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Where did your cells come from?

Where did your complex cells come from? A new model literally turns an old theory inside out.

If you look at your cells under a microscope, you’ll see nearly all of them have a nucleus, mitochondria and other equipment inside them. Eukaryotic cells, cells with a nucleus, are the basis of all complex life fungi, plants and us. The change from prokaryotic cell to complex cell is profoundly important to evolution of life, but how did it happen?

The favoured explanation has been that an archaeon swallowed a bacterium. The two developed a symbiotic relationship and evolved into eukaryotes. This explanation bothers me slightly because it needs the pair to do a lot of work fast, but I suppose if archaea are eating bacteria millions upon millions of times each day, then they’re making a lot of attempts.

David Baum, a University of Wisconsin-Madison professor of botany and evolutionary biologist, has proposed a new model for eukaryote evolution. His model is inside out and, to a non-biologist like me, it looks plausible.

Baum and his cousin Buzz Baum at UCL, argue that archaea developed protrusions called blebs, little arms if you like. These enabled the cells to interact with their environment better. Along the way they encountered bacteria and started to develop ways to exploit the energy of bacteria, while the bacteria were still outside the cell. The cells that did this better survived more often and reproduced until they had engulfed the bacterium.

Inside-out model for the evolution of eukaryotic cell organization. Model showing the stepwise evolution of eukaryotic cell organization from (A) an eocyte ancestor with a single bounding membrane and a glycoprotein rich cell wall (S-layer) interacting with epibiotic α-proteobacteria (proto-mitochondria). (B) We envision the eocyte cell forming protrusions, aided by protein-membrane interactions at the protrusion neck. These protrusions facilitated material exchange with proto-mitochondria. (C) Selection for a greater area of contact between the symbionts would have led to bleb enlargement and the eventual loss of the S-layer from the protrusions. (D) Blebs would have then been further stabilized by the development of a symmetric nuclear pore outer ring complex (Figure 2) and through the establishment of LINC complexes that, following the gradual loss of the S-layer, physically connected the original cell body (the nascent nuclear compartment) to the inner bleb membranes. (E) With the expansion of blebs to enclose the proto-mitochondria, a process that would have facilitated the acquisition of bacterial lipid biosynthesis machinery by the host, the site of cell growth would have progressively shifted to the cytoplasm, facilitated by the development of regulated traffic through the nuclear pore. At the same time, the spaces between blebs would have enabled the gradual maturation of proteins secreted into the environment via the perinuclear space through glycosylation and proteolytic cleavage. (F) Finally, bleb fusion would have connected cytoplasmic compartments and driven the formation of an intact plasma membrane, perhaps through a process akin to phagocytosis whereby one bleb enveloped the whole. This simple topological transition would have isolated the endoplasmic reticulum from the outside world, driven the full development of a system of vesicular trafficking, and established strict vertical transmission of mitochondria, leading to a cell with modern eukaryotic cell organization. Baum and Baum BMC Biology 2014 12:76   doi:10.1186/s12915-014-0076-2
Inside-out model for the evolution of eukaryotic cell organization. Model showing the stepwise evolution of eukaryotic cell organization from
(A) an eocyte ancestor with a single bounding membrane and a glycoprotein rich cell wall (S-layer) interacting with epibiotic α-proteobacteria (proto-mitochondria).
(B) We envision the eocyte cell forming protrusions, aided by protein-membrane interactions at the protrusion neck. These protrusions facilitated material exchange with proto-mitochondria.
(C) Selection for a greater area of contact between the symbionts would have led to bleb enlargement and the eventual loss of the S-layer from the protrusions.
(D) Blebs would have then been further stabilized by the development of a symmetric nuclear pore outer ring complex (Figure 2) and through the establishment of LINC complexes that, following the gradual loss of the S-layer, physically connected the original cell body (the nascent nuclear compartment) to the inner bleb membranes.
(E) With the expansion of blebs to enclose the proto-mitochondria, a process that would have facilitated the acquisition of bacterial lipid biosynthesis machinery by the host, the site of cell growth would have progressively shifted to the cytoplasm, facilitated by the development of regulated traffic through the nuclear pore. At the same time, the spaces between blebs would have enabled the gradual maturation of proteins secreted into the environment via the perinuclear space through glycosylation and proteolytic cleavage.
(F) Finally, bleb fusion would have connected cytoplasmic compartments and driven the formation of an intact plasma membrane, perhaps through a process akin to phagocytosis whereby one bleb enveloped the whole. This simple topological transition would have isolated the endoplasmic reticulum from the outside world, driven the full development of a system of vesicular trafficking, and established strict vertical transmission of mitochondria, leading to a cell with modern eukaryotic cell organization.
Baum and Baum BMC Biology 2014 12:76 doi:10.1186/s12915-014-0076-2

What I like is that there are steps to bringing the bacterium inside the cell, instead of Pow! it’s there and everything has to develop now. That’s probably an unfair over-simplication of the standard model, but the inside-out model makes sense as each step along the way seems to either use material it already has, or confer a small advantage for survival by itself.

While the event happened unseen billions of years ago, Baum and Baum have some ideas of how they can test the idea. Genetic data could help indicate that an inside out model is more likely than the standard model. Their model predicts that some parts of the cell developed in the opposite order to the standard model, though I’ll admit I don’t understand the details of how “COPII-like coatomers are derived from structural components of the nuclear pore, rather than the reverse”. However, I can see a list of clear predictions that Baum and Baum are making that someone can test, even if it’s clearly not me.

Fossil data would be nice, but highly unlikely, but there is another prediction. If prokaryotes can gain an advantage by developing blebs to interact with bacteria, then it should be possible to see some prokaryotes in the wild that look like the first eukaryote before it engulfed its partner.

Best of all, it’s a very positive paper. Baum and Baum aren’t simply saying everyone else is wrong, they’re proposing new topics to research and new things to study, new ways to look at problems. Even if it turns out they’re wrong, they could be wrong in a really interesting and helpful way.

You can pick up the paper through Open Access from BMC Biology.

Baum D.A. & Baum B. (2014). An inside-out origin for the eukaryotic cell, BMC Biology, 12 (1) 76. DOI: http://dx.doi.org/10.1186/s12915-014-0076-2

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