Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium

Abstract

Mitochondria originated by permanent enslavement of purple non-sulphur bacteria. These endosymbionts became organelles through the origin of complex protein-import machinery and insertion into their inner membranes of protein carriers for extracting energy for the host. A chicken-and-egg problem exists: selective advantages for evolving import machinery were absent until inner membrane carriers were present, but this very machinery is now required for carrier insertion. I argue here that this problem was probably circumvented by conversion of the symbiont protein-export machinery into protein-import machinery, in three phases. I suggest that the first carrier entered the periplasmic space via pre-existing beta-barrel proteins in the bacterial outer membrane that later became Tom40, and inserted into the inner membrane probably helped by a pre-existing inner membrane protein, thereby immediately providing the protoeukaryote host with photosynthesate. This would have created a powerful selective advantage for evolving more efficient carrier import by inserting Tom70 receptors. Massive gene transfer to the nucleus inevitably occurred by mutation pressure. Finally, pressure from harmful, non-selected gene transfer to the nucleus probably caused evolution of the presequence mechanism, and photosynthesis was lost.

Figure 1

Origin of mitochondria by permanent internal cell enslavement. (a) Phagocytosis of a photosynthetic purple non-sulphur bacterium (α-proteobacterium) placed it inside the cytoplasm of a protoeukaryote host. Though shown with a cilium, cytoskeleton, endomembrane system, nucleus and peroxisomes, these organelles were probably still actively coevolving in this stem eukaryote, only acquiring their full complement of modern properties during conversion of the purple bacterium into a mitochondrion. (b) The phagosomal membrane failed to fuse with lysosomes, was broken and lost, allowing the purple bacterium to multiply freely in the cytosol of the host that was able to use any photosynthesate leaking from it. Pre-existing outer membrane (OM: blue) proteins, e.g. porins (yellow), allowed host carrier proteins (green: probably arising by gene duplication of a peroxisomal carrier) to enter the bacterial periplasmic space and spontaneously insert into its inner membrane (IM: purple). By extracting photosynthesate for itself, and providing the bacterium with CO₂ and minerals, e.g. phosphate, sulphate, the phagotrophic host established a mutualistic endosymbiosis. A pre-existing OM protein evolved into the core protein (Tom40) of the protein translocator of the premitochondrial OM (TOM), allowing numerous other proteins to be inserted to improve small molecule exchanges across its envelope. (c) Following transfer of duplicates of much of the protomitochondrial genome (grey) to the nucleus and integrating them into nuclear DNA, Tim23 IM translocons and OM presequence receptors evolved to retarget many proteins coded by them back into the protomitochondrion, where they would be beneficial, not harmful or wasted. Loss of such genes and others essential for free-living life (Boussau et al. 2004) from the mitochondrial genome permanently enslaved the mitochondrion. Its peptidoglycan murein and genes needed for photosynthesis, but not respiration, were lost during this major streamlining and efficiency increase prior to the last common ancestor (cenancestor) of all eukaryotes.

Figure 2

Origin of the mitochondrial protein-import systems (d) from the ancestral α-proteobacterial protein-export systems (a) The outer membrane (OM) β-barrel proteins (Sam50, Tom40, porins) all evolved directly from symbiont OM proteins and Oxa1/2 evolved from the inner membrane (IM) protein YidC. (b) Enslavement was initiated by the insertion of novel carrier proteins able to enter through Tom40 with the help of pre-existing host and periplasmic chaperone proteins and insert into the IM. The first carrier, possibly descended from the peroxisomal ATP importer, exported ATP or photosynthesate to the host and generated over 30 other carriers by gene duplication. Their import was made efficient by evolution of receptor Tom70, possibly of cyanobacterial origin by lateral gene transfer, inserting by its N-terminal membrane-spanning α-helix, and Tim22 entering via the Tom40 pore (c) Following massive transfer of genes from symbiont to nucleus, the presequence mechanism evolved by gene duplication of Tim22 to Tim23 and Tim17 to generate the inner membrane translocase and the addition of Tom20 and Tom22 to recognize the hydrophobic and positively charged parts, respectively, of the presequences, of Tim44 to transfer the symbiont/matrix chaperone Hsp70 more efficiently onto the emerging preproteins and a matrix peptidase to remove their presequences. Pre-existing periplasmic chaperones diversified and adapted to prevent periplasmic aggregation and improve transfer between membrane–protein complexes, and various less key proteins were added to each to increase stability and improve transfer rates and efficiency. Sec machinery was retained by the excavate jakobid protozoa (Gray et al. 2004), but lost by other mitochondria. Acquisition of presequences by approximately 1000 proteobacterial genes transferred to the nucleus (Esser et al. 2004; greater similarity of many of these to γ- not α-proteobacteria may be an artefact stemming from major divergence during mitochondriogenesis) allowed loss of their symbiont versions and huge mitochondrial genome reduction, raising efficiency by increasing space for matrix enzymes and sparing nutrients and energy previously wasted on multiple copies of their DNA. IMP; inner membrane proteins other than carriers and translocons.