Skip to main content

Hydrogenosomes of Anaerobic Ciliates

  • Chapter
  • First Online:

Part of the book series: Microbiology Monographs ((MICROMONO,volume 9))

Abstract

Ciliates are highly complex unicellular eukaryotes. Most of them live in aerobic environments and possess mitochondria that use oxygen as final electron acceptor. However, in several orders of ciliates, anaerobic species evolved that contain hydrogenosomes, ATP-producing organelles that use protons as final electron acceptor, producing hydrogen in this process. These hydrogenosomes of ciliates have not been studied in the same detail as those of trichomonads and anaerobic fungi. Therefore, generalizations on the characteristics of hydrogenosomes of ciliates are somewhat premature, especially since phylogenetic studies suggest that hydrogenosomes have evolved independently several times in ciliates. In this chapter, the hydrogenosomes of the anaerobic, heterotrichous ciliate Nyctotherus ovalis from the hindgut of cockroaches will mainly be described as these are the ones that are, at the moment, the most thoroughly studied. This was the first hydrogenosome shown to possess a genome, and this genome is clearly of mitochondrial origin. In fact, the hydrogenosome of N. ovalis unites typical mitochondrial features such as a genome and an electron-transport chain with the characteristic hydrogenosomal property, the production of hydrogen. The hydrogenosomal metabolism of N. ovalis will be compared with that of two other ciliates that have been studied in less detail, i.e. the holotrichous rumen ciliate Dasytricha and the free-living plagiopylid ciliate Trimyema. All studies combined show that the hydrogenosomes of anaerobic ciliates are different from those of anaerobic fungi and from the well-studied ones in trichomonads.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Akhmanova A, Voncken F, van Alen T, van Hoek A, Boxma B, Vogels G, Veenhuis M, Hackstein JHP (1998) A hydrogenosome with a genome. Nature 396:527–528

    Article  CAS  PubMed  Google Scholar 

  • Biagini GA, Hayes AJ, Suller MTE, Winters C, Finlay BJ, Lloyd D (1997) Hydrogenosomes of Metopus contortus physiologically resemble mitochondria. Microbiology 143:1623–1629

    Article  CAS  PubMed  Google Scholar 

  • Boxma B, Voncken F, Jannink S, van Alen T, Akhmanova A, van Weelden SWH, van Hellemond JJ, Ricard G, Huynen M, Tielens AGM, Hackstein JHP (2004) The anaerobic chytridiomycete fungus Piromyces sp. E2 produces ethanol via pyruvate: formate lyase (PFL) and an alcohol dehydrogenase E (ADHE). Mol Microbiol 51:1389–1399

    Article  CAS  PubMed  Google Scholar 

  • Boxma B, deGraaf RM, van der Staay GWM, van Alen TA, Ricard G, Gabaldon T, van Hoek AHAM, Moon-van der Staay SY, Koopman WJH, van Hellemond JJ, Tielens AGM, Friedrich T, Veenhuis M, Huynen MA, Hackstein JHP (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434:74–79

    Article  CAS  PubMed  Google Scholar 

  • Cameron SL, O’Donoghue PJ (2002a) The ultrastructure of Amylovorax dehori tyi comb. Nov. and erection of the Amylovoracidae fam. Nov. (Ciliophora: Trichostomatia). Eur J Protistol 38:29–44

    Article  Google Scholar 

  • Cameron SL, O’Donoghue PJ (2002b) The ultrastructure of Macropodinium moiri and revised diagnosis of the Macropodiniidae (Litostomatea: Trichostomatia). Eur J Protistol 38:79–194

    Google Scholar 

  • Clarke KJ, Finlay BJ, Esteban G, Guhl BE, Embley TM (1993) Cyclidium porcatum N. sp. – a free-living anaerobic scuticociliate containing a stable complex of hydrogenosomes, eubacteria and archaeobacteria. Eur J Protistol 29:262–270

    Article  CAS  PubMed  Google Scholar 

  • Corliss JO (1979) The ciliated protozoa: characterization, classification, and guide to the literature. Pergamon Press, London

    Google Scholar 

  • De Graaf RM, van Alen TA, Dutilh BE, Kuiper JW, van Zoggel HJ, Huynh MB, Görtz HD, Huynen MA, Hackstein JH (2009) The mitochondrial genomes of the ciliates Euplotes minuta and Euplotes crassus. BMC Genomics 10:514

    Article  PubMed  PubMed Central  Google Scholar 

  • De Graaf RM, Ricard G, van Alen TA, Duarte I, Dutilh BE, Burgtorf C, Kuiper JWP, van der Staay GWM, Tielens AGM, Huynen MA, Hackstein JHP (2011) The organellar genome and metabolic potential of the hydrogen-producing mitochondrion of Nyctotherus ovalis. Mol Biol Evol 28:2379–2391

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong XZ, Plugge CM, Stams AJM (1994) Anaerobic degradation of propionate by a mesophilic acetogenic bacterium in coculture and triculture with different methanogens. Appl Environ Microbiol 60:2834–2838

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dyall SD, Brown MT, Johnson PJ (2004) Ancient invasions: from endosymbionts to organelles. Science 304:253–257

    Article  CAS  PubMed  Google Scholar 

  • Ellis JE, Mclntyre PS, Saleh M, Williams AG, Lloyd D (1991a) Influence of CO2 and low concentrations of O2 on fermentative metabolism of the ruminal ciliate Polyplastron multivesiculatum. Appl Environ Microbiol 57:1400–1407

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis JE, Mclntyre PS, Saleh M, Williams AG, Lloyd D (1991b) Influence of CO2 and low concentrations of O2 on fermentative metabolism of the rumen ciliate Dasytricha ruminantium. J Gen Microbiol 137:1409–1417

    Article  CAS  PubMed  Google Scholar 

  • Ellis JE, Mclntyre PS, Saleh M, Williams AG, Lloyd D (1991c) The influence of ruminal concentrations of O2 and CO2 on fermentative metabolism of the rumen entodiniomorphid ciliate Eudiplodinium maggii. Curr Microbiol 23:245–251

    Article  CAS  Google Scholar 

  • Embley TM (2006) Multiple secondary origins of the anaerobic lifestyle in eukaryotes. Philos Trans R Soc B Biol Sci 361:1055–1067

    Article  CAS  Google Scholar 

  • Embley TM, Finlay BJ (1994) The use of small-subunit ribosomal-RNA sequences to unravel the relationships between anaerobic ciliates and their methanogen endosymbionts. Microbiology 140:225–235

    Article  CAS  PubMed  Google Scholar 

  • Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630

    Article  CAS  PubMed  Google Scholar 

  • Embley TM, Finlay BJ, Dyal PL, Hirt RP, Wilkinson M, Williams AG (1995) Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc R Soc Lond Ser B Biol Sci 262:87–93

    Article  CAS  Google Scholar 

  • Embley TM, van der Giezen M, Horner DS, Dyal PL, Bell S, Foster PG (2003) Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55:387–395

    Article  CAS  PubMed  Google Scholar 

  • Fenchel T, Finlay BJ (1995) Ecology and evolution in anoxic worlds. Oxford University Press, New York

    Google Scholar 

  • Finlay BJ, Fenchel T (1989) Hydrogenosomes in some anaerobic protozoa resemble mitochondria. FEMS Microbiol Lett 65:311–314

    Article  CAS  Google Scholar 

  • Gentekaki E, Curtis BA, Stairs CW, Klimeš V, Eliáš M, Salas-Leiva DE, Herman EK, Eme L, Arias MC, Henrissat B, Hilliou F, Klute MJ, Suga H, Malik SB, Pightling AW, Kolisko M, Rachubinski RA, Schlacht A, Soanes DM, Tsaousis AD, Archibald JM, Ball SG, Dacks JB, Clark CG, van der Giezen M, Roger AJ (2017) Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis. PLoS Biol 15(9):e2003769

    Article  PubMed  PubMed Central  Google Scholar 

  • Gijzen HJ, Broers CAM, Barughare M, Stumm CK (1991) Methanogenic bacteria as endosymbionts of the ciliate Nyctotherus ovalis in the cockroach hindgut. Appl Environ Microbiol 57:1630–1634

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goosen NK, Horemans AMC, Hillebrand SJW, Stumm CK, Vogels GD (1988) Cultivation of the sapropelic ciliate Plagiopyla nasuta Stein and isolation of the endosymbiont Methanobacterium formickum. Arch Microbiol 150:165–170

    Article  Google Scholar 

  • Goosen NK, Van der Drift C, Stumm CK, Vogels GD (1990) End products of metabolism in the anaerobic ciliate Trimyema compressutn. FEMS Microbiol Lett 69:171–175

    Article  CAS  Google Scholar 

  • Hackstein JHP, Akhmanova A, Boxma B, Harhangi HR, Voncken FGJ (1999) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol 7:441–447

    Article  CAS  PubMed  Google Scholar 

  • Hackstein JHP, Akhmanova A, Voncken F, van Hoek A, van Alen T, Boxma B, Moon, van der Staay SY, van der Staay G, Leunissen J, Huynen M, Rosenberg J, Veenhuis M (2001) Hydrogenosomes: convergent adaptations of mitochondria to anaerobic environments. Zool Anal Complex Syst 104:290–302

    CAS  Google Scholar 

  • Hackstein JHP, van Hoek AHAM, Leunissen JAM, Huynen M (2002) Anaerobic ciliates and their methanogenic endosymbionts. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer Academic, Dordrecht, pp 451–464

    Google Scholar 

  • Hackstein JHP, Tjaden J, Huynen M (2006) Mitochondria, hydrogenosomes and mitosomes: products of evolutionary tinkering! Curr Genet 50:225–245

    Article  CAS  PubMed  Google Scholar 

  • Hackstein JHP, Baker SE, van Hellemond JJ, Tielens AGM (2019) Hydrogenosomes of anaerobic fungi: an alternative way to adapt to anaerobic environments. In: Tachezy J (ed) Hydrogenosomes and mitosomes: mitochondria of anaerobic eukaryotes. Springer, Heidelberg

    Google Scholar 

  • Hirt RP, Wilkinson AG, Embley TM (1998) Molecular and cellular evolution of ciliates: a phylogenetic perspective. In: Coombs GH, Vickerman K, Sleigh MA, Warren A (eds) Evolutionary relationships among protozoa. Chapman and Hall, London, pp 327–340

    Google Scholar 

  • Hrdý I, Müller M, Tachezy J (2019) Metabolism of trichomonad hydrogenosomes. In: Tachezy J (ed) Hydrogenosomes and mitosomes: mitochondria of anaerobic eukaryotes. Springer, Heidelberg

    Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405

    Article  CAS  PubMed  Google Scholar 

  • Lantsman Y, Tan KS, Morada YN (2008) Biochemical characterization of a mitochondrial-like organelle from Blastocystis sp. subtype 7. Microbiology 154:2757–2766

    Article  CAS  PubMed  Google Scholar 

  • Lloyd D, Hillman K, Yarlett N, Williams AG (1989) Hydrogen-production by rumen holotrich protozoa – effects of oxygen and implications for metabolic control by in situ conditions. J Protozool 36:205–213

    Article  CAS  PubMed  Google Scholar 

  • Martin W (2005) The missing link between hydrogenosomes and mitochondria. Trends Microbiol 13:457–459

    Article  CAS  PubMed  Google Scholar 

  • Müller M (1993) The hydrogenosome. J Gen Microbiol 139:2879–2889

    Article  PubMed  Google Scholar 

  • Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu RY, van der Giezen M, Tielens AGM, Martin WF (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495

    Article  PubMed  PubMed Central  Google Scholar 

  • Paul RG, Williams AG, Butler RD (1990) Hydrogenosomes in the rumen entodiniomorphid ciliate Polyplastron multivesiculatum. J Gen Microbiol 136:1981–1989

    Article  CAS  PubMed  Google Scholar 

  • Perez-Brocal V, Clark CG (2008) Analysis of two genomes from the mitochondrion-like organelle of the intestinal parasite Blastocystis: complete sequences, gene content, and genome organization. Mol Biol Evol 25:2475–2482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Regensbogenova M, McEwan NR, Javorsky P, Kisidayova S, Michalowski T, Newbold CJ, Hackstein JHP, Pristas P (2004) A re-appraisal of the diversity of the methanogens associated with the rumen ciliates. FEMS Microbiol Lett 238:307–313

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Snyers L, Hellings P, Bovy-Kesler C, Thines-Sempoux D (1982) Occurrence of hydrogenosomes in the rumen ciliates Ophryoscolecidae. FEBS Lett 137:35–39

    Article  CAS  Google Scholar 

  • Stechmann A, Hamblin K, Perez-Brocal V, Gaston D, Richmond GS, van der Giezen M, Clark CG, Roger AJ (2008) Organelles in Blastocystis that blur the distinction between mitochondria and hydrogenosomes. Curr Biol 18(8):580–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Struder-Kypke MC, Wright ADG, Foissner W, Chatzinotas A, Lynn DH (2006) Molecular phylogeny of litostome ciliates (Ciliophora, Litostomatea) with emphasis on free-living Haptorian genera. Protist 157:261–278

    Article  CAS  PubMed  Google Scholar 

  • Tielens AGM, Rotte C, van Hellemond JJ, Martin W (2002) Mitochondria as we don’t know them. Trends Biochem Sci 27:564–572

    Article  CAS  PubMed  Google Scholar 

  • Tielens AGM, van Grinsven K, Henze K, van Hellemond JJ, Martin W (2010) Acetate formation in the energy metabolism of parasitic helminths and protists. Int J Parasitol 40:387–397

    Article  CAS  PubMed  Google Scholar 

  • Tokura M, Chagan I, Ushida K, Kojima Y (1999) Phylogenetic study of methanogens associated with rumen ciliates. Curr Microbiol 39:123–128

    Article  CAS  PubMed  Google Scholar 

  • van Bruggen JJA, Stumm CK, Vogels GD (1983) Symbiosis of methanogenic bacteria and sapropelic protozoa. Arch Microbiol 136:89–95

    Article  Google Scholar 

  • van Bruggen JJA, Zwart KB, van Assema RM, Stumm CK, Vogels GD (1984) Methanobacterium formicicum, an endosymbiont of the anaerobic ciliate Metopus striatus McMurrich. Arch Microbiol 139:1–7

    Article  Google Scholar 

  • van Bruggen JJA, Zwart KB, Hermans JGF, van Hove EM, Stumm CK, Vogels GD (1986) Isolation and characterization of Methanoplanus endosymbiosus sp. nov, an endosymbiont of the marine sapropelic ciliate Metopus contortus Quennerstedt. Arch Microbiol 144:367–374

    Article  Google Scholar 

  • van Bruggen JJA, van Rens GLM, Geertman EJM, Zwart KB, Stumm CK, Vogels GD (1988) Isolation of a methanogenic endosymbiont of the sapropelic ameba Pelomyxa palustris Greeff. J Protozool 35:20–23

    Article  Google Scholar 

  • van Hoek AHAM, van Alen TA, Sprakel VSI, Hackstein JHP, Vogels GD (1998) Evolution of anaerobic ciliates from the gastrointestinal tract: phylogenetic analysis of the ribosomal repeat from Nyctotherus ovalis and its relatives. Mol Biol Evol 15:1195–1206

    Article  PubMed  Google Scholar 

  • van Hoek AHAM, Sprakel VSI, Van Alen TA, Theuvenet APR, Vogels GD, Hackstein JHP (1999) Voltage-dependent reversal of anodic galvanotaxis in Nyctotherus ovalis. J Eukaryot Microbiol 46:427–433

    Article  PubMed  Google Scholar 

  • van Hoek AHAM, Akhmanova AS, Huynen MA, Hackstein JHP (2000a) A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Mol Biol Evol 17:202–206

    Article  PubMed  Google Scholar 

  • van Hoek AHAM, van Alen TA, Sprakel VSI, Leunissen JAM, Brigge T, Vogels GD, Hackstein JHP (2000b) Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol Biol Evol 17:251–258

    Article  PubMed  Google Scholar 

  • Vogels GD, Hoppe WF, Stumm CK (1980) Association of methanogenic bacteria with rumen ciliates. Appl Environ Microbiol 40:608–612

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wawrzyniak I, Roussel M, Diogon M, Couloux A, Texier C, Tan KSW, Vivares CP, Delbac F, Wincker P, El Alaoui H (2008) Complete circular DNA in the mitochondria-like organelles of Blastocystis hominis. Int J Parasitol 38:1377–1382

    Article  CAS  PubMed  Google Scholar 

  • Williams AG, Coleman GS (1992) The rumen protozoa. Springer, New York

    Book  Google Scholar 

  • Yarlett N, Hann AC, Lloyd D, Williams A (1981) Hydrogenosomes in the rumen protozoan Dasytricha ruminantium Schuberg. Biochem J 200:365–372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yarlett N, Lloyd D, Williams AG (1982) Respiration of the rumen ciliate Dasytricha ruminantium Schuberg. Biochem 206:259–266

    Article  CAS  Google Scholar 

  • Yarlett N, Hann AC, Lloyd D, Williams AG (1983) Hydrogenosomes in a mixed isolate of Isotricha prostoma and Isotricha intestinalis from ovine rumen contents. Comp Biochem Physiol B Biochem Mol Biol 74:357–364

    Article  CAS  Google Scholar 

  • Yarlett N, Coleman GS, Williams AG, Lloyd D (1984) Hydrogenosomes in known species of rumen entodiniomorphid protozoa. FEMS Microbiol Lett 21:15–19

    Article  CAS  Google Scholar 

  • Yarlett N, Lloyd D, Williams AG (1985) Butyrate formation from glucose by the rumen protozoan Dasytricha ruminantium. Biochem J 228:187–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zwart KB, Goosen NK, van Schijndel MW, Broers CAM, Stumm CK, Vogels GD (1988) Cytochemical-localization of hydrogenase activity in the anaerobic protozoa Trichomonas vaginalis, Plagiopyla nasuta and Trimyema compressum. J Gen Microbiol 134:2165–2170

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aloysius G. M. Tielens .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Hackstein, J.H.P., de Graaf, R.M., van Hellemond, J.J., Tielens, A.G.M. (2019). Hydrogenosomes of Anaerobic Ciliates. In: Tachezy, J. (eds) Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes. Microbiology Monographs, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-030-17941-0_5

Download citation

Publish with us

Policies and ethics