Cultivating the Ancestors… (2|4)

by Christoph
 

A model for eukaryogenesis

Based on their knowledge of the morphology of P. syntrophicum MK-D1 from electron micro­scopy and their knowledge of its physiology from growth assays and genome analysis, Imachi, Nobu et al. (2020) propose a hypothetical model, the E3 model, of how the first evolution­ary steps towards eukaryogenesis might have occurred in an ancestral archaeon living ~2 billion years ago. I quote their comments on Figure 3 verbatim, with my remarks in square bracketts:

(click to enlarge)
Figure 3. Proposed hypothetical model for eukar­yo­ge­ne­sis (E3). See text for details. Modified from Source. Frontispiece: Promethearchaeum syntrophi­cum MK-D1. Scale bar, 500 nm. Source

a  The syntrophic/fermentative host archaeon ['Asgard' branch] is suggested to degrade amino acids to short-chain fatty acids and hydrogen (H2), possibly by interacting with H2-scavenging (and indirectly O2-scavenging) sulfate-reducing bacteria (SRB) (orange).

b  The host may have further inter­acted [during/after the Great Oxidation Event (GOE)] with a facultatively aerobic organotrophic partner that could scavenge toxic O2 (the future mitochon­drion; red). Continued interaction with SRB could have been beneficial but not necessarily es­sential; dotted arrows indicate the inter­action.

c  Host ex­ternal structures [blebs, protrusions] could have interacted (for example, mechanical or biological fusion) with the aerobic partner to en­hance physical interaction and further en­gulf the partner for simultaneous de­velopment of endosymbiosis and a primitive nucleoid-bounding membrane.

d  After engulfment, the host and symbiont could have continued the interaction shown in b as a primitive type of endosym­biosis.

e  Development of ADP/ATP carrier (AAC) by the endosymbiont (the initial direction of ATP trans­port remains unclear).

f  Endogenization of partner sym­bio­sis by the host through delegation of catabolism and ATP generation to the endosymbiont and establishment of a symbiont-to-host ATP channel.
 

Note  Masaru Nobu explained the E3 model in more detail than I can here in his recorded contribution to the JGI2021 Meeting.
 

Another model for eukaryogenesis

Older models of eukaryogenesis posited that evolving the capability for endocytosis was a prerequisite for the uptake of a (future) mitochondrion by the progenitor of the eukaryotic cell (Outside-in Model(s)). This was turned on its head in the 'Inside-out Model' (IoM) by Baum & Baum (2014), in which "classical" endocytosis comes as the last evolutionary step, after the internali­za­tion of the (future) mitochondrion:

(click to enlarge)
Figure 4. Inside-out model (IoM) for the evolution of eu­karyotic cell organization. See text for details. Source

A  Model showing the stepwise evolution of eukaryotic cell organization from 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 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.
 

The E3 model proposed by Imachi, Nobu et al. (2020) is largely congruent with the IoM, but, in contrast to the latter, less detailed in the expansion of the protrusions to finally cover the facultatively aerobic organo­trophic partner (step c), and in the formation of the primordial nucleus by con­verting the pro­trusions into nuclear pores (step d). Both models remain somewhat vague as to when, in the sequence of steps towards an in­ter­nalized proto-mitochondrion, a complete transformation of the archaeal genome into a eu­kar­y­otic genome might occur. The genome of P. syn­trophicum MK‑D1 is organized as a typical prokaryotic genome in a (circular) chromosome. All known eukaryotic genomes are organized in a varying number of (mostly) linear chromosomes. The importance of this transition can be inferred from the fact that most genes encoding ribo­somal proteins are organized as small and larger operonss in 'Asgard' archaea, whereas in eukaryotes they are widely distributed as single genes across several chro­mosomes.
 

Addendum You might enjoy reading in his own words how Masaru Nobu and his colleagues went from being sewage engineers to microbiologists to evolu­tion­ary biologists. Addressing the reader, he ended his account with: "...Every time you flush the toilet, you may very well be feeding engineered reactor ecosystems that inspired discovery of the domain Archaea and cultivation of syntrophic archaea closely related to our ancestors".
 

In parts 3+4 of Cultivating the Ancestors…, I will show that Promethearchaeum syntrophicum MK-D1 is not a maverick among the 'Asgard' archaea, but a member of a family that occurs all over the world with similar physiological and cellular properties, including dependence on syntrophy, a penchant for blebbing, and those characteristic protrusions, the "tiny arms".

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