Eukaryotes without Mitochondria and Aristotle’s Ladder of Life

In 348/7 BC, fearing anti-Macedonian sentiment or disappointed with the control of Plato’s Academy passing to Speusippus, Aristotle left Athens for Asian Minor across the Aegean sea. Based on his five years[1] studying of the natural history of Lesbos, he wrote the pioneering work of zoology: The History of Animals. In it, he set out to catalog the what of biology before searching for the answers of why. He initiated a tradition of naturalists that continues to this day.

Aristotle classified his observations of the natural world into a hierarchical ladder of life: humans on top, above the other blooded animals, bloodless animals, and plants. Although we’ve excised Aristotle’s insistence on static species, this ladder remains for many. They consider species as more complex than their ancestors, and between the species a presence of a hierarchy of complexity with humans — as always — on top. A common example of this is the rationality fetish that views Bayesian learning as a fixed point of evolution, or ranks species based on intelligence or levels-of-consciousness. This is then coupled with an insistence on progress, and gives them the what to be explained: the arc of evolution is long, but it bends towards complexity.

In the early months of TheEGG, Julian Xue turned to explaining the why behind the evolution of complexity with ideas like irreversible evolution as the steps up the ladder of life.[2] One of Julian’s strongest examples of such an irreversible step up has been the transition from prokaryotes to eukaryotes through the acquisition of membrane-bound organelles like mitochondria. But as an honest and dedicated scholar, Julian is always on the lookout for falsifications of his theories. This morning — with an optimistic “there goes my theory” — he shared the new Kamkowska et al. (2016) paper showing a surprising what to add to our natural history: a eukaryote without mitochondria. An apparent example of a eukaryote stepping down a rung in complexity by losing its membrane-bound ATP powerhouse.

Before jumping into Kamkowska et al. (2016), some background is essential.

For biologists, the most important distinction among organisms is the one between prokaryotes and eukaryotes:

  • Prokaryotes (bacteria and archaea) make up most of the biomass of living things on Earth and are defined by their lack of a membrane-bound nucleus containing their DNA. They are exclusively unicellular, although sometimes organizing into cooperatives like biofilms. Their reproduction is asexual, although they are capable of horizontal gene-transfer through means like plasmid endosymbiosis.
  • Eukaryotes make up most of what we encounter as life, including ourselves. They are defined by the presence of a membrane-bound nucleus and — typically — other membrane-bound organelles like mitochondria. They are capable of both asexual and sexual reproduction, and contain both unicellular — like yeast or slime molds — and multicellular organisms.

From the perspective of evolution, the last common ancestor of eukaryotes and prokaryotes was a prokaryote. In fact, some of the popular — although speculative, but generally accepted — chimeric symbiogenesis theories posit that the first eukaryote arose from an archae that consumed and became endosymbiotic with a bacteria (Martin & Müller, 1998; Moreira & López-García, 1998). Some of the free living functionality of bacteria eventually decayed, and they became the first mitochondria (Huynen, Duarte, & Szklarczy, 2013).

For many biologists, this was the most important moment in history. The first rung on the ladder of life:

In recent years, the central role that the acquisition of mitochondria plays in the evolutionary history of eukaryotes has elevated the mitochondria, or mitochondrion-related organelles, to a defining feature of eukaryotes. Until yesterday — for many — being a eukaryote meant having mitochondria. But now, Karnkowska et al. (2016) showed us that mitochondria can be completely absent from a eukaryote, by finding a eukaryote with no trace of mitochondrion-related organelles. This organism is Monocercomonoides sp. PA203, an endobiotic oxymonads.[3] Monocercomonoides is a eukaryote with a clear membrane-bound nucleus, and even genes coding for other membrane-bound organelles like the Golgi body, that is a unicellular symbiont dependent on its animal host for survival.[4] This particular strain was isolated in 1993 by Jaroslav Kulda from a long-tailed chinchilla.

In addition to demonstrating the absence of mitochondria in a eukaryote, Karnkowska et al. (2016) showed that this is due to a complete loss — and not just degradation or ancestral absence — of the mitochondrial organelle. This suggests that mitochondria are not ratcheted into eukaryotes. They are not a necessary rung on the ladder of life. The complexity associated with mitochondria can be lost in discrete steps — and not just vestigial degradation through disuse — of similar size to the ones that gained them.

Further, the metabolism functionality of the mitochondria in Monocercomonoides sp. PA203 is replaced by another gift from bacteria: cytosolic sulfur mobilization system acquired through horizontal gene transfer. The cell — like other organisms with reduced mitochondria — is not capable of aerobic energy generation, containing no encodings of enzymes associated with the Krebs cycle or electron transport chain proteins. Instead, it relies completely on glycolysis, containing enzymes for the extended pathways, anaerobic fermentation, and three genes for for enzymes in the arginine deiminase pathway. In the place of mitochondria, the organism relies on an array of alternative power sources for the cell.

For me, this finding highlights the best aspects of Aristotle’s traditional: the finding of whats that demand radical rethinking of our whys. It also helps to push us to abandon faulty parts of Aristotle like the ladder of life. By pulling out the first rung, Karnkowska et al. (2016) help us question evolution as an irreversible progressive that climbs ever higher.

Notes and References

  1. Before returning to Macedonia to tutor Alexander the Great, and that to Athens to found the Lyceum and probably write The History of Animals and many of his other texts.
  2. He recently started to ground this more formally in his theory of supply driven evolution (Xue et al., 2014a,b). Although I think this aspect of Julian’s work is great, we have always been at odds about the ladder of complexity.
  3. Here, there is also some interesting history. In the late 80s, Thomas Cavalier-Smith (1987, 1989) thought that he had identified the first eukaryotes without mitochondria. He named these archezoa and proposed a hypothesis that their last common ancestor with the other eukaryotes was from a stage before the mitochondria were engulfed into endosymbiosis. But new tools allowed later research (Mai et al., 1999; Tovar et al., 1999; Williams et al., 2002) to show that there were mitochondrial remnants in these cells. Metamonada were originally part of Cavalier-Smith’s archezoa and the author’s Monocercomonoides sp. PA203 (and the endobiotic oxymonads, more generally) belong to the least studied parts of the former archezoa. This means that Cavalier-Smith was looking in the right place for mitochondria-less eukaryotes, but it also means that the Karnkowska et al. (2016) need to worry about improved detection tools in future research. As always, a negative statement — the absence of mitochondria — is extremely difficult for science.
  4. The dependence on other organisms for existence, makes this finding a little less exciting from the perspective of complexity reduction. Since it places it the same camp as many known parasites, and cancers. Not being completely free-living, means one can argue that the proper unit for analyzing the complexity is the Monocercomonoides + the chinchilla in which it lives. That unit is surely not less complex — in any drastic way — than its predecessors.

Cavalier-Smith, T. (1987). Eukaryotes with no mitochondria. Nature, 326: 332-333.

Cavalier-Smith, T. (1989). Archaebacteria and Archezoa. Nature, 339(6220): 100.

Huynen, M. A., Duarte, I., & Szklarczyk, R. (2013). Loss, replacement and gain of proteins at the origin of the mitochondria. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1827(2): 224-231.

Karnkowska, A., Vacek, V., Zubáčová, Z., Treitli, S., Petrželková, R., Eme, L., Novák, L., Žárský, V., Barlow, L., Herman, E., Soukal, P., Hroudová, M., Doležal, P., Stairs, C., Roger, A., Eliáš, M., Dacks, J., Vlček, C., & Hampl, V. (2016). A Eukaryote without a Mitochondrial Organelle. Current Biology, 26, 1-11 DOI: 10.1016/j.cub.2016.03.053

Mai, Z., Ghosh, S., Frisardi, M., Rosenthal, B., Rogers, R., & Samuelson, J. (1999). Hsp60 is targeted to a cryptic mitochondrion-derived organelle (“crypton”) in the microaerophilic protozoan parasite Entamoeba histolytica. Molecular and Cellular Biology, 19(3): 2198-2205.

Martin, W., & Müller, M. (1998). The hydrogen hypothesis for the first eukaryote. Nature, 392(6671): 37-41.

Moreira, D., & López-García, P. (1998). Symbiosis between methanogenic archaea and δ-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. Journal of Molecular Evolution, 47(5): 517-530.

Tovar, J., Fischer, A., & Clark, C. G. (1999). The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Molecular Microbiology, 32(5): 1013-1021.

Williams, B. A., Hirt, R. P., Lucocq, J. M., & Embley, T. M. (2002). A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature, 418(6900): 865-869.

Xue, J.Z., Costopoulos, A., & Guichard, F. (2015a). A Trait-based framework for mutation bias as a driver of long-term evolutionary trends. Complexity.

Xue, J.Z., Kaznatcheev, A., Costopoulos, A., & Guichard, F. (2015b). Fidelity drive: A mechanism for chaperone proteins to maintain stable mutation rates in prokaryotes over evolutionary time. Journal of Theoretical Biology, 364: 162-167.

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About Artem Kaznatcheev
From the Department of Computer Science at Oxford University and Department of Translational Hematology & Oncology Research at Cleveland Clinic, I marvel at the world through algorithmic lenses. My mind is drawn to evolutionary dynamics, theoretical computer science, mathematical oncology, computational learning theory, and philosophy of science. Previously I was at the Department of Integrated Mathematical Oncology at Moffitt Cancer Center, and the School of Computer Science and Department of Psychology at McGill University. In a past life, I worried about quantum queries at the Institute for Quantum Computing and Department of Combinatorics & Optimization at University of Waterloo and as a visitor to the Centre for Quantum Technologies at National University of Singapore. Meander with me on Google+ and Twitter.

One Response to Eukaryotes without Mitochondria and Aristotle’s Ladder of Life

  1. Pingback: Cataloging a year of blogging: complexity in evolution, general models, and philosophy | Theory, Evolution, and Games Group

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