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Mosaic Nature of the Mitochondrial Proteome: COLLOQUIUM Implications for the Origin and Evolution of Mitochondria

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Mosaic Nature of the Mitochondrial Proteome: COLLOQUIUM Implications for the Origin and Evolution of Mitochondria PAPER Mosaic nature of the mitochondrial proteome: COLLOQUIUM Implications for the origin and evolution of mitochondria Michael W. Gray1 Department of Biochemistry and Molecular Biology and Centre for Comparative Genomics and Evolutionary Bioinformatics, Dalhousie University, Halifax, NS, Canada B3H 4R2 Edited by Patrick J. Keeling, University of British Columbia, Vancouver, BC, Canada, and accepted by the Editorial Board March 11, 2015 (received for review December 23, 2014) Comparative studies of the mitochondrial proteome have identi- during mitochondrial evolution. This essay briefly highlights the fied a conserved core of proteins descended from the α-proteo- results of studies that revealed the mosaic nature of the mito- bacterial endosymbiont that gave rise to the mitochondrion and chondrial proteome and discusses the implications of that obser- was the source of the mitochondrial genome in contemporary vation for models of mitochondrial origin and evolution. eukaryotes. A surprising result of phylogenetic analyses is the rel- atively small proportion (10–20%) of the mitochondrial proteome Proteins Encoded by Mitochondrial DNA displaying a clear α-proteobacterial ancestry. A large fraction of The mitochondrial genome specifies a miniscule but essential mitochondrial proteins typically has detectable homologs only in portion of the mitochondrial proteome, ranging from a low of 3 other eukaryotes and is presumed to represent proteins that proteins of defined function in apicomplexans such as Plasmo- emerged specifically within eukaryotes. A further significant frac- dium to a high of 66 in the excavate Andalucia godoyi, a member tion of the mitochondrial proteome consists of proteins with ho- of the core jakobids. The latter assemblage of protists contains mologs in prokaryotes, but without a robust phylogenetic signal the most ancestral (bacteria-like) mitochondrial genomes known affiliating them with specific prokaryotic lineages. The presump- (22, 23), with mitochondrial-gene content varying only slightly EVOLUTION tive evolutionary source of these proteins is quite different in con- within the group. Among them, jakobid mtDNAs encode 67 pro- tending models of mitochondrial origin. teins: 25 components of the mitochondrial respiratory chain, 29 translation proteins (mostly ribosomal proteins), 9 proteins involved mitochondria | proteome | endosymbiont | phagotrophy | syntrophy in protein import and maturation, and 4 proteins constituting a multisubunit bacteria-like α2ββ′σ RNA polymerase. Mitochondrial- nderstanding the origin and evolution of the mitochon- gene content, although extremely variable among eukaryotes, is Udrion remains a challenge, despite the flood of relevant bio- largely a subset of that in the core jakobids (15), whose mitochon- chemical, cell and molecular biological, and phylogenetic data drial genomes lack only genes for small subunit ribosomal protein and insights that have accumulated in the almost five decades S16 (rps16), recently identified in the mtDNAs of Acanthamoeba since the modern resurrection (1, 2) of the long-standing endo- castellanii and Vermamoeba vermiformis (6, 24) and large subunit symbiont hypothesis: the idea that this organelle is a tamed and ribosomal protein L36 (rpl36), annotated in the mtDNA sequence highly reworked endosymbiotic bacterium. The abundance of of Malawimonas jakobiformis (www.ncbi.nlm.nih.gov/gene?cmd= information bearing on eukaryotic cell evolution (particularly Retrieve&dopt=full_report&list_uids=2695583). On that basis, and most recently sequence data) and differences over how the we can infer that the mitochondrial genome of the last eukaryotic data are analyzed and interpreted have prompted a plethora of common ancestor (LECA) encoded a minimum of ∼70 proteins often-conflicting ideas about when and how, within an endosymbi- (6, 23). In extant eukaryotes, the role of the mitochondrial genome otic context, the mitochondrion originated (3, 4). Considering the is a highly circumscribed and critical one: It supports the trans- spate of recent papers dealing with various aspects of mitochondrial lation and maturation of a small number of proteins that are origin and evolution either explicitly (e.g., refs. 5–10)oraspartofa components of complexes I to IV (CI–CIV) of the electron broader view of eukaryotic cell evolution (e.g., refs. 11–14), interest transport chain (ETC) as well as complex V (CV; ATP synthase). in this subject is unlikely to wane any time soon. These mtDNA-encoded proteins are assembled with nucleus- That the mitochondrial genome is of bacterial (specifically encoded partner proteins to generate a functional respiratory α-proteobacterial) origin is now indisputable (15, 16), and that fact chain capable of carrying out coupled electron transport–oxidative has underpinned the current wide acceptance of a xenogenous/ phosphorylation. exogenous (endosymbiotic) origin of the mitochondrion (17, 18), effectively vanquishing autogenous/endogenous (nonsymbiotic) Composition of the Mitochondrial Proteome origin hypotheses (e.g., refs. 19–21). However, the mitochondrial The basic approach to identifying bona fide mitochondrial pro- proteome, most of which is nucleus-encoded, tells another, teins currently comprises a combination of direct subcellular murkier story. It was expected that many mitochondrial proteins would not have obvious bacterial homologs because they would have emerged specifically within eukaryotes, as part of the This paper results from the Arthur M. Sackler Colloquium of the National Academy of endosymbiont-to-organelle retailoring process. What was not Sciences, “Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of Organelles,” held October 15–17, 2014, at the Arnold and Mabel Beckman Center of the anticipated was how relatively few mitochondrial proteins with National Academies of Sciences and Engineering in Irvine, CA. The complete program bacterial homologs would group specifically with α-Proteobac- and video recordings of most presentations are available on the NAS website at www. teria in phylogenetic reconstructions: At most, only 10–20% of nasonline.org/Symbioses. any of the mitochondrial proteomes examined so far display a Author contributions: M.W.G. wrote the paper. robust α-proteobacterial signal. This minority group includes The author declares no conflict of interest. proteins encoded by the mitochondrial genome as well as nucleus- This article is a PNAS Direct Submission. P.J.K. is a Guest Editor invited by the Editorial encoded mitochondrial proteins whose genes we infer were Board. transferred to the nucleus via endosymbiotic gene transfer (EGT) 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1421379112 PNAS | August 18, 2015 | vol. 112 | no. 33 | 10133–10138 Downloaded by guest on September 27, 2021 proteomics techniques [tandem mass spectrometry (MS/MS) was essentially complete before divergence of the main eukary- applied to purified mitochondria or submitochondrial fractions] otic supergroups, with novel nucleus-encoded subunits in place in combination with indirect bioinformatics-based prediction of and many of the original endosymbiont-encoded ribosomal proteins exhibiting N-terminal mitochondrial targeting se- protein genes having already undergone EGT to the nucleus. quences (25–27). The two techniques have their complementary Subsequent evolution involved additional mitochondrion- strengths and limitations, with MS/MS capable of revealing novel to-nucleus gene relocation, as well as lineage-specific gains and mitochondrial proteins (ones having no known homologs) but losses (41, 42). The most extreme examples of mitoribosome often missing low-abundance proteins that may be identified by retailoring are seen in the kinetoplastid protists, Trypanosoma in silico analyses, which, however, fail to retrieve mitochondrial brucei (43) and Leishmania tarentole (44). In T. brucei, the ri- proteins that lack well-defined N-terminal mitochondrial tar- bosomal SSU and LSU contain 56 and 77 proteins, compared geting signals. Delineation of the mitochondrial proteome in any with 21 and 34, respectively, in a bacterial (e.g., Escherichia coli) organism requires a list of cellular proteins predicted from ribosome, with the novel mitochondrial proteins displaying very complete nuclear and mitochondrial genome sequences, as well limited sequence similarity with their counterparts within as assessment of possible nonmitochondrial contamination. Kinetoplastidae and no detectable similarity outside this lineage. Given these requirements and constraints, it is hardly surprising These focused studies highlight the dynamics of mitochondrial- that a relatively small number of largely complete and robustly proteome evolution, as well as emphasizing the importance of validated mitochondrial proteomes have been determined to direct MS/MS analysis in revealing novel mitochondrial proteins date, primarily from multicellular animals (notably human and that cannot be identified through sequence comparisons. mouse), fungi (e.g., the yeast Saccharomyces cerevisiae), and As the database for mitochondrial-proteome comparisons has plants (e.g., Arabidopsis thaliana, rice). Although eukaryotic expanded, it has become apparent that the LMCA was already as microbes (protists) constitute most of the evolutionary diversity complex in its key functions as modern mitochondria; impor- within the eukaryotic domain, comprehensive proteomic analy- tantly, for example, it possessed an essentially complete protein-
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