An ancestral bacterial division system is widespread in eukaryotic mitochondria
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
Canadian Institutes of Health Research - Canada
PubMed
25831547
PubMed Central
PMC4547283
DOI
10.1073/pnas.1421392112
PII: 1421392112
Knihovny.cz E-zdroje
- Klíčová slova
- Min proteins, MinCDE, mitochondria, mitochondrial division, mitochondrial fission,
- MeSH
- adenosintrifosfatasy metabolismus MeSH
- Arabidopsis genetika MeSH
- Bacteria cytologie MeSH
- bakteriální proteiny genetika metabolismus MeSH
- buněčné dělení MeSH
- cytoskeletální proteiny genetika MeSH
- databáze genetické MeSH
- Dictyostelium metabolismus MeSH
- DNA bakterií genetika MeSH
- fylogeneze MeSH
- mitochondriální dynamika * MeSH
- mitochondrie metabolismus MeSH
- molekulární evoluce MeSH
- molekulární sekvence - údaje MeSH
- plastidy metabolismus MeSH
- pravděpodobnostní funkce MeSH
- proteiny buněčného cyklu metabolismus MeSH
- proteiny z Escherichia coli metabolismus MeSH
- Saccharomyces cerevisiae genetika metabolismus MeSH
- sekvence nukleotidů MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- adenosintrifosfatasy MeSH
- bakteriální proteiny MeSH
- cytoskeletální proteiny MeSH
- DNA bakterií MeSH
- FtsZ protein, Bacteria MeSH Prohlížeč
- MinC protein, Bacteria MeSH Prohlížeč
- MinD protein, E coli MeSH Prohlížeč
- MinE protein, E coli MeSH Prohlížeč
- proteiny buněčného cyklu MeSH
- proteiny z Escherichia coli MeSH
Bacterial division initiates at the site of a contractile Z-ring composed of polymerized FtsZ. The location of the Z-ring in the cell is controlled by a system of three mutually antagonistic proteins, MinC, MinD, and MinE. Plastid division is also known to be dependent on homologs of these proteins, derived from the ancestral cyanobacterial endosymbiont that gave rise to plastids. In contrast, the mitochondria of model systems such as Saccharomyces cerevisiae, mammals, and Arabidopsis thaliana seem to have replaced the ancestral α-proteobacterial Min-based division machinery with host-derived dynamin-related proteins that form outer contractile rings. Here, we show that the mitochondrial division system of these model organisms is the exception, rather than the rule, for eukaryotes. We describe endosymbiont-derived, bacterial-like division systems comprising FtsZ and Min proteins in diverse less-studied eukaryote protistan lineages, including jakobid and heterolobosean excavates, a malawimonad, stramenopiles, amoebozoans, a breviate, and an apusomonad. For two of these taxa, the amoebozoan Dictyostelium purpureum and the jakobid Andalucia incarcerata, we confirm a mitochondrial localization of these proteins by their heterologous expression in Saccharomyces cerevisiae. The discovery of a proteobacterial-like division system in mitochondria of diverse eukaryotic lineages suggests that it was the ancestral feature of all eukaryotic mitochondria and has been supplanted by a host-derived system multiple times in distinct eukaryote lineages.
Zobrazit více v PubMed
de Boer PA. Advances in understanding E. coli cell fission. Curr Opin Microbiol. 2010;13(6):730–737. PubMed PMC
Meier EL, Goley ED. Form and function of the bacterial cytokinetic ring. Curr Opin Cell Biol. 2014;26:19–27. PubMed
Natale P, Pazos M, Vicente M. The Escherichia coli divisome: Born to divide. Environ Microbiol. 2013;15(12):3169–3182. PubMed
Lutkenhaus J, Pichoff S, Du S. Bacterial cytokinesis: From Z ring to divisome. Cytoskeleton (Hoboken) 2012;69(10):778–790. PubMed PMC
Lutkenhaus J. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem. 2007;76:539–562. PubMed
Ghosal D, Trambaiolo D, Amos LA, Löwe J. MinCD cell division proteins form alternating copolymeric cytomotive filaments. Nat Commun. 2014;5:5341. PubMed PMC
Hale CA, Meinhardt H, de Boer PA. Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. EMBO J. 2001;20(7):1563–1572. PubMed PMC
Loose M, Fischer-Friedrich E, Ries J, Kruse K, Schwille P. Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science. 2008;320(5877):789–792. PubMed
Park KT, Wu W, Lovell S, Lutkenhaus J. Mechanism of the asymmetric activation of the MinD ATPase by MinE. Mol Microbiol. 2012;85(2):271–281. PubMed PMC
Hu Z, Lutkenhaus J. Topological regulation of cell division in E. coli. spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol Cell. 2001;7(6):1337–1343. PubMed
Hale CA, de Boer PA. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell. 1997;88(2):175–185. PubMed
Wang X, Huang J, Mukherjee A, Cao C, Lutkenhaus J. Analysis of the interaction of FtsZ with itself, GTP, and FtsA. J Bacteriol. 1997;179(17):5551–5559. PubMed PMC
Pichoff S, Lutkenhaus J. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 2002;21(4):685–693. PubMed PMC
Hale CA, de Boer PA. Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ and independent of FtsA. J Bacteriol. 1999;181(1):167–176. PubMed PMC
Galli E, Gerdes K. Spatial resolution of two bacterial cell division proteins: ZapA recruits ZapB to the inner face of the Z-ring. Mol Microbiol. 2010;76(6):1514–1526. PubMed
Egan AJ, Vollmer W. The physiology of bacterial cell division. Ann N Y Acad Sci. 2013;1277:8–28. PubMed
den Blaauwen T, Andreu JM, Monasterio O. Bacterial cell division proteins as antibiotic targets. Bioorg Chem. 2014;55:27–38. PubMed
Fraunholz MJ, Moerschel E, Maier UG. The chloroplast division protein FtsZ is encoded by a nucleomorph gene in cryptomonads. Mol Gen Genet. 1998;260(2-3):207–211. PubMed
Sato M, Nishikawa T, Yamazaki T, Kawano S. Isolation of the plastid ftsZ gene from Cyanophora paradoxa (Glaucocystophyceae, Glaucocystophyta) Phycol Res. 2005;53:93–96.
Osteryoung KW, Vierling E. Conserved cell and organelle division. Nature. 1995;376(6540):473–474. PubMed
Wakasugi T, et al. Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: The existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA. 1997;94(11):5967–5972. PubMed PMC
Colletti KS, et al. A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol. 2000;10(9):507–516. PubMed
Itoh R, Fujiwara M, Nagata N, Yoshida S. A chloroplast protein homologous to the eubacterial topological specificity factor minE plays a role in chloroplast division. Plant Physiol. 2001;127(4):1644–1655. PubMed PMC
Miyagishima SY, Kabeya Y, Sugita C, Sugita M, Fujiwara T. DipM is required for peptidoglycan hydrolysis during chloroplast division. BMC Plant Biol. 2014;14:57. PubMed PMC
Douglas SE, Penny SL. The plastid genome of the cryptophyte alga, Guillardia theta: Complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol. 1999;48(2):236–244. PubMed
Vieler A, et al. Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS Genet. 2012;8(11):e1003064. PubMed PMC
Gilson PR, et al. Two Dictyostelium orthologs of the prokaryotic cell division protein FtsZ localize to mitochondria and are required for the maintenance of normal mitochondrial morphology. Eukaryot Cell. 2003;2(6):1315–1326. PubMed PMC
Beech PL, et al. Mitochondrial FtsZ in a chromophyte alga. Science. 2000;287(5456):1276–1279. PubMed
Kiefel BR, Gilson PR, Beech PL. Diverse eukaryotes have retained mitochondrial homologues of the bacterial division protein FtsZ. Protist. 2004;155(1):105–115. PubMed
Takahara M, et al. A putative mitochondrial ftsZ gene is present in the unicellular primitive red alga Cyanidioschyzon merolae. Mol Gen Genet. 2000;264(4):452–460. PubMed
Takahara M, Kuroiwa H, Miyagishima S, Mori T, Kuroiwa T. Localization of the mitochondrial FtsZ protein in a dividing mitochondrion. Cytologia (Tokyo) 2001;66:421–425.
Bleazard W, et al. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol. 1999;1(5):298–304. PubMed PMC
Labrousse AM, Zappaterra MD, Rube DA, van der Bliek AM. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell. 1999;4(5):815–826. PubMed
Smirnova E, Griparic L, Shurland DL, van der Bliek AM. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell. 2001;12(8):2245–2256. PubMed PMC
Arimura S, Tsutsumi N. A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division. Proc Natl Acad Sci USA. 2002;99(8):5727–5731. PubMed PMC
Mano S, Nakamori C, Kondo M, Hayashi M, Nishimura M. An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant J. 2004;38(3):487–498. PubMed
Arimura S, Aida GP, Fujimoto M, Nakazono M, Tsutsumi N. Arabidopsis dynamin-like protein 2a (ADL2a), like ADL2b, is involved in plant mitochondrial division. Plant Cell Physiol. 2004;45(2):236–242. PubMed
Wexler-Cohen Y, Stevens GC, Barnoy E, van der Bliek AM, Johnson PJ. A dynamin-related protein contributes to Trichomonas vaginalis hydrogenosomal fission. FASEB J. 2014;28(3):1113–1121. PubMed PMC
Wienke DC, Knetsch ML, Neuhaus EM, Reedy MC, Manstein DJ. Disruption of a dynamin homologue affects endocytosis, organelle morphology, and cytokinesis in Dictyostelium discoideum. Mol Biol Cell. 1999;10(1):225–243. PubMed PMC
Nishida K, et al. Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci USA. 2003;100(4):2146–2151. PubMed PMC
Purkanti R, Thattai M. Ancient dynamin segments capture early stages of host-mitochondrial integration. Proc Natl Acad Sci USA. 2015;112(9):2800–2805. PubMed PMC
Altschul SF, et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–3402. PubMed PMC
Benson DA, et al. GenBank. Nucleic Acids Res. 2014;42(Database issue):D32–D37. PubMed PMC
Origins of Multicellularity Sequencing Project, Broad Institute of Harvard and MIT www.broadinstitute.org/. Accessed April 23, 2014.
Grigoriev IV, et al. The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res. 2012;40(Database issue):D26–D32. PubMed PMC
Nordberg H, et al. The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res. 2014;42(Database issue):D26–D31. PubMed PMC
Kreppel L, et al. dictyBase: A new Dictyostelium discoideum genome database. Nucleic Acids Res. 2004;32(Database issue):D332–D333. PubMed PMC
Basu S, et al. DictyBase 2013: Integrating multiple Dictyostelid species. Nucleic Acids Res. 2013;41(Database issue):D676–D683. PubMed PMC
Fey P, Dodson RJ, Basu S, Chisholm RL. One stop shop for everything Dictyostelium: dictyBase and the Dicty Stock Center in 2012. Methods Mol Biol. 2013;983:59–92. PubMed PMC
Flicek P, et al. Ensembl 2014. Nucleic Acids Res. 2014;42(Database issue):D749–D755. PubMed PMC
Aurrecoechea C, et al. ApiDB: Integrated resources for the apicomplexan bioinformatics resource center. Nucleic Acids Res. 2007;35(Database issue):D427–D430. PubMed PMC
Keeling PJ, et al. The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 2014;12(6):e1001889. PubMed PMC
Sun S, et al. Community cyberinfrastructure for Advanced Microbial Ecology Research and Analysis: The CAMERA resource. Nucleic Acids Res. 2011;39(Database issue):D546–D551. PubMed PMC
Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol. 2000;300(4):1005–1016. PubMed
Emanuelsson O, Brunak S, von Heijne G, Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc. 2007;2(4):953–971. PubMed
Park JS, Simpson AG. 2011. Characterization of Pharyngomonas kirbyi (= “Macropharyngomonas halophila” nomen nudum), a very deep-branching, obligately halophilic heterolobosean flagellate. Protist 162(5):691–709.
Harding T, et al. Amoeba stages in the deepest branching heteroloboseans, including Pharyngomonas: Evolutionary and systematic implications. Protist. 2013;164(2):272–286. PubMed
Edgar RC. MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004;5:113. PubMed PMC
Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059–3066. PubMed PMC
Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: Improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005;33(2):511–518. PubMed PMC
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780. PubMed PMC
Criscuolo A, Gribaldo S. BMGE (Block Mapping and Gathering with Entropy): A new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol. 2010;10:210. PubMed PMC
Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–1313. PubMed PMC
Le SQ, Dang CC, Gascuel O. Modeling protein evolution with several amino acid replacement matrices depending on site rates. Mol Biol Evol. 2012;29(10):2921–2936. PubMed
Lartillot N, Lepage T, Blanquart S. PhyloBayes 3: A Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics. 2009;25(17):2286–2288. PubMed
Shimodaira H, Hasegawa M. CONSEL: For assessing the confidence of phylogenetic tree selection. Bioinformatics. 2001;17(12):1246–1247. PubMed
Price DC, et al. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science. 2012;335(6070):843–847. PubMed
Simpson AG, Patterson DJ. On core jakobids and excavate taxa: The ultrastructure of Jakoba incarcerata. J Eukaryot Microbiol. 2001;48(4):480–492. PubMed
Stairs CW, et al. A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia. Curr Biol. 2014;24(11):1176–1186. PubMed
Miyagishima SY, et al. Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: The duplication of FtsZ is implicated in endosymbiosis. J Mol Evol. 2004;58(3):291–303. PubMed
TerBush AD, Yoshida Y, Osteryoung KW. FtsZ in chloroplast division: Structure, function and evolution. Curr Opin Cell Biol. 2013;25(4):461–470. PubMed
Heidel AJ, et al. Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication. Genome Res. 2011;21(11):1882–1891. PubMed PMC
Romeralo M, Cavender JC, Landolt JC, Stephenson SL, Baldauf SL. An expanded phylogeny of social amoebas (Dictyostelia) shows increasing diversity and new morphological patterns. BMC Evol Biol. 2011;11:84. PubMed PMC
Lara E, Chatzinotas A, Simpson AGB. Andalucia (n. gen.): The deepest branch within jakobids (Jakobida; Excavata), based on morphological and molecular study of a new flagellate from soil. J Eukaryot Microbiol. 2006;53(2):112–120. PubMed
Brown MW, Sharpe SC, Silberman JD, Heiss AA, Lang BF, et al. Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. P Roy Soc B-Biol Sci. 2013;280(1769) PubMed PMC
Heiss AA, Walker G, Simpson AG. The microtubular cytoskeleton of the apusomonad Thecamonas, a sister lineage to the opisthokonts. Protist. 2013;164(5):598–621. PubMed
Barberà MJ, et al. Sawyeria marylandensis (Heterolobosea) has a hydrogenosome with novel metabolic properties. Eukaryot Cell. 2010;9(12):1913–1924. PubMed PMC
Bendich AJ, Gauriloff LP. Morphometric analysis of cucurbit mitochondria: The relationship between chondriome volume and DNA content. Protoplasma. 1984;119:1–7.
Seguí-Simarro JM, Coronado MJ, Staehelin LA. The mitochondrial cycle of Arabidopsis shoot apical meristem and leaf primordium meristematic cells is defined by a perinuclear tentaculate/cage-like mitochondrion. Plant Physiol. 2008;148(3):1380–1393. PubMed PMC
Buetow DE. 1989. The mitochondrion. The Biology of Euglena: Subcellular Biochemistry and Molecular Biology, ed Buetow DE (Academic, San Diego), Vol 4, pp 247–314.
Hogan MJ, Yoneda C, Feeney L, Zweigart P, Lewis A. Morphology and culture of Toxoplasma. Arch Ophthalmol. 1960;64:655–667. PubMed
van Dooren GG, et al. Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol Microbiol. 2005;57(2):405–419. PubMed
Hardham AR. Ultrastructure and serial section reconstruction of zoospores of the fungus Phytophthora cinnamomi. Exp Mycol. 1987;11(4):297–306.
Yoshida Y, et al. The bacterial ZapA-like protein ZED is required for mitochondrial division. Curr Biol. 2009;19(17):1491–1497. PubMed
Friedman JR, et al. ER tubules mark sites of mitochondrial division. Science. 2011;334(6054):358–362. PubMed PMC
Miyagishima SY, Nishida K, Kuroiwa T. An evolutionary puzzle: chloroplast and mitochondrial division rings. Trends Plant Sci. 2003;8(9):432–438. PubMed
Evidence for an Independent Hydrogenosome-to-Mitosome Transition in the CL3 Lineage of Fornicates
Vestiges of the Bacterial Signal Recognition Particle-Based Protein Targeting in Mitochondria
ZapE/Afg1 interacts with Oxa1 and its depletion causes a multifaceted phenotype
Mitochondrial dynamics in parasitic protists
GENBANK
KP258196, KP258197, KP258198, KP258199, KP258200, KP258201, KP258202, KP258203, KP258204, KP271960, KP271961, KP271962, KP271963, KP271964, KP324909, KP324910, KP324911, KP324912, KP738110