Analysis of diverse eukaryotes suggests the existence of an ancestral mitochondrial apparatus derived from the bacterial type II secretion system

Abstract

Modern mitochondria have preserved few traits of the original bacterial endosymbiont. Unexpectedly, we find that certain representatives of heteroloboseans, jakobids and malawimonads possess homologues of four core components of the type 2 secretion system (T2SS) so far restricted to eubacteria. We show that these components are localized to the mitochondrion, and their behaviour in functional assays is consistent with the formation of a mitochondrial T2SS-derived protein secretion system. We additionally identified 23 protein families exactly co-occurring in eukaryotes with the T2SS. Seven of these proteins could be directly linked to the core T2SS by functional data and/or sequence features, whereas others may represent different parts of a broader functional pathway, possibly linking the mitochondrion with the peroxisome. Its distribution in eukaryotes and phylogenetic evidence indicate that the whole mitochondrial T2SS-centred pathway is an ancestral eukaryotic trait. Our findings thus have direct implications for the functional properties of the early mitochondrion.

The draft nuclear genome sequence and predicted mitochondrial proteome of Andalucia godoyi, a protist with the most gene-rich and bacteria-like mitochondrial genome

“…The second bacterial-type protein translocation pathway found in Andalucia is characterized in detail in a separate study [171]. Briefly, jakobids (including A. godoyi) and representatives of several other eukaryotic lineages (heteroloboseans, malawimonads, hemimastigophorans) possess homologs of the core components of the Type II Secretion System (T2SS) seemingly localized to the mitochondrial envelope.…”

“…In a similar fashion, Andalucia godoyi might be considered the eukaryote whose mitochondrion likely resembles the LECA mitochondrion more closely than does the mitochondrion in other eukaryotes studied to date, in that it retains a collection of ancestral bacterial features that have been lost or have a highly punctate distribution within eukaryotes. These features include (1) a bacterial-type GreA/GreB transcription elongation/transcript cleavage factor, complementing the bacterial-type mitochondrial RNAP, (2) RnpA, the protein component of bacterial RNase P, (3) a bacterial-type RecA, (4) an FtsZ-Min pathway, involved in cell division in bacteria [137], (5) a type 2 protein secretion system (T2SS) [171], (6) a complete twin-arginine translocation (TAT) pathway, (7) a Ccm cytochrome c biogenesis system, notably including the CcmD subunit, (8) bacterialtype tmRNA-SmpB, (9) a three-component aerobic-type rubrerythrin system, and (10) HslUV protease. An additional ancestral feature might be the bacterial-type Pol I mitochondrial DNAP that is unrelated to the common mitochondrial POP DNAP (Fig.…”

Eukaryotic cellular intricacies shape mitochondrial proteomic complexity

“…Moreover, several traits that could have been lost from the mitochondria of most eukaryotes are occasionally detected in the organelles of distantly related and understudied unicellular lineages, [81] such as the bacterial secretion system [82] and the signal recognition particle-based machinery. [83] The sporadic distribution in separate protist lineages might imply that they were indeed present in the LECA mitochondrion, although alternative explanations (e.g., later instances of horizontal gene transfer to unicellular recipients [16] ) also need to be considered.…”

Scaffolding protein GspB/OutB facilitates assembly of the Dickeya dadantii type 2 secretion system by anchoring the outer membrane secretin pore to the inner membrane and to the peptidoglycan cell wall

“…The secretins are also shared by the type 3 secretion system (T3SS), type 4 pili (T4P) as well as by the competence and the filamentous phage assembly systems (16)(17)(18)(19). Secretin homologs have also been identified in mitochondria of some eukaryotes (20). Recent cryo-EM structures have revealed important molecular details of the assembly of the MDa-sized secretin channels consisting of 12 to 16 subunits, with a clear predominance of 15-fold symmetry in more recent, near-atomic resolution structures of the T2SS and T3SS secretins (15,(21)(22)(23)(24)(25)(26)(27)(28).…”