Ancient Invasions: From Endosymbionts to Organelles

Dyall, Sabrina D.; Brown, Mark T.; Johnson, Patricia J.

doi:10.1126/science.1094884

Cited by 695 publications

(496 citation statements)

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“…The same holds true for the Omp85 of plastids. This proposal is in accordance with the classical endosymbiont theory (36,37). The common ancestry of plastidic and cyanobacterial Omp85s is also reflected by their physical properties.…”

Section: Relationship Between Prokaryotic and Eukaryotic Members Of Tsupporting

confidence: 73%

Functional and Phylogenetic Properties of the Pore-forming β-Barrel Transporters of the Omp85 Family

Bredemeier

Schlegel

Ertel

et al. 2007

Journal of Biological Chemistry

101

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␤-Barrel-shaped channels of the Omp85 family are involved in the translocation or assembly of proteins of bacterial, mitochondrial, and plastidic outer membranes. We have compared these proteins to understand the evolutionary development of the translocators. We have demonstrated that the proteins from proteobacteria and mitochondria have a pore diameter that is at least five times smaller than found for the Omp85 in cyanobacteria and plastids. This finding can explain why Omp85 from cyanobacteria (but not the homologous protein from proteobacteria) was remodeled to become the protein translocation pore after endosymbiosis. Further, the pore-forming region of the Omp85 proteins is restricted to the C terminus. Based on a phylogenetic analysis we have shown that the pore-forming domain displays a different evolutionary relationship than the N-terminal domain. In line with this, the affinity of the N-terminal domain to the C-terminal region of the Omp85 from plastids and cyanobacteria differs, even though the N-terminal domain is involved in gating of the pore in both groups. We have further shown that the N-terminal domain of nOmp85 takes part in homo-oligomerization. Thereby, the differences in the phylogeny of the two domains are explained by different functional constraints acting on the regions. The poreforming domain, however, is further divided into two functional regions, where the distal C terminus itself forms a dimeric pore. Based on functional and phylogenetic analysis, we suggest an evolutionary scenario that explains the origin of the contemporary translocon.Polypeptide transport and assembly of proteins into or across the outer membrane of endosymbiotic organelles or Gram-negative bacteria depend on ␤-barrel-shaped channels (1-4). One class of these proteins is composed of polypeptide-transporting ␤-barrel (PTB) 6 channels, whose topology was determined by modeling (5-7). PTBs of recent interest are, e.g. outer membrane proteins (which secrete adhesins such as hemagglutinin) (8, 9) and bacterial (1, 7, 10 -12), mitochondrial (Tob55/Sam50) (5, 13, 14), and chloroplast outer membrane proteins (Toc75) (15) of the Omp85 family. The PTBs are partitioned into two functional categories, namely in translocation of precursor proteins across the membrane and in the assembly of outer membrane proteins (3). Furthermore, comparison between chloroplastic, mitochondrial, and bacterial Omp85 protein sequences revealed a high similarity of these PTBs (14,16,17).The PTB Toc75 forms a complex with Toc34, Toc64, and Toc159 (3). A precursor protein-binding site at Toc75 (15, 18), together with the action of Toc159 (19), facilitates the translocation of precursor proteins across the membrane. In contrast, the Omp85 proteins from Neisseria meningitidis, Escherichia coli, and mitochondria are involved in the assembly of outer membrane proteins (1,5,7,(11)(12)(13)(14). As found for Toc75, the mitochondrial PTB is a component of a larger complex with Mas37 (20, 13) and Tob38/Sam35 (21,22).Recently, it was demonstrated that t...

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Section: Relationship Between Prokaryotic and Eukaryotic Members Of Tsupporting

confidence: 73%

Functional and Phylogenetic Properties of the Pore-forming β-Barrel Transporters of the Omp85 Family

Bredemeier

Schlegel

Ertel

et al. 2007

Journal of Biological Chemistry

101

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“…36, 37 Not surprisingly, the GatBs from Arapadopsis thalina and Oryza sativa clustered with the Cynanobacteria in agreement with the cynanobacterial origins of the organelle. 38 The Pet112 family forms a group with the α-Proteobacteria, with a specific relationship with the Rickettsia, this result indicates Pet112 is not a component of the nuclear line of decent but is of mitochondrial origin. 39,40 The function of Pet112, the mitochondrial GatB-like protein, in eukaryotes such as S. cerevisae is unresolved.…”

Section: Ancient Divergence Between Gatb and Gatementioning

confidence: 68%

On the Evolution of the tRNA-Dependent Amidotransferases, GatCAB and GatDE

Sheppard

Söll

2008

Journal of Molecular Biology

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SummaryGlutaminyl-tRNA synthetase and asparaginyl-tRNA synthetase evolved from glutamyl-tRNA synthetase and aspartyl-tRNA synthetase, respectively, after the split in the last universal communal ancestor (LUCA). Glutaminyl-tRNA Gln and asparaginyl-tRNA Asn were likely formed in LUCA by amidation of the mischarged species, glutamyl-tRNA Gln and aspartyl-tRNA Asn , by tRNA-dependent amidotransferases as is still the case in most bacteria and all known archaea. The amidotransferase GatCAB is found in both domains of life while the heterodimeric amidotransferase, GatDE, is found only in Archaea. The GatB and GatE subunits belong to a unique protein family with Pet112 that is encoded in the nuclear genomes of numerous eukaryotes. GatE was thought to have evolved from GatB after the emergence of the modern lines of decent. Our phylogenetic analysis though places the split between GatE and GatB prior to the phylogenetic divide between Bacteria and Archaea and Pet112 to be of mitochondrial origin. In addition, GatD appears to have emerged prior to the bacterialarchaeal phylogenetic divide. Thus, while GatDE is an archaeal signature protein it likely was present in LUCA together with GatCAB. Archaea retained both amidotransferases while Bacteria emerged with only GatCAB. The presence of GatDE has favored a unique archaeal tRNA Gln that may be preventing acquisition of glutaminyl-tRNA synthetase in Archaea. Archaeal GatCAB on the other hand has not favored a distinct tRNA Asn suggesting tRNA Asn recognition is not a major barrier to the retention of asparaginyl-tRNA synthetase in more Archaea.

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“…The mitochondrion is a eukaryotic organelle acquired through endosymbiosis of an α-proteobacterium by either an ancestral eukaryote (Dyall et al, 2004;Gray et al, 1999) or an archaeon (Martin and Muller, 1998). Subsequently the vast majority of genes encoding mitochondrial proteins were transferred from the mitochondrial genome to the nuclear genome, and the residual mitochondrial genome mainly encodes products involved in the synthesis of mitochondrial proteins (tRNA and rRNA) and some subunits of the oxidative phosphorylation complexes (Gabaldon and Huynen, 2005;Saccone et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

The mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae

et al. 2014

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The mitochondrion is an essential organelle for the production of cellular ATP in most eukaryotic cells. It is extensively studied, including in parasitic organisms such as trypanosomes, as a potential therapeutic target. Recently, numerous additional subunits of the respiratory-chain complexes have been described in Trypanosoma brucei and Trypanosoma cruzi. Since these subunits had apparently no counterparts in other organisms, they were interpreted as potentially associated with the parasitic trypanosome lifestyle. Here we used two complementary approaches to characterise the subunit composition of respiratory complexes in Euglena gracilis, a non-parasitic secondary green alga related to trypanosomes. First, we developed a phylogenetic pipeline aimed at mining sequence databases for identifying homologs to known respiratory-complex subunits with high confidence. Second, we used MS/MS proteomics after two-dimensional separation of the respiratory complexes by Blue Native-and SDS-PAGE to both confirm in silico predictions and to identify further additional subunits. Altogether, we identified 41 subunits that are restricted to E. gracilis, T. brucei and T. cruzi, along with 48 classical subunits described in other eukaryotes (i.e. plants, mammals and fungi). This moreover demonstrates that at least half of the subunits recently reported in T. brucei and T. cruzi are actually not specific to Trypanosomatidae, but extend at least to other Euglenozoa, and that their origin and function are thus not specifically associated with the parasitic lifestyle. Furthermore, preliminary biochemical analyses suggest that some of these additional subunits underlie the peculiarities of the respiratory chain observed in Euglenozoa.Liège, february 06 th 2014Dear Editor, Please find the fully revised version of our manuscript "The mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae."We are grateful to you for having encouraged us to resubmit a modified manuscript. We have addressed all the comments raised by the reviewers on our first submission. A point to point answer has been submitted along with the manuscript. Main changes are : (i) additional explanations about the phylogenic/bioinformatic strategy including some phylogenetic trees (supplemental figures 1 and 2); (ii) all data that were previously not shown (mass spectrometry data, in vivo respiratory assays) are now included in the manuscript as supplemental figures/tables.We hope that we have now significantly improved our manuscript so you'll find it suitable for publication in the special issue of Mitochondrion dedicated to "Plant Mitochondria Biology". R: Primary MS data are now given in Supplemental Table 3 for each polypeptide for which the score was > 60. (BLAST alignments, Evalues, etc.) are actually presented in the paper to support the inference that a particular E. gracilis protein is a true homolog of a given kinetoplastid protein. The most important conclusion of t...

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Ancient Invasions: From Endosymbionts to Organelles

Cited by 695 publications

References 48 publications

Functional and Phylogenetic Properties of the Pore-forming β-Barrel Transporters of the Omp85 Family

Functional and Phylogenetic Properties of the Pore-forming β-Barrel Transporters of the Omp85 Family

On the Evolution of the tRNA-Dependent Amidotransferases, GatCAB and GatDE

The mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae

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