The Origin of Eukarya; Evidence behind an old debate.

From multicellular giants to microscopic protists, the eukaryotes contain the most complex forms of life that Earth has to offer. It is a fascinating prospect that the diverse eukaryotic kingdoms were all derived from a common ancestor. Explaining the origins of this ancestor has been problematic and inspiring of countless hypotheses. Many textbooks will speak of three primary domains in the tree of life; Archaeabacteria, Eubacteria and the Eukarya. These are usually depicted so that Eukarya are more closely related to the Archaeabacteria (Archaea) than Eubacteria (Bacteria)[1](Figure1A). In this tree arrangement all three domains are deemed monophyletic lineages that arose about the same time. The three domains hypothesis is one of many hypotheses that suggest an autogeneous origin for the eukaryotes. An autogeneous origin would mean that Eukaryotes emerged and developed all of their complexities, through stepwise mutation, without any external genetic material[2].This is certainly perplexing when you consider it has been widely accepted that mitochondria, the organelle responsible for the production of cellular energy, has a bacterial origin[3,4] . Those in favour of an autogeneous origin of eukaryotes do not discard the fact that an endosymbiosis of the mitochondrial ancestor occurred, nor do they discard that this was a landmark event in biological history.  They just believe the eukaryotic cell was well established before this event occurred[2] (Figure1B). There is a strong opposing argument to the various autogeneous models and these differ in two vital aspects. The first is that there were only two primary domains; Bacteria and Archaea (Figure1C). Eukarya emerged much later as the result of an endosymbiosis event between an Archaeon and an alphaproteobacterium; the mitochondrial ancestor[2,5] (Figure1D) The mutual exclusivity of these two arguments has led to much debate over the past decades. In this blog I shall look at the current evidence to see which argument has the most backing.

1: The Two Arguments. A) The three domains tree. B) An autogeneous view on the endosymbiosis event. C) A tree depicting only two primary lineages with Eukarya emerging late. D) The endosymbiosis view on the origin of Eukarya.

The autogeneous model initially appears to be supported by many phylogenetic studies. When looking at particular genes that are known to be highly conserved, such as ribosomal genes, the trees form to resemble that of the three domains hypothesis[2]. Phylogenetics has however become more sophisticated in recent years, with broader analysis over entire genomes now possible. The new trees indicate 2 primary lineages with the eukaryotes arising later from the archaeal lineage[2]. Thus modern phylogenetic evidence actually backs the endosymbiosis argument. But what about the hard evidence in the fossil records?

Earth is thought to be 4.5 billion years old and the earliest evidence for life are inclusions of minerals found in the rocks of Greenland. These inclusions are dated back to 3.85 billion years ago [6]. The oldest remnants of cells to be found are 3.4 billion years old, and these are undistinguishable in terms of domain. What is certain is that these ancient cells showed no signs of any characteristic features of eukaryotes. The oldest confirmed eukaryotic fossils are approximately 1.6-1.8 billion years old which is coherent with the predicted emergence of extant eukaryotes from molecular clock studies [7,8]. Until a eukaryotic fossil that predates 3.4billion years is identified, the fossil records will remain in agreement with a later emergence of eukaryotes.

A seemingly glaring fault in the endosymbiosis argument is that prokaryotic cells cannot undergo cell fusion. Without the ability to take up the mitochondrial ancestor how could this event define the origin of eukaryotes? Many Eukaryotic cells have the ability to engulf others through phagocytosis. Actin proteins form structures called lamellipodia or filopodia which allow this engulfment and fusion [2]. For an alphaproteobacterium to be taken up, the host must have been an established eukaryote with actin proteins. This seemed the case until it was discovered that some Archaea contain actin like proteins that can also facilitate cell fusions[9]. It is plausible that primitive versions of these actin resembling proteins enabled the uptake of the mitochondrial ancestor[9].

Another key line of evidence that has been assessed is bioenergetics. For a cell to be as complex as a eukaryote, relatively large amounts of energy are required. One study has highlighted that without a sophisticated method of energy production, a cell is not capable of reaching the levels of complexity exhibited by the  eukaryotes. They go on to explore the best ways of producing such an energy source in such a confined space; only to end up describing what is ultimately a mitochondria. Without the mitochondria it would be energetically impossible for the eukaryotes to exist as they do [10]. Furthermore in order for the mitochondria to become established it’s ancestor would have needed to lose most of its genes as to prevent overeplication within in the host cell. This provided a selection advantage for those cells where endosymbiosis gene transfer (EGT) took place. Genetic analysis has unveiled a chimeric nature to the eukaryotic genome that supports such extensive EGT and horizontal gene transfer from other  sources[11]. It has been shown that the majority of housekeeping genes appear to be of archaeal decent whereas the genes involved in metabolism are more closely related to those from bacteria[12]. It is paradoxical for an organism to autogenously materialise with a chimeric genome. This becomes even more confusing when you consider the proposed genetic donors for this chimera, and the chimera itself, are all supposed to have emerged separately and in parallel of each other.

It appears the majority of evidence across a wide variety fields supports an endosymbiosis origin over an autogenous origin for Eukarya. This has significant consequences to how we perceive and depict the tree of life. We should have the two prokaryotic domains as the primary lineages of the tree. Eukaryotes should be regarded as a secondary lineage arising much later as the consequence of an endosymbiosis between the other domains[2]. It is hard to ignore the weight of evidence and so I too support the endosymbiosis argument. The hypothesis that best describes what it think occurred is the Phagocytosing Archaeon and I shall summarise below (Figure2).

2: Phagocytosing Archaeon Theory. 1) Archaeon with first actin like proteins (blue). 2) Loss of cell wall allows evolution of basic cytoskeleton with cellular protrusions. 3) Primitive phagocytic machinery established and uptake of foreign DNA (red, green, yellow, pink, purple) is now possible. 4) Invagination results in a protective boundary around the DNA. 5) Endosymbiosis of the mitochondrial ancestor and EGT leads to increased energy supply, development of cellular complexities and the formation of an early eukaryotic cell [5].

Here an Archaeon containing the first actin-like proteins slowly develops a primitive cytoskeleton. In the process it loses the prokaryotic cell wall. Without a cell wall the actin like proteins could form cellular protrusions resembling phagocytotic machinery. The engulfing of passing prokaryotes would have exposed the cell to large amounts of foreign DNA. Frequent horizontal gene transfer could explain some of the mosaic nature in the eukaryotic genome. A by product of all this random recombination is genetic instability. This in turn may have sped up evolution in these organisms. Which could explain why similarities between eukaryotic and archaeal genes are usually minimal compared to the more extensive conservation seen in Alphaproteobacteria and mitochondria. Next is the compartmentalisation of the genome through invaginations of the cell membrane. This would protect the genome from engulfed genetic material and restabilise its rate of evolution. An alphaproteobacterium is phagocytosed but not degraded and develops a symbiosis. They even speculate that a symbiosis may have been present before phagocytosis. As said the additional energy production could permit all the eukaryotic complexities to arise and develop to how we see them today[5]. The mitochondrial ancestor undergoes reductive evolution to eventually become the organelle we recognise today.

Many other endosymbiosis theories are equally justified as we have no evidence of the intermediary stages eukaryotic evolution to prove otherwise. Although this hypothesis is the one I personally feel is the most intellectually pleasing, I would happily have it proven wrong if any contradictory evidence should arise.

Sources

  1. WOESE, C. R., KANDLER, O. & WHEELIS, M. L. 1990. TOWARDS A NATURAL SYSTEM OF ORGANISMS – PROPOSAL FOR THE DOMAINS ARCHAEA, BACTERIA, AND EUCARYA.Proceedings of the National Academy of Sciences of the United States of America, 87, 4576-4579.
  2. MCINERNEY, J. O., O’CONNELL, M. J. & PISANI, D. 2014. The hybrid nature of the Eukaryota and a consilient view of life on Earth.Nature Reviews Microbiology, 12, 449-455.
  3. GRAY, M. W., BURGER, G. & LANG, B. F. 1999. Mitochondrial evolution.Science,283, 1476-1481.
  4. GRAY, M. W., BURGER, G. & LANG, B. F. 2001. The origin and early evolution of mitochondria.Genome Biology,
  5. MARTIJN, J. & ETTEMA, T. J. G. 2013. From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell.Biochemical Society Transactions, 41, 451-457.
  6. MOJZSIS, S. J., ARRHENIUS, G., MCKEEGAN, K. D., HARRISON, T. M., NUTMAN, A. P. & FRIEND, C. R. L. 1996. Evidence for life on Earth before 3,800 million years ago.Nature, 384, 55-59.
  7. KNOLL, A. H., JAVAUX, E. J., HEWITT, D. & COHEN, P. 2006. Eukaryotic organisms in Proterozoic oceans.Philosophical Transactions of the Royal Society B-Biological Sciences, 361, 1023-1038.
  8. PARFREY, L. W., LAHR, D. J. G., KNOLL, A. H. & KATZ, L. A. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks.Proceedings of the National Academy of Sciences of the United States of America,108, 13624-13629.
  9. YUTIN, N., WOLF, M. Y., WOLF, Y. I. & KOONIN, E. V. 2009. The origins of phagocytosis and eukaryogenesis.Biology Direct,
  10. LANE, N. & MARTIN, W. 2010. The energetics of genome complexity.Nature, 467,929-934.
  11. TIMMIS, J. N., AYLIFFE, M. A., HUANG, C. Y. & MARTIN, W. 2004. Endosymbiotic gene transfer: Organelle genomes forge eukaryotic chromosomes.Nature Reviews Genetics, 5, 123-U16.
  12. RIVERA, M. C., JAIN, R., MOORE, J. E. & LAKE, J. A. 1998. Genomic evidence for two functionally distinct gene classes. Proceedings of the National Academy of Sciences of the United States of America, 95, 6239-6244.

Featured image: https://www.google.co.uk/search?q=the+eukaryotic+cell&rlz=1C1CHFX_en-GBGB450GB450&espv=2&biw=1366&bih=681&source=lnms&tbm=isch&sa=X&ei=eKUaVZywAYzX7QaMt4CYBQ&ved=0CAYQ_AUoAQ#tbm=isch&q=the+eukaryotic+cell+3D&imgdii=_&imgrc=-bgaMgb2j6Vr2M%253A%3BguH4zXFRwULLPM%3Bhttps%253A%252F%252Fc2.staticflickr.com%252F4%252F3020%252F5839627161_46c1610918.jpg%3Bhttps%253A%252F%252Fwww.flickr.com%252Fphotos%252F61048931%2540N08%252F5839627161%252F%3B500%3B500

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