colloquium paper an ancestral bacterial division system is ... · pdf...

Click here to load reader

Post on 05-Jun-2019

212 views

Category:

Documents

0 download

Embed Size (px)

TRANSCRIPT

An ancestral bacterial division system is widespreadin eukaryotic mitochondriaMichelle M. Legera, Markta Petrub, Vojtech rskb, Laura Emea, Cestmr Vlcekc, Tommy Hardinga, B. Franz Langd,Marek Elie, Pavel Dolezalb, and Andrew J. Rogera,1

aCentre for Comparative Genomics and Evolutionary Bioinformatics (CGEB), Department of Biochemistry and Molecular Biology, Dalhousie University,Halifax, NS, Canada, B3H 4R2; bBiotechnology and Biomedicine Centre of the Academy of Sciences and Charles University in Vestec (BIOCEV) Group,Department of Parasitology, Faculty of Science, Charles University in Prague, 128 44 Prague, Czech Republic; cLaboratory of Genomics and Bioinformatics,Institute of Molecular Genetics, Academy of Sciences of the Czech Republic, 142 20 Prague 4, Czech Republic; dRobert Cedergren Centre for Bioinformaticsand Genomics, Dpartement de Biochimie, Universit de Montral, Montreal, QC, Canada, H3T 1J4; and eDepartment of Biology and Ecology, Faculty ofScience, University of Ostrava, 710 00 Ostrava, Czech Republic

Edited by Patrick J. Keeling, University of British Columbia, Vancouver, BC, Canada, and accepted by the Editorial Board February 24, 2015 (received for reviewJanuary 14, 2015)

Bacterial division initiates at the site of a contractile Z-ring com-posed of polymerized FtsZ. The location of the Z-ring in the cellis controlled by a system of three mutually antagonistic proteins,MinC, MinD, and MinE. Plastid division is also known to bedependent on homologs of these proteins, derived from theancestral cyanobacterial endosymbiont that gave rise to plastids.In contrast, the mitochondria of model systems such as Saccharo-myces cerevisiae, mammals, and Arabidopsis thaliana seem tohave replaced the ancestral -proteobacterial Min-based divisionmachinery with host-derived dynamin-related proteins that formouter contractile rings. Here, we show that the mitochondrial di-vision system of these model organisms is the exception, ratherthan the rule, for eukaryotes. We describe endosymbiont-derived,bacterial-like division systems comprising FtsZ and Min proteins indiverse less-studied eukaryote protistan lineages, including jako-bid and heterolobosean excavates, a malawimonad, strameno-piles, amoebozoans, a breviate, and an apusomonad. For two ofthese taxa, the amoebozoan Dictyostelium purpureum and thejakobid Andalucia incarcerata, we confirm a mitochondrial locali-zation of these proteins by their heterologous expression in Sac-charomyces cerevisiae. The discovery of a proteobacterial-likedivision system in mitochondria of diverse eukaryotic lineagessuggests that it was the ancestral feature of all eukaryotic mito-chondria and has been supplanted by a host-derived system mul-tiple times in distinct eukaryote lineages.

mitochondria | mitochondrial division | Min proteins | MinCDE |mitochondrial fission

During bacterial division, septum formation is mediated bythe Z-ring, a contractile ring structure made up of the po-lymerized tubulin homolog FtsZ (reviewed in refs. 1 and 2). Thesite at which FtsZ polymerizes is determined by the Min system(reviewed in refs. 1 and 35), comprising the three septum site-determining proteins MinC, MinD, and MinE. ATP-bound,dimerized MinD binds the inner cell membrane at the poles ofthe cell, forming aggregates. These MinD aggregates bind andactivate dimerized MinC (6), which then inhibits local FtsZ po-lymerization (Fig. 1A). Concomitantly, dimerized MinE formsa spiral ring whose constant polymerization and depolymerizationcauses it to oscillate across the cell (7, 8). Where MinE comesinto contact with MinD, it causes the release of ATP and thesubsequent liberation of MinD from the membrane (9, 10). Inthis way, MinD and MinC cannot inhibit FtsZ polymerizationnear the midpoint of the cell. The polymerizing Z-ring is stabi-lized and tethered to the membrane by FtsA, ZipA, and thenonessential ZapA and (in some organisms) ZapB (1115).Maturation of the Z-ring into a complete septal ring continueswith the subsequent recruitment by FtsA of further componentsof the divisome (i.e., FtsB, FtsE, FtsI/PBP3, FtsK, FtsL, FtsN,FtsQ, FtsW, and FtsX), which proceed to stabilize FtsZ and

contribute to peptidoglycan synthesis (reviewed in refs. 3, 4, 16and 17) (Fig. 1B) before Z-ring constriction and the completionof septum formation (Fig. 1C).Plastids are known to possess FtsZ (1820), MinD (21, 22),

MinE (21, 23), and, in some cases, MinC (24) homologs ofcyanobacterial endosymbiotic origin; in some cases, the latter areencoded on the plastid genome (21, 25). In contrast, only twoexamples of putative mitochondrial Min proteins have beenreported, in the stramenopiles Nannochloropsis oceanica andEctocarpus siliculosus (26). Indeed, although eukaryotic mito-chondria are derived from an -proteobacterial endosymbiont,the ancestral bacterial division machinery has been partly orwholly replaced by eukaryote-specific proteins in model systemeukaryotes where mitochondrial division has been studied.Whereas Amoebozoa (27), stramenopiles (28, 29), and the redalga Cyanidioschyzon merolae (30, 31) have retained experi-mentally confirmed mitochondrial FtsZ, animals and fungi(opisthokonts) and plants examined to date lack this protein. Inthe latter taxa, an outer contractile ring is instead formed byDnm1p/Drp1, a eukaryote-specific dynamin GTPase (3234).This protein is implicated in mitochondrial division in organismsacross the eukaryotic tree, including Arabidopsis thaliana (3537), the parabasalid Trichomonas vaginalis (38), Dictyosteliumdiscoideum (39), and C. merolae (40), suggesting that the outercontractile ring is a widespread eukaryotic feature. In T. vaginalisand A. thaliana, the nature of the inner contractile ring is not yetunderstood, although the presence of two Dnm1/Drp1 homologsin A. thaliana (37) raises the possibility that they form an outer andan inner contractile ring, respectively. Recent work (41) recon-structing the evolution of eukaryotic dynamins suggests that theancestral mitochondrial dynamin was a bifunctional protein thatalso mediated vesicle scission. This protein underwent duplica-tion events, followed by subfunctionalization, independently in at

This paper results from the Arthur M. Sackler Colloquium of the National Academy ofSciences, Symbioses Becoming Permanent: The Origins and Evolutionary Trajectoriesof Organelles, held October 1517, 2014, at the Arnold and Mabel Beckman Center ofthe National Academies of Sciences and Engineering in Irvine, CA. The complete programand video recordings of most presentations are available on the NAS website at www.nasonline.org/Symbioses.

Author contributions: M.M.L., M.P., and P.D. designed research; M.M.L., M.P., C.V., andT.H. performed research; B.F.L. contributed new reagents/analytic tools; M.M.L., M.P.,V.., L.E., C.V., and M.E. analyzed data; and M.M.L., M.P., T.H., and A.J.R. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission. P.J.K. is a guest editor invited by the EditorialBoard.

Data deposition: The sequences reported in this paper have been deposited in the GenBankdatabase (accession nos. KP271960KP271964, KP324909KP324912, KP258196KP258204,and KP738110).1To whom correspondence should be addressed. Email: [email protected]

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1421392112/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1421392112 PNAS Early Edition | 1 of 8

CELL

BIOLO

GY

COLLOQUIUM

PAPE

R

http://crossmark.crossref.org/dialog/?doi=10.1073/pnas.1421392112&domain=pdf&date_stamp=2015-03-20http://www.nasonline.org/Symbioseshttp://www.nasonline.org/Symbioseshttp://www.ncbi.nlm.nih.gov/nuccore/KP271960http://www.ncbi.nlm.nih.gov/nuccore/KP271964http://www.ncbi.nlm.nih.gov/nuccore/KP324909http://www.ncbi.nlm.nih.gov/nuccore/KP324912http://www.ncbi.nlm.nih.gov/nuccore/KP258196http://www.ncbi.nlm.nih.gov/nuccore/KP258204http://www.ncbi.nlm.nih.gov/nuccore/KP738110mailto:[email protected]://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1421392112/-/DCSupplementalhttp://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1421392112/-/DCSupplementalwww.pnas.org/cgi/doi/10.1073/pnas.1421392112

Fig. 1. Partial schematic overview of division machinery in E. coli. (A) Roles of Min proteins during FtsZ polymerization. (B) Subsequent recruitment of earlyand late stage proteins involved in Z-ring stabilization and attachment to the cell membrane. (C) Overview of septation initiation at the cell level. Dark-bluerectangles, FtsZ; dark-green circles, MinD; light-blue shapes, late-stage cell-division proteins; light-green circles, MinC; magenta circles, MinE; red shapes, early-stage cell-division proteins. For the sake of clarity, not all proteins known to localize to the mid-cell during division are shown. In particular, this schematicfocuses on proteins known to localize to the cytoplasmic membrane and excludes most proteins localizing primarily to the peptidoglycan layer and the outermembrane. Based on reviews in refs. 1, 16, and 17.

2 of 8 | www.pnas.org/cgi/doi/10.1073/pnas.1421392112 Leger et al.

www.pnas.org/cgi/doi/10.1073/pnas.1421392112

Fig. 2. Presence and absence of bacterial Min proteins and FtsZ in selected eukaryotic taxa. Blue, predicted mitochondrial proteins; gray, no protein foundencoded in complete genome data; green, predicted plastid proteins; ?, no protein found encoded in transcriptome or incomplete genome data; *, chro-matophore protein; , predicted pseudogene; , with the exception of Physcomitrella patens. Boxes shaded half blue and half green represent multipleparalogs, predicted to be mitochondrial and plastid, respectively. In cases where only a transcriptome or incomplete genome is available, it should be notedthat t