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The Pre-Endosymbiont Hypothesis: a New Perspective on the Origin and Evolution of Mitochondria

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The Pre-Endosymbiont Hypothesis: a New Perspective on the Origin and Evolution of Mitochondria Downloaded from http://cshperspectives.cshlp.org/ on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press The Pre-Endosymbiont Hypothesis: A New Perspective on the Origin and Evolution of Mitochondria Michael W. Gray Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia B3M 4R2, Canada Correspondence: [email protected] Mitochondrial DNA (mtDNA) is unquestionably the remnant of an a-proteobacterial ge- nome, yet only 10%–20% of mitochondrial proteins are demonstrably a-proteobacterial in origin (the “a-proteobacterial component,” or APC). The evolutionary ancestry of the non- a-proteobacterial component (NPC) is obscure and not adequately accounted for in current models of mitochondrial origin. I propose that in the host cell that accommodated an a- proteobacterial endosymbiont, much of the NPC was already present, in the form of a membrane-bound metabolic organelle (the premitochondrion) that compartmentalized many of the non-energy-generating functions of the contemporary mitochondrion. I suggest that this organelle also possessed a protein import system and various ion and small-molecule transporters. In such a scenario, an a-proteobacterial endosymbiont could have been converted relatively directly and rapidly into an energy-generating organelle that incorporated the extant metabolic functions of the premitochondrion. This model (the “pre- endosymbiont hypothesis”) effectively represents a synthesis of previous, contending mito- chondrial origin hypotheses, with the bulk of the mitochondrial proteome (much of the NPC) having an endogenous origin and the minority component (the APC) having a xenogenous origin. onsidering the central role played in all eu- evolution, focusing particularly on how well the Ckaryotic cells by mitochondria or mito- accumulating molecular data can be accommo- chondrion-related organelles (MROs, such as dated in current models of mitochondrial ori- hydrogenosomes and mitosomes) (Hjort et al. gin. In this context, the origin and evolution of 2010; Shiflett and Johnson 2010; Mu¨ller et al. the mitochondrial proteome, as opposed to the 2012), the question of the origin and subse- origin and evolution of the mitochondrial ge- quent evolution of the mitochondrion has nome, were examined from the perspective of long captivated and challenged biologists. In a comparative mitochondrial proteomics. Some- recent article in this series (Gray 2012), I dis- what disconcertingly, as more data have become cussed in detail several aspects of mitochondrial available, we find ourselves considerably less Editors: Patrick J. Keeling and Eugene V. Koonin Additional Perspectives on The Origin and Evolution of Eukaryotes available at www.cshperspectives.org Copyright # 2014 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a016097 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016097 1 Downloaded from http://cshperspectives.cshlp.org/ on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press M.W. Gray certain about key aspects of how mitochondria † We know that the most bacteria-like (least- originated than we were (or thought we were) derived) and gene-rich mitochondrial ge- several decades ago. nomes are found within the core jakobids Here, I summarize key points discussed in (Fig. 1) (Lang et al. 1997; Burger et al. more detail in the previous article before pre- 2013), a group of flagellated protozoa that senting a novel perspective on how the mito- are members of the proposed eukaryotic chondrion might have originated. The new supergroup Excavata (Hampl et al. 2009). model proposed here, which represents a syn- Jakobid mtDNAs specify strikingly bacteria- thesis of both endogenous (“origin from with- like large subunit (LSU), small subunit (SSU) in”) and xenogenous (“origin from outside”) and 5S ribosomal RNAs (rRNAs) and trans- modes, is advanced in an attempt to account fer RNAs (tRNAs), as well as upward of 70 0 for the inability of a purelyendosymbiotic mod- proteins, including subunits of an a2bb s el, whose strongest support has come from RNA polymerase, the enzyme used for tran- studies of the mitochondrial genome, to ade- scription in Bacteria. Other notable features quately accommodate data on the mitochondri- include genes encoding transfer-messenger al proteome. RNA (tmRNA) and the RNA component of RNase P; bacteria-like operon organization; and putative Shine–Dalgarno-like motifs in- A RUMSFELDIAN TAKE ON THE ORIGIN volved in translation initiation in Bacteria. OF THE MITOCHONDRION † We know that certain components of the ... there are known knowns; there are things we original, bacteria-like systems used for repli- know we know. cation and transcription of mtDNA (e.g., the We also know there are known unknowns; that is to mitochondrial RNA polymerase) have been say, we know there are some things we do not know. replaced in some or virtually all eukaryotes But there are also unknown unknowns—the ones we by bacteriophage-like counterparts (Shutt don’t know we don’t know. and Gray 2006). —U.S. Secretary of Defense Donald Rumsfeld † We know that mitochondrial genome evolu- Press briefing, February 12, 2002 tion has been characterized by extensive gene This Rumsfeldian view provides a useful loss, with relocation of many of the genes in framework for outlining key aspects of what the protomitochondrial genome to the nu- we know and what we don’t know about the cleus and import of their protein products origin and evolution of the mitochondrion. back into the organelle. Such endosymbiotic gene transfer (EGT) usually involves com- plete genes, but EGT may also relocate only Known Knowns a portion of a mtDNA-encoded gene, with the rest of that gene remaining in and ex- † We know from comparative mitochondrial pressed from the mitochondrial genome genomics—through the analysis of genes (Burger et al. 2003). contained in mtDNA and the protein se- quences they specify—that the mitochondri- † We know that the mitochondrion originated al genome is of (eu)bacterial origin. These only once, that is, mitochondria in all eu- sequences point us to members of a particu- karyotic lineages descend from a common lar bacterial phylum, a-proteobacteria (also ancestor, the LMCA (last mitochondrial termed Alphaproteobacteria), as the closest common ancestor). Commonality in key as- extant free-living relatives of mitochondria, pects of genetic and biochemical function, and therefore the bacterial group from within the presence of shared mitochondrion-spe- which the mitochondrial genome emerged cific deletions in bacteria-like operons pre- (Gray and Doolittle 1982; Gray 1992). sent in some mtDNAs, and phylogenetic 2 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016097 Downloaded from http://cshperspectives.cshlp.org/ on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press The Pre-Endosymbiont Hypothesis rpl31 rns rrn5 rnl rpl34 rps1 rpl27 atp8 orf97 atp4 nad7 nad9 cob orf35 nad10 atp1 nad3 C atp3 rpl20 L rpl35 E P rpl11 rpl1 sdh3 I Me sdh4 K W rpl10 sdh2 S nad4L nad5 nad4 65 67/0 5 rpoB nad2 60 kbp rps2 R 10 VD ssrA FA 55 Andalucia orf240 godoyi 15 orf203 rpoC orf123 50 rps12 mtDNA orf146 20 rps7 ccmF 67,656 bp ccmC 45 nad11 ccmB 25 nad1 ccmA I G 40 cox11 RQ 30 rpl32 35 cox3 atp6 N tufA tatA rps10 cox2 S rp12 nad6 H nad8 T L Y rps19 cox1 Mf V G rps3 S rpoD L rpl16 cox15 rpl14 tatC rpl5 atp9 rpl19 rps14 rps4 rps8 rnpB rpl6 rpoA rpl18 rps11 rpl13 Figure 1. Genetic map of the strikingly bacteria-like mitochondrial genome of the core jakobid, Andalucia godoyi: the most gene-rich mitochondrial genome known (Burger et al. 2013). (Solid rectangles) Genes, with those on the outer circle transcribed in a clockwise direction, and those on the inner circle transcribed coun- terclockwise. Colors denote taxonomic gene distribution: (black) common genes found in most animal, fungal, and protist mtDNAs; (blue) expanded gene set, mostly present in protist and plant mtDNAs; (red) genes predominantly found in jakobid mtDNAs; (green) hypothetical protein-coding genes (ORFs). A. godoyi mtDNA encodes 25 proteins involved in coupled electron transport–oxidative phosphorylation (nad, sdh, cob, cox, atp; complexes I–V, respectively); 12 SSU (rps) and 16 LSU (rpl) ribosomal proteins; one translation elongation factor (tuf ); four subunits of a bacteria-like multisubunit RNA polymerase (rpoA,B,C,D); eight proteins involved in protein import (ccmA,B,C; tatA,C) and protein maturation (cox11,15; ccmF); LSU (rnl), SSU (rns), and 5S (rrn5) rRNAs; 25 tRNAs—single uppercase letters: (Mf ) initiator methionine; (Me) elongator methionine; transfer-messenger RNA (tmRNA) (ssrA); and the RNA component of RNase P (rnpB). Five additional open reading frames (orf ) encode putative proteins of unknown function. (Arrows) Positions of predicted promoters. (Figure courtesy of G. Burger.) Cite this article as Cold Spring Harb Perspect Biol 2014;6:a016097 3 Downloaded from http://cshperspectives.cshlp.org/ on September 25, 2021 - Published by Cold Spring Harbor Laboratory Press M.W. Gray tree reconstruction strongly support this in- such as Rickettsia, Anaplasma, and Ehrli- ference (Gray et al. 1999). chia—asthe closestrelativesof mitochondria. Rickettsiales comprises two distinct families, † We know that despite an evident a-proteo- Rickettsiaceae and Anaplasmataceae, with bacterial origin of the mitochondrial ge- several studies suggesting that mitochondria nome, only 10%–20% of the mitochon- are more closely related to the former family, drial proteome—the collection of proteins containing various Rickettsia species, than to making up the organelle—can confidently thelatter,whichencompassesthegeneraAna- be traced to a-proteobacteria (this a-proteo- plasma, Ehrlichia, and Wolbachia. However, bacterial component is referred to here as the there is currently no consensus in the litera- APC). The 80%–90% non-a-proteobacte- ture astowhether mitochondria branchwith- rial component, or NPC, appears from phy- in or as sister to either of the two Rickettsiales logenetic analysis either to be of diverse pro- families,oroutsideofRickettsialesaltogether.
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