I never – ever realized that bacteria don’t phagocytose! This is a serious eye-opener for me. Most readings of the endosymbiont theory I came across gloss over this. I’ll be a lot clearer about this the next time I write something about mitochondrial origins! The whole issue does raise interesting questions though (as you already mentioned!).. The problem of course is that since both phagocytosis and mitochondria are exclusive to eukaryote lineages, it is difficult to reconstruct what exactly happened in our ancestor.

There’s some work being done on dating the emergence of the actin/myosin remodeling system right? I know there’s nice work on the origins of membrane trafficking (see how I snuck in that self-reference ;) ?), what do you think of this? Could the PVC cluster be the bacterial phylum that eukaryotes are most closely related to? They do seem to share some remarkable characteristics with eukaryotes..

I definitely want to read some work by Cavalier-Smith now. I rarely come across papers that I can call insane, absurd and a masterpiece at the same time, so this should be a welcome change of pace. I guess it does take someone with a stroke of genius and the capability of integrating insights from a wide variety of fields to create some order in this mess! I’m still working my way through the recent issue of Phil Transactions R Soc though..

Again thanks for bringing this up!

Now, I do have a couple comments about the intro though.

This is a story about an event that took place 2 billion years ago.

Maybe it’s better to write 1-2 billion years? The fossil data for early eukaryotic origin is quite rather weak (Cavalier-Smith 2006 Phil Trans R Soc B; Cavalier-Smith 2006 Biol Direct); and from phylogeny it makes a lot more sense for archaeans and eukaryotes to be fairly recent clades (although all the preceding divergences (cyanobacteria, glycobacteria, posibacteria (‘gram positives’, and the ‘gracilicutes’, including the fairly late-diverging proteobacteria necessary for our eukaryogenesis), etc) could have exploded ultra rapidly in a very short period of time, but then why the relative stagnation in the eukaryote clade after its emergence?).

But even if we don’t subscribe to the eubacterial root (which is the only one that makes any modicum of sense, IMNSHO), instead going by the root being between eubacteria and archaea+eukarya, then the proto-eukaryote that swallowed the proteobacterium would’ve either been a proto-archaeon or an actual archaeon (if archaea are paraphyletic to eukaryotes, which would be awkward as multiple origins or origin and subsequent loss of the strange archaeal membrane lipids would be required). Now, I use bacteria=prokaryotes, but most microbiologists would twitch uncontrollably upon seeing that. So proto-bacteria wouldn’t be a good choice of words, perhaps.

(now, the root between eubacteria and eukaryotes+archaea would allow early origins for the latter, but makes very little sense from a cell biological perspective (eg. Cavalier-Smith 2006))

But this leads us to bigger problems:

Life was well underway at the time, with proto-bacteria already populating the oceans for over hundreds of millions of years. One of the cells alive at the time, swallowed an alpha-proteobacterium.

Bacteria cannot phagocytose. There is one weird case, Bdellvibrio, which manages to get inside what appears to be the space between the outer and inner membranes (http://www.nature.com/nrmicro/journal/v2/n8/fig_tab/nrmicro959_F1.html). This often used as ‘proof’ that bacteria are full of cryptic endosymbiotic events (or that “eukaryote = eubacterium eats archaeon” anyway…), but note that it doesn’t penetrate the inner membrane. The outer one is weird and porous and not quite the same thing as THE cytoplasmic membrane (inner membrane in double-membraned eubacteria, most likely homologous in all bacteria), so this is NOT a case of [involuntary] phagocytosis!

AFAIK, no archaeon can do phagocytosis either. Thus, a proto-bacterium or proto-archaeon could not have engulfed an endosymbiont. The thing that did was already fairly diverged from its bacterial brethren; probably with a fairly developed actin cytoskeleton and a membrane trafficking system (Cavalier-Smith 2008 Int J Biochem Cell Biol). Thus, it was by definition a proto-eukaryote. This may seem pedantic, but I think it’s important to note that the creature that endosymbiosed the alpha-proteobacterium was already quite weird.

It is rather strange that no primarily amitochondriate eukaryotes have been found [yet?]. This would imply that the changes associated with gaining the ability to phagocytose and the subsequent ‘enslavement’ of the mitochondrion happened mind-numbingly quickly; and/or that the mitochondrion gave SUCH an advantage to its host that they completely wiped out (by competition) all relatives without one. Probably a bit of both.

Oh, and I’d love to cite someone besides Cavalier-Smith (and read papers that are NOT 80 pages of DENSE on CRACK…), but he’s about the only one out there who can actually integrate cell biology, phylogeny, molecular genetics, genomics, paleogeology, climate, ecology, etc. into one comprehensive synthesis that actually makes some sort of coherent sense. Everyone else seems overly obsessed with endosymbiosis (eg. JA Lake, who also fails membrane topology 101 in his 2009 Nature hypothesis piece) or LGT and this bizarre attitude of hopelessness to the whole question of the early history of life.

Cavalier-Smith’s hypotheses are a brilliant mix of the insane, the rigorous, the factual and the utterly absurd into one integrated masterpiece encompassing as many fields as humanly (almost superhumanly, even) possible. It would be great if some bacteriologists followed along and tested + modified his theories as needed, rather than simply dismissing them…

[apologies for long comment! I just finished reading all 56 long pages of Cavalier-Smith 2006 Biol Direct, and bacteria are clogging my mind right now...]

I really like your explanation of gene loss! Right now I’m wishing that my curriculum included a course on endosymbiont evolution ;).

I’d love to see your post on chloroplast import! Be sure to let me know when it’s done, so I can place a link in this article.

In terms of this question: “Or maybe it was the evolution of protein import machinery that drove the loss of genes in the first place?” Definitely that way around. You need the import machinery before you can loose the genes, otherwise the symbiont would just die. Gene transfer is a ratchet system, genes only go from chloroplast to nucleus (usually by chloroplasts lysing and bits of their genes getting stuck in the nucleus) and once they are in the nucleus they stay there. Protein import systems make the gene in the chloroplast mostly redundant (and it’s safer in the nucleus anyway) so it gets lost.

I am very tempted to write a sister post for this, about chloroplast import mechanisms. Would you mind?