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Plausible evolutionary theory suggests eukaryotes might have evolved “inside-out”

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Posted October 29, 2014

The events that took place in the primeval Earth and gave rise to all eukaryotic life as we know it today (including ourselves) is by all means a subject of great interest. Yet, what was happening billions of years ago is hard to pinpoint, and the key transition of prokaryotic-to-eukaryotic cell is still subject to some contradictory theories.

Saccharomyces cerevisiae cells in DIC microscopy. Saccharomyces cerevisiae was the first eukaryotic organism to have its complete genome sequence determined. Image credit: Masur via Wikipedia.

Saccharomyces cerevisiae cells in DIC microscopy. Saccharomyces cerevisiae was the first eukaryotic organism to have its complete genome sequence determined. Image credit: Masur via Wikipedia.

One of the predominant views on the topic suggests the first eukaryotic cell took its stand when it figured out how to make internal organelles – either by internalization of the outside membrane or phagocytosis of other prokaryotes. The theory states that mitochondria were formed when a progenitor cell engulfed an α-proteobacteria. Other organelles, including the nucleus, were acquired either the same way or by reorganizing existing membranes within the cell. This is known as the “outside-in” hypothesis.

Today, researchers David Baum and Buzz Baum provide an alternative hypothesis for the origin of eukaryotic life. Their paper arguing for an “inside-out” theory was published yesterday (Oct 28) in BMC Biology. The authors claim their model is plausible enough to explain one of the key transitions in the evolution of life and may outcompete other theories in solving some of the more quirky aspects of eukaryotic biology.

“The inside-out model provides a simple stepwise path for the evolution of eukaryotes, which, we argue, fits the existing data at least as well as any current theory. Further, it sheds new light on previously enigmatic features of eukaryotic cell biology, including those that led others to suggest the need to revise current cell theory,” the authors said.

Organelles formed from external membrane “blebs”

Contradictory to the common view, the inside-out theory suggests the first eukaryotic cells evolved from a mutualistic relationship between an archaeal host that gradually extended its membranes to wrap around a “hitchhiker” bacteria (an ectosymbiont). Subject to the selective forces of the environment, the host archaeon would have benefited from keeping its ectosymbiont close enough for material exchange to take place. Therefore it formed membrane “blebs” around the bacteria, which would later become mitochondria.

The inside-out hypothesis of eukaryote evolution states the ancestral archaeon formed membrane “blebs” and gradually wrapped around its ectosymbiont, which gave rise to mitochondria. Extracellular membrane protrusions also formed the ER, which facilitated material transfer. Lastly, a cytoplasm and an external membrane formed around the organelles closing them off from the environment and completing the first eukaryotic cell. Image courtesy of the researchers.

The inside-out hypothesis of eukaryote evolution states the ancestral archaeon formed membrane “blebs” and gradually wrapped around its ectosymbiont, which gave rise to mitochondria. Extracellular membrane protrusions also formed the ER, which facilitated material transfer. Lastly, a cytoplasm and an external membrane formed around the organelles closing them off from the environment and completing the first eukaryotic cell. Image courtesy of the researchers.

With time, external membrane protrusions developed further, protecting the ectosymbiont from pathogens and other environmental challenges. The ever-growing membrane network then formed into the endoplasmic reticulum (ER), which provided an even more sophisticated secretory system between the two organisms. Lastly, a cytoplasm formed outside of the ER and the mitochondria, and another layer of the membrane closed the whole system off from the environment.

Most importantly, the theory suggests the eukaryotic nucleus is in fact the relic of the ancestral archaeon, which remained largely intact during the prokaryote-to-eukaryote transition. This is in agreement with the fact that eukaryotic nuclei are similar in size to some ancestral archaea and helps explain the double nuclear membrane, which is shared with the ER. Therefore the nucleus is actually the oldest part of the cell, rather than being acquired through phagocytosis or organization of internal membranes in the developing eukaryote.

The simplest answer to multiple questions in eukaryote evolution

Although such billion-year-old events are difficult to verify, the theory is supported by several lines of evidence, including phylogenetic data. For example, phylogenomic studies have identified α-proteobacteria, which later became mitochondria, as the source of proteins required for phagocytosis. This challenges the common view that mitochondria were acquired by one prokaryote engulfing the other. In fact, the ancestral archaeon would have had no way to engulf the proto-mitochondria, as they themselves held the original phagocytosis machinery in the first place. This is where the inside-out hypothesis gains the lead.

Moreover, the model provides quite a simple explanation for other features of eukaryote cell organization, including why the nucleus has no internal organelles and shares a membrane with the ER, why the ER forms a continuous network within the cytoplasm etc. While outside-in models do provide acceptable hypotheses for these questions, the inside-out theory is the most parsimonious in that the simple stepwise process solves many problems of eukaryote evolution in one go.

As one the strengths of their theory, the authors the set of predictions within the model are testable both by current evidence and findings anticipated in the near future. And, at the very least, challenging the conventional models is bound to advance our understanding of eukaryote evolution.

“We are optimistic that the effort to evaluate it will spawn new cell biological discoveries and, in so doing, improve our understanding of the biology of archaeal and eukaryotic cells as they grow and divide,” said the researchers.

Written by Eglė Marija Ramanauskaitė

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