Response of Anaerobic Protozoa to Oxygen Tension in Anaerobic System

  • Priya MEmail author
  • Shibuvardhan Y
  • Manilal V BEmail author
Original Article


The effect of oxygen on anaerobic protozoa was studied in anaerobic batch reactors inoculated with sludge and protozoa cultures. Among the protozoa genera, Metopus, Brachonella, Plagiopyla, Trepomonas, and Vanella were more sensitive to oxygen compared to other genera. Protozoa genera Menoidium, Rhynchomonas, Cyclidium, Spathidium, and Amoeba were found to survive under aerobic conditions, and the growth rate was slightly higher or similar to anaerobic condition. O2 tension resulted in the loss of free and endosymbiotic methanogens in anaerobic system, while methanogens were observed inside the protozoan cysts. Survival of anaerobic protozoa declined considerably when the O2 tension exceeded 1% atm. sat. and showed chemosensory behavior in response to O2 exposure. Superoxide dismutase activity was detected in survived protozoa cells under O2 tension. Facultative anaerobic protozoa with SOD activity can provide a mechanism to overcome possible occurrence of oxygen toxicity in the treatment of wastewater in anaerobic reactor.


Anaerobic protozoa Oxygen sensitivity Protozoa cyst Methanogens Enzyme activity 


Funding Information

Priya M received financial assistance from the University Grants Commission in the form of research fellowship (Award No. F 15-6 (Dec 2001)/2002(NET))

Supplementary material

10123_2019_58_MOESM1_ESM.docx (352 kb)
ESM 1 (DOCX 351 kb)


  1. Ajit H, Suresh S, Chitra KR, Manilal VB (2005) The Buoyant Filter Bioreactor: a high-rate anaerobic reactor for complex wastewater-process dynamics with dairy effluent. Water Res 39:993–1004CrossRefGoogle Scholar
  2. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925Google Scholar
  3. Amann RI, Springer N, Ludwig W, Görtz HD, Schleifer KH (1991) Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature 351:161–164CrossRefGoogle Scholar
  4. APHA, AWWA, WEF. 1998. Standard methods for examination of wastes and wastewater. Washington DC, USAGoogle Scholar
  5. Bernard B, Fenchel T (1996) Some microaerobic ciliates are facultative anaerobes. Eur J Protistol 32:293–297CrossRefGoogle Scholar
  6. Biagini GA, Suller MTE, Finlay BJ, Llyod D (1997) Oxygen uptake and antioxidant responses of the free living diplomonad Hexamita sp. J Eukaryot Microbiol 44:447–453CrossRefGoogle Scholar
  7. Broers CAM, Berkhout RJM, Hua LY, Stumm CK, Vogels GD (1992) Oxygen responses of the free living amoeboflagellate, Psalteriomonas lanterna. FEMS Microbiol Ecol 101:165–172CrossRefGoogle Scholar
  8. Cadenas E (1989) Biochemistry of oxygen toxicity. Annu Rev Biochem 58:79–110CrossRefGoogle Scholar
  9. Fenchel T (1993) Methanogenesis in marine shallow water sediments: the qualitative role of anaerobic protozoa with endosymbiotic methanogenic bacteria. Ophelia 37:67–82CrossRefGoogle Scholar
  10. Fenchel T, Finlay BJ (1990) Oxygen toxicity, respiration and behavioural responses to oxygen in free-living anaerobic ciliate. J Gen Microbiol 136:1953–1959CrossRefGoogle Scholar
  11. Fenchel T, Finlay BJ (1991) The biology of free living anaerobic ciliates. Eur J Protistol 26:201–215CrossRefGoogle Scholar
  12. Finlay BJ, Fenchel T (1989) Hydrogenosomes in some anaerobic protozoa resemble mitochondria. FEMS Microbiol Lett 65:311–314CrossRefGoogle Scholar
  13. Finlay BJ, Fenchel T (1991) An anaerobic protozoon, with symbiotic methanogens, living in municipal landfill material. FEMS Microbiol Ecol 85:169–180CrossRefGoogle Scholar
  14. Finlay BJ, Fenchel T, Gardener S (1986) Oxygen perception and oxygen toxicity in the freshwater ciliated protozoon Loxodes. J Protozool 33:157–165CrossRefGoogle Scholar
  15. Foissner W, Berger H (1996) A user-friendly guide to the ciliates (protozoa, ciliophora) commonly used by hydrobiologists as bioindicators in river, lakes and wastewater, with notes. Limnologica 27:179–238Google Scholar
  16. Goosen N, Horemans AMC, Hillerbrand SJW, Stumm CK, Vogels GD (1988) Cultivation of the sapropelic ciliate Plagiopyla nasuta stein and isolation of the endosymbiont Methanobacterium formicicum. Arch Microbiol 150:165–170CrossRefGoogle Scholar
  17. Goosen NK, Wagener S, Stumm CK (1990) Comparison of two strains of the anaerobic ciliate Trimyema compressum. Arch Microbiol 153:187–192CrossRefGoogle Scholar
  18. Harada H, Uemura S, Momonoi K (1994) Interaction between sulfate-reducing bacteria and methane-producing bacteria in a UASB reactors fed with low strength waste water containing different level of sulfate. Water Res 28:355–367CrossRefGoogle Scholar
  19. Imai JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309CrossRefGoogle Scholar
  20. McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055Google Scholar
  21. McCord JM, Keele BB, Fridovich I (1971) An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase. Proc Natl Acad Sci U S A 68:1024–1102CrossRefGoogle Scholar
  22. Mueller M (1988) Energy metabolism of protozoa without mitochondria. Annu Rev Microbiol 42:465–488CrossRefGoogle Scholar
  23. Newbold C, Lassalas B, Jouany J (1995) The importance of methanogens associated with ciliate protozoa in ruminal methane production in vitro. Lett Appl Microbiol 21:230–243CrossRefGoogle Scholar
  24. Patterson DJ (1995) Free living freshwater protozoa: A colour guide. John Wiley and Sons, UNSW Press, SydneyGoogle Scholar
  25. Priya M, Ajit H, Manilal VB (2007) Involvement of protozoa in anaerobic wastewater treatment processes. Water Res 41:4639–4645CrossRefGoogle Scholar
  26. Priya M, Ajit H, Manilal VB (2008) Anaerobic protozoa and their growth in biomethanation systems. Biodegradation 19:179–185CrossRefGoogle Scholar
  27. Robert SB, Ronald A, David S, Gill G, Gary S (1998) Techniques in microbial ecology. Oxford University press, New YorkGoogle Scholar
  28. Van Bruggen JJA, Stumm CK, Vogels GD (1983) Symbiosis of methanogenic bacteria and sapropelic protozoa. Arch Microbiol 136:89–95CrossRefGoogle Scholar
  29. Williams AG, Coleman GS (1991) The rumen protozoa. Springer-Verlag Inc., New YorkGoogle Scholar
  30. Yu BP (1994) Cellular defences against damage from reactive oxygen species. Physiol Rev 74:139–162CrossRefGoogle Scholar
  31. Zehnder AJB (1988) Biology of anaerobic microorganisms. John Wiley and Sons, New YorkGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.School of Environmental StudiesCochin University of Science and TechnologyCochinIndia
  2. 2.Department of ZoologyUniversity of CalicutMalappuramIndia
  3. 3.Process Engineering and Environmental Technology DivisionNational Institute for Interdisciplinary Science and Technology, CSIRThiruvananthapuramIndia

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