Alternating terminal electron‐acceptors at the basis of symbiogenesis: How oxygen ignited eukaryotic evolution

Abstract

What kind of symbiosis between archaeon and bacterium gave rise to their eventual merger at the origin of the eukaryotes? I hypothesize that conditions favouring bacterial uptake were based on exchange of intermediate carbohydrate metabolites required by recurring changes in availability and use of the two different terminal electron chain acceptors, the bacterial one being oxygen. Oxygen won, and definitive loss of the archaeal membrane potential allowed permanent establishment of the bacterial partner as the proto-mitochondrion, further metabolic integration and highly efficient ATP production. This represents initial symbiogenesis, when crucial eukaryotic traits arose in response to the archaeon-bacterium merger. The attendant generation of internal reactive oxygen species (ROS) gave rise to a myriad of further eukaryotic adaptations, such as extreme mitochondrial genome reduction, nuclei, peroxisomes and meiotic sex. Eukaryotic origins could have started with shuffling intermediate metabolites as is still essential today.

Unmiraculous? Yes. Ancient? Probably not. (Response to DOI 10.1002/bies.201700041)

“…The logical evolution of the metabolic rewiring starting with the exchange of intermediate carbohydrate metabolites and extensive ROS signalling nicely fits with what we find in present-day eukaryotes [2]. I want to end by saying that I appreciated the remark "Speijer has made very important contributions to our understanding of peroxisomes and oxygen.…”

“…In his commentary [1] regarding my recent article proposing that the original symbiosis at the basis of the eukaryotes was based on exchange of intermediate carbohydrate metabolites [2], instead of hydrogen [3], William Martin makes a few assumptions that (alas!) are incorrect.…”

Evolution of peroxisomes illustrates symbiogenesis

“…OMV's containing metabolic modules could also have been at the basis of lysosome and ER evolution. Of note, this does not mean that metabolic pathways are easily duplicated or relocated in cells during evolution (see [24] and references therein). In this hypothetical scenario, gene migration to the nucleus, which occurs much more easily, and organelle targeting would stabilize the situation in the evolving eukaryote.…”

“…I originally thought such phagocytic capabilities not unlikely [54], but actually there are many arguments against it, see e.g. [22,24]. Though the archaeal host thus already seems to have had some important components for later phagocytosis, the process is still missing many key pieces that have to come from the bacterial endosymbiont and others that we have to classify as "eukaryotic inventions".…”

“…Though the archaeal host thus already seems to have had some important components for later phagocytosis, the process is still missing many key pieces that have to come from the bacterial endosymbiont and others that we have to classify as "eukaryotic inventions". There are no indications that the archaea in question do not have an ATP generating membrane potential anymore, which seems unlikely to coexist with a phagocytotic capability [24]. Then there is the question of size and cost: a cell that, to all intents and purposes, is still an archaeon taking up a bacterium with a machinery that is beyond its energetic means in operation and maintenance (the advent of mitochondrial ATP generation will allow this to evolve later on).…”