Abstract
Decades of investigations have clearly shown that protists living in low-oxygen environments possess mitochondria despite their textbook function, oxidative phosphorylation, is usually absent. The presence of these, in some cases, very rudimental mitochondria has been ascribed to their irreplaceable role in the synthesis of FeS clusters, prosthetic groups of several essential proteins. The deep investigation of the oxymonad Monocercomonoides exilis (Preaxostyla, Metamonada) revealed that this organism very likely represents a notable exception, in which the synthesis of FeS clusters runs in the cytosol and mitochondrion is absent. Investigation of a broader spectrum of oxymonads and their relatives provided evidence that the profound reorganisation of FeS cluster synthesis was initiated by a HGT of the bacterial pathway SUF and a loss of the mitochondrial pathway ISC already before the last common ancestor of this clade. This innovation was very likely a preadaptation for (and not a consequence of) the mitochondrial loss, which happened much later and only in the oxymonad lineage. M. exilis and other oxymonads are being further studied because they represent valuable examples relevant to our understanding of the reductive evolution of organelles and to the origin of the eukaryotic cell.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adl SM, Bass D, Lane CE et al (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 66:4–119
Braymer JJ, Lill R (2017) Iron–sulfur cluster biogenesis and trafficking in mitochondria. J Biol Chem 292:12754–12763. https://doi.org/10.1074/jbc.R117.787101
Brugerolle G, Koenig H, Konig H (1997) Ultrastructure and organization of the cytoskeleton in Oxymonas, an intestinal flagellate of termites. J Eukaryot Microbiol 44:305–313
Carpenter KJ, Waller RF, Keeling PJ (2008) Surface morphology of Saccinobaculus (Oxymonadida): implications for character evolution and function in oxymonads. Protist 159:209–221. https://doi.org/10.1016/j.protis.2007.09.002
Cavalier-Smith T (2014) The neomuran revolution and phagotrophic origin of eukaryotes and cilia in the light of intracellular coevolution and a revised tree of life. Cold Spring Harb Perspect Biol 6:a016006. https://doi.org/10.1101/cshperspect.a016006
Cleveland LR (1950) Hormone-induced sexual cycles of flagellates. IV. Meiosis after syngamy and before nuclear fusion in Notila. J Morphol 87(2):317–347
Embley TM, Van Der Giezen M, Horner DS et al (2003) Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55:387–395. https://doi.org/10.1080/15216540310001592834
Hackstein JHP, Tjaden J, Huynen M (2006) Mitochondria, hydrogenosomes and mitosomes: products of evolutionary tinkering! Curr Genet 50:225–245. https://doi.org/10.1007/s00294-006-0088-8
Hadariová L, Vesteg M, Hampl V, Krajčovič J (2017) Reductive evolution of chloroplasts in non-photosynthetic plants, algae and protists. Curr Genet 64:365. https://doi.org/10.1007/s00294-017-0761-0
Hampl V (2016) Preaxostyla. In: Handbook of the protists. Springer, Cham, pp 1–36
Hampl V, Silberman JD, Stechmann A et al (2008) Genetic evidence for a mitochondriate ancestry in the ‘amitochondriate’ flagellate Trimastix pyriformis. PLoS One 3(9):e1383. https://doi.org/10.1371/journal.pone.0001383
Hampl V, Hug L, Leigh JW et al (2009) Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups”. Proc Natl Acad Sci U S A 106:3859–3864. https://doi.org/10.1073/pnas.0807880106
Hampl V, Čepička I, Eliáš M (2018) Was the mitochondrion necessary to start eukaryogenesis? Trends Microbiol 27:1–9. https://doi.org/10.1016/j.tim.2018.10.005
Heiss A, Keeling PJ (2006) The phylogenetic position of the oxymonad Saccinobaculus based on SSU rRNA. Protist 157:335–344. https://doi.org/10.1016/j.protis.2006.05.007
Karnkowska A, Hampl V (2016) The curious case of vanishing mitochondria. Microb Cell 3:491–494. https://doi.org/10.15698/mic2016.10.531
Karnkowska A, Vacek V, Zubáčová Z et al (2016) A eukaryote without a mitochondrial organelle. Curr Biol 26:1274–1284. https://doi.org/10.1016/j.cub.2016.03.053
Keeling PJ, Leander BS (2003) Characterisation of a non-canonical genetic code in the oxymonad Streblomastix strix. J Mol Biol 326:1337–1349
Kispal G, Csere P, Prohl C, Lill R (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J 18:3981–3989. https://doi.org/10.1093/emboj/18.14.3981
Lane N (2011) Energetics and genetics across the prokaryote-eukaryote divide. Biol Direct 6:35. https://doi.org/10.1186/1745-6150-6-35
Lane N, Martin W (2010) The energetics of genome complexity. Nature 467:929–934. https://doi.org/10.1038/nature09486
Leander BS, Keeling PJ (2004) Symbiotic innovation in the oxymonad Streblomastix strix. J Eukaryot Microbiol 51:291–300. https://doi.org/10.1111/j.1550-7408.2004.tb00569.x
Leger MM, Eme L, Hug LA, Roger AJ (2016) Novel hydrogenosomes in the microaerophilic jakobid Stygiella incarcerata. Mol Biol Evol 33:2318–2336. https://doi.org/10.1093/molbev/msw103
Leger MM, Kolisko M, Kamikawa R et al (2017) Organelles that illuminate the origins of Trichomonas hydrogenosomes and Giardia mitosomes. Nat Ecol Evol 1:0092. https://doi.org/10.1038/s41559-017-0092
Liapounova NA, Hampl V, Gordon PMK et al (2006) Reconstructing the mosaic glycolytic pathway of the anaerobic eukaryote Monocercomonoides. Eukaryot Cell 5:2138–2146. https://doi.org/10.1128/EC.00258-06
Lill R, Dutkiewicz R, Freibert SA et al (2015) The role of mitochondria and the CIA machinery in the maturation of cytosolic and nuclear iron-sulfur proteins. Eur J Cell Biol 94:280–291. https://doi.org/10.1016/j.ejcb.2015.05.002
Maralikova B, Ali V, Nakada-Tsukui K et al (2010) Bacterial-type oxygen detoxification and iron-sulfur cluster assembly in amoebal relict mitochondria. Cell Microbiol 12:331–342. https://doi.org/10.1111/j.1462-5822.2009.01397.x
Martijn J, Ettema TJG (2013) From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem Soc Trans 41:451–457. https://doi.org/10.1042/BST20120292
McIntosh JR (1973) The axostyle of Saccinobaculus. II. Motion of the microtubule bundle and a structural comparison of straight and bent axostyles. J Cell Biol 56:324–339
Mi-ichi F, Abu Yousuf M, Nakada-Tsukui K, Nozaki T (2009) Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc Natl Acad Sci U S A 106:21731–21736. https://doi.org/10.1073/pnas.0907106106
Nie D (1950) Morphology and taxonomy of the intestinal Protozoa of the Guinea-pig, Cavia porcella. J Morphol 86:381–494. https://doi.org/10.1002/jmor.1050860302
Noda S, Inoue T, Hongoh Y et al (2006) Identification and characterization of ectosymbionts of distinct lineages in Bacteroidales attached to flagellated protists in the gut of termites and a wood-feeding cockroach. Environ Microbiol 8:11–20. https://doi.org/10.1111/j.1462-2920.2005.00860.x
Novák L, Zubáčová Z, Karnkowska A et al (2016) Arginine deiminase pathway enzymes: evolutionary history in metamonads and other eukaryotes. BMC Evol Biol 16:197. https://doi.org/10.1186/s12862-016-0771-4
Nývltová E, Šuták R, Harant K et al (2013) NIF-type iron-sulfur cluster assembly system is duplicated and distributed in the mitochondria and cytosol of Mastigamoeba balamuthi. Proc Natl Acad Sci U S A 110:7371–7376. https://doi.org/10.1073/pnas.1219590110
Poinar G Jr (2009) Early cretaceous protist flagellates (Parabasalia: Hypermastigia: Oxymonada) of cockroaches (Insecta: Blattaria) in Burmese amber. Cretac Res 30:1066–1072. https://doi.org/10.1016/j.cretres.2009.03.008
Radek R (1994) Monocercomonides termitis n. sp., an oxymonad from the lower termite Kalotermes sinaicus. Arch Protistenkd 144:373–382. https://doi.org/10.1016/S0003-9365(11)80240-X
Roche B, Aussel L, Ezraty B et al (2013) Iron/sulfur proteins biogenesis in prokaryotes: formation, regulation and diversity. Biochim Biophys Acta 1827:455–469. https://doi.org/10.1016/j.bbabio.2012.12.010
Roger AJ, Silberman JD (2002) Cell evolution: mitochondria in hiding. Nature 418:827–829
Roger AJ, Muñoz-Gómez SA, Kamikawa R (2017) The origin and diversification of mitochondria. Curr Biol 27:R1177–R1192. https://doi.org/10.1016/j.cub.2017.09.015
Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:255–274
Schofield PJ, Edwards MR, Matthews J, Wilson JR (1992) The pathway of arginine catabolism in Giardia intestinalis. Mol Biochem Parasitol 51:29–36
Slamovits CH, Keeling PJ (2006a) Pyruvate-phosphate dikinase of oxymonads and Parabasalia and the evolution of pyrophosphate-dependent glycolysis in anaerobic eukaryotes. Eukaryot Cell 5:148–154. https://doi.org/10.1128/EC.5.1.148
Slamovits CH, Keeling PJ (2006b) A high density of ancient spliceosomal introns in oxymonad excavates. BMC Evol Biol 6(34):34. https://doi.org/10.1186/1471-2148-6-34
Stairs CW, Eme L, Brown MW et al (2014) A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia. Curr Biol 24:1176–1186. https://doi.org/10.1016/j.cub.2014.04.033
Treitli SC, Kotyk M, Yubuki N, Jirounková E, Vlasáková J, Smejkalová P, Šípek P, Čepička I, Hampl V (2018) Molecular and morphological diversity of the oxymonad genera Monocercomonoides and Blattamonas gen. nov. Protist 169(5):744–783. https://doi.org/10.1016/j.protis.2018.06.005
Tsaousis AD, Ollagnier de Choudens S, Gentekaki E et al (2012) Evolution of Fe/S cluster biogenesis in the anaerobic parasite Blastocystis. Proc Natl Acad Sci U S A 109:10426–10431. https://doi.org/10.1073/pnas.1116067109
Utami YD, Kuwahara H, Igai K et al (2018) Genome analyses of uncultured TG2/ZB3 bacteria in “Margulisbacteria” specifically attached to ectosymbiotic spirochetes of protists in the termite gut. ISME J 13:455. https://doi.org/10.1038/s41396-018-0297-4
Vacek V, Novák LVF, Treitli SC et al (2018) Fe-S cluster assembly in oxymonads and related protists. Mol Biol Evol. https://doi.org/10.1093/molbev/msy168
Williams BAP, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865–869
Yarlett N, Martinez MP, Moharrami MA, Tachezy J (1996) The contribution of the arginine dihydrolase pathway to energy metabolism by Trichomonas vaginalis. Mol Biochem Parasitol 78:117–125. https://doi.org/10.1016/S0166-6851(96)02616-3
Yutin N, Wolf MY, Wolf YI, Koonin EV (2009) The origins of phagocytosis and eukaryogenesis. Biol Direct 4:9. https://doi.org/10.1186/1745-6150-4-9
Zachar I, Szathmáry E (2017) Breath-giving cooperation: critical review of origin of mitochondria hypotheses. Biol Direct 12:19. https://doi.org/10.1186/s13062-017-0190-5
Zhang Q, Táborský P, Silberman JD et al (2015) Marine isolates of Trimastix marina form a plesiomorphic deep-branching lineage within Preaxostyla, separate from other known trimastigids (Paratrimastix n. Gen.). Protist 166:468–491. https://doi.org/10.1016/j.protis.2015.07.003
Zubáčová Z, Novák L, Bublíková J et al (2013) The mitochondrion-like organelle of Trimastix pyriformis contains the complete glycine cleavage system. PLoS One 8:e55417. https://doi.org/10.1371/journal.pone.0055417
Acknowledgement
The salary of VH was funded from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No 771592), from the Centre for research of pathogenicity and virulence of parasites reg. nr.: CZ.02.1.01/0.0/0.0/16_019/0000759, from the Ministry of Education, Youth and Sports of CR within the National Sustainability Program II (Project BIOCEV-FAR) LQ1604 and from the project ‘BIOCEV’ (CZ.1.05/1.1.00/02.0109).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Hampl, V. (2019). Organisms Without Mitochondria, How It May Happen?. 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_13
Download citation
DOI: https://doi.org/10.1007/978-3-030-17941-0_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-17940-3
Online ISBN: 978-3-030-17941-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)