A wise man once said “sometimes you’ve got to go back to actually move forward” (this man was later mocked by a wiser man, which is a subject for another post that I probably won’t get around to writing). After much reflection, I have discovered the true meaning of this purposefully and poetically vague declaration. The well-spoken chauffer was in fact referencing how understanding early eukaryotic evolution can help us interpret the biological processes and cellular mechanisms of modern eukaryotes, which in turn can give us a better appreciation for the origin and diversity of complex life. It’s an insightful message, but I’d expect nothing else from a company whose slogan is “Lincoln: our cars are fine and all but how about the intricacies of cellular biology?*”. Luckily for us, some members of the scientific community have taken this quote to heart by examining the origin of eukaryotic cells. One main objective for many of these studies is to explain how plants, animals, fungi, and other eukaryotes developed all those special bits and pieces (such as a nucleus, an endoplasmic reticulum, and mitochondria) that separate them from prokaryotes.

For many years the prevailing idea was called the endosymbiotic theory, which basically said that one cell engulfed another and boom, nucleus in cell. A key aspect of this theory is that the plasma membrane of the eukaryotic-precursor was the membrane of the original host cell, and the nucleus was derived from the engulfed bacteria. Thus, the outside of the eukaryotic cell as we know it didn’t change much, while the interior of the host cell experienced more drastic modifications. However, a new paper by David and Buzz Baum in BMC Biology proposes a different theory of early eukaryotic evolution. Coined the “inside-out” theory, it claims that the early host cell was in fact the precursor to the nucleus, and that the bacteria (which were the precursor to mitochondria) were slowly engulfed by protrusions extending from the host cell. These protrusions eventually grew large enough to surround the bacteria and the host cell, and eventually became closed off to the external environment, forming the plasma membrane found in modern eukaryotes. The authors suggest that natural selection may have favored larger protrusions, since they would have increased the surface area of the host cell, potentially making any symbiotic relationship with external bacteria more metabolically efficient.

An illustration of Baum and Baum’s “inside-out” theory, taken with permission from their 2014 article “An inside-out origin for the eukaryotic cell” published in BMC Biology.

Ok, you may be saying, but tell me about these fabled mitochondria. Specifically, what were they before they became organelles? Well, a separate paper by Wang and Wu out of the University of Virginia attempts to recreate the ancient pre-mitochondria using primarily phylogenomic data. With this genetic information from mitochondria and their close relatives, the authors hypothesized the structure, metabolism, and ecology of these ancient bacteria. Their results suggest that these premitochondria were capable of more diverse cellular processes than their specialized descendants, including DNA translation, replication, and maintenance, membrane biogenesis, energy production, motility via flagella, and respiration at low oxygen levels. Interestingly, their data also predicted that premitochondria utilized a specific translocase protein that exchanges bacterial ADP with ATP from a host cell. The presence of this protein suggests that premitochondria were internal “energy parasites,” and did not develop a mutualistic relationship with their host until later on down the road. Therefore, the initial symbiotic relationship between the eukaryotic ancestor and premitochondria may not have been one of mutual benefit (gold-diggin bacteria amirite?).

There are still plenty of unanswered questions from these two articles. If the early relationship was not mutualisitic, then you would not expect the host cell’s protrusions to necessarily be a result of a gain in fitness. In fact, if premitochondria were parasitic, then increased surface area resulting in a greater number of bacterial symbionts would seem to be a trait to be selected against (unless the protrusions provided some other fitness benefit that outweighed the increase in parasites). But probably the most pressing question is how and why did premitochondria do a complete 180 and suddenly become generous with their energy production? Evolution isn’t a Charles Dickens Christmas novel. Instead, I’d like to see a study geared towards reconstructing the events that led up to such a drastic change in the relationship dynamics between the early eukaryotic cell and its premitochondria, and how exactly these bacteria became energy producing organelles. Regardless of what future studies may show, it appears that the origin of early complex life, and ultimately the evolution of much of Earth’s biodiversity, may be more enigmatic than previously thought.

*If anyone from Lincoln’s HR department is reading this, let me know where I should send my resume.

November 25, 2014