar 

  98. Wilson BW, James TW (1963) The respiration and growth of synchronized populations of the cellAstasia longa. Exp Cell Res 32:305–319

    PubMed  Google Scholar 

  99. Wu TY (1977) Introduction to the scaling of aquatic animal locomotion. In: Pedley TJ (ed) Scale effects in animal locomotion. Academic Press, London, New York, pp 203–232

    Google Scholar 

  100. Zeuthen E (1943) A cartesian diver micro-respirometer with a gas volume of 0.1 μl. Respiration measurements with an experimental error of 2.10−5 μl. C R Trav Lab Carlsberg 24:479–518

    Google Scholar 

  101. Zeuthen E (1953) Oxygen uptake as related to body size in organisms. Quart Rev Biol 28:1–12

    PubMed  Google Scholar 

  102. Zeuthen E, Hamburger K (1977) Microgasometry with single cells using ampulla divers operated in density gradients. In: Glick D, Rosenbaum RR (eds) Techniques of biochemical and biophysical morphology Vol 3, John Wiley pp 59–79

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Fenchel, T., Finlay, B.J. Respiration rates in heterotrophic, free-living protozoa. Microb Ecol 9, 99–122 (1983). https://doi.org/10.1007/BF02015125

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