Ignicoccus hospitalis and Nanoarchaeum equitans: Ultrastructure, cell-cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography

Archives of Microbiology

Volumn 190, Issue 3, 2008, Pages 395-408

  Junglas, Benjamin ^a   Briegel, Ariane ^b,c   Burghardt, Tillmann ^a   Walther, Paul ^d   Wirth, Reinhard ^a   Huber, Harald ^a   Rachel, Reinhard ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

3D reconstruction; Cell cell interaction; Crenarchaeota; Cytoskeleton; Ignicoccus hospitalis; Nanoarchaeum equitans; Serial sections; Ultrastructure

Indexed keywords

ANALYTIC METHOD; ARTICLE; BACTERIAL CELL; CELL DIVISION; CELL INTERACTION; CELL MEMBRANE; CELL SURFACE; CELL ULTRASTRUCTURE; CRENARCHAEOTA; CYTOPLASM; CYTOSKELETON; ELECTRON CRYOTOMOGRAPHY; EURYARCHAEOTA; FREEZE DRYING; IGNICOCCUS HOSPITALIS; NANOARCHAEOTA; NANOARCHAEUM EQUITANS; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; THREE DIMENSIONAL IMAGING;

CELL MEMBRANE; CYTOPLASM; DESULFUROCOCCACEAE; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, ELECTRON, TRANSMISSION; NANOARCHAEOTA; TOMOGRAPHY;

CRENARCHAEOTA; EURYARCHAEOTA; IGNICOCCUS; NANOARCHAEUM EQUITANS;

EID: 49749094746     PISSN: 03028933     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00203-008-0402-6     Document Type: Article

References (46)

1. A Al-Amoudi J-J Chang A Leforestier A McDowall LM Salamin LPO Norlén K Richter N Sartori Blanc D Studer J Dubochet 2004 Cryo-electron microscopy of vitreous sections EMBO J 23 3583 3588
2. A Briegel D Prabha Dias Z Li RB Jensen AS Frangakis GJ Jensen 2006 Multiple large filament bundles observed in Caulobacter crescentus by electron cryotomography Mol Microbiol 62 5 14
3. T Burghardt DJ Näther B Junglas H Huber R Rachel 2007 The dominating outer membrane protein of the hyperthermophilic archaeum Ignicoccus hospitalis: a novel pore-forming complex Mol Microbiol 63 166 176
4. Burghardt T, Saller M, Gürster S, Müller D, Meyer C, Jahn U, Hochmuth E, Deutzmann R, Siedler F, Babinger P, Wirth R, Huber H, Rachel R (2008) Insight into the proteome of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis: the major cytosolic and membrane proteins. Arch Microbiol. doi: 10.1007/s00203-008-0399-x
5. C Buser P Walther T Mertens D Michel 2007 Cytomegalovirus primary envelopment occurs at large infoldings of the inner nuclear membrane J Virol 81 3042 3048
6. G Danscher 1981 Localisation of gold in biological tissue. A photochemical method for light- and electron microscopy Histochemistry 71 81 88
7. M Dean Y Hamon G Chimini 2001 The human ATP-binding cassette (ABC) transporter superfamily J Lipid Res 42 1007 1017
8. Frank J (1992) Electron tomography. Plenum Press, New York
9. R Grimm H Singh R Rachel D Typke W Zillig W Baumeister 1998 Electron tomography of ice-embedded prokaryotic cells Biophys J 74 1031 1042
10. R Hegerl 1996 The EM program package: a platform for image processing in biological electron microscopy J Struct Biol 116 30 34
11. JAW Heymann M Mayles I Gestmann LA Giannuzzi B Lich S Subramaniam 2006 Site-specific 3D imaging of cells and tissues with a dual beam microscope J Struct Biol 155 63 73
12. H Hohenberg K Mannweiler M Müller 1994 High-pressure freezing of cell suspensions in cellulose capillaries J Microsc 175 34 43
13. JL Höög C Schwartz AT Noon ET O'Toole DN Mastronarde JR McIntosh C Antony 2007 Organization of interphase microtubules in fission yeast analyzed by electron tomography Dev Cell 12 349 361
14. K Hollenstein DC Frei KP Locher 2007 Structure of an ABC transporter in complex with its binding protein Nature 446 213 216
15. C Horn B Paulmann G Kerlen N Junker H Huber 1999 In vivo observation of cell division of anaerobic hyperthermophiles by using a high-intensity dark-field microscope J Bacteriol 181 5114 5118
16. H Huber S Burggraf T Mayer I Wyschkony R Rachel KO Stetter 2000 Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophic Archaea, represented by two new species, Ignicoccus islandicus sp. nov. and Ignicoccus pacificus sp. nov Int J Syst Evol Microbiol 50 2093 2100
17. H Huber MJ Hohn R Rachel T Fuchs VC Wimmer KO Stetter 2002 A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont Nature 417 63 67
18. H Huber M Gallenberger U Jahn E Eylert IA Berg D Kockelkorn W Eisenreich G Fuchs 2008 A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis Proc Natl Acad Sci USA 105 7851 7856
19. U Jahn R Summons H Sturt E Grosjean H Huber 2004 Composition of the lipids of Nanoarchaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/I Arch Microbiol 182 404 413
20. 2 fixation pathway of the archaeon Ignicoccus hospitalis: comprehensive analysis of the central carbon metabolism J Bacteriol 189 4108 4119
21. U Jahn M Gallenberger W Paper B Junglas W Eisenreich KO Stetter R Rachel H Huber 2008 Nanoarchaeum equitans and Ignicoccus hospitalis: new insights into a unique, intimate association of two Archaea J Bacteriol 190 1743 1750
22. GJ Jensen A Briegel 2007 How electron cryotomography is opening a new window onto prokaryotic ultrastructure Curr Opin Struct Biol 17 260 267
23. König H, Rachel R, Claus H (2007) Proteinaceous surface layers of Archaea: ultrastructure and biochemistry. In: Cavicchioli R (ed) Archaea-molecular and cellular biology. ASM Press, Washington, pp 315-340
24. J Kürner AS Frangakis W Baumeister 2005 Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum Science 307 436 438
25. Z Li MJ Trimble YV Brun GJ Jensen 2007 The structure of FtsZ filaments in vivo suggests a force-generating role in cell division EMBO J 26 4694 4708
26. J Löwe F van den Ent LA Amos 2004 Molecules of the bacterial cytoskeleton Annu Rev Biophys Biomol Struct 33 177 198
27. V Lucic F Förster W Baumeister 2005 Structural studies by electron tomography: from cells to molecules Ann Rev Biochem 74 833 865
28. X Ma DW Ehrhardt W Margolin 1996 Colocalization of cell division proteins Ftsz and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein Proc Natl Acad Sci USA 93 12998 13003
29. DA Mastronarde 1997 Dual-axis tomography: an approach with alignment methods that preserve resolution J Struct Biol 120 343 352
30. R McIntosh D Nicastro DA Mastronarde 2005 New views of cells in 3D: an introduction to electron tomography Trends Cell Biol 15 43 51
31. O Medalia I Weber AS Frangakis D Nicastro G Gerisch W Baumeister 2002 Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography Science 298 1209 1213
32. AML van de Meene MF Hohmann-Marriott WFJ Vermaas RW Roberson 2006 The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803 Arch Microbiol 184 259 270
33. DJ Näther R Rachel 2004 The outer membrane of the hyperthermophilic archaeon Ignicoccus: dynamics, ultrastructure and composition Biochem Soc Trans 32 199 203
34. DJ Näther R Rachel G Wanner R Wirth 2006 Flagella of Pyrococcus furiosus: multifunctional organelles, made for swimming, adhesion to various surfaces, and cell-cell contacts J Bacteriol 188 6915 6923
35. S Nickell R Hegerl W Baumeister R Rachel 2003 Pyrodictium cannulae enter the periplasmic space but do not enter the cytoplasm, as revealed by cryo-electron tomography J Struct Biol 141 34 42
36. W Paper U Jahn MJ Hohn J Kronner DJ Näther T Burghardt R Rachel KO Stetter H Huber 2007 Ignicoccus hospitalis sp. nov., the host of 'Nanoarchaeum equitans' Int J System Evol Microbiol 57 803 808
37. R Rachel I Wyschkony S Riehl H Huber 2002 The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon Archaea 1 9 18
38. G Rieger R Rachel R Hermann KO Stetter 1995 Ultrastructure of the hyperthermophilic archaeon Pyrodictium abyssi J Struct Biol 115 78 87
39. G Rieger K Müller R Hermann KO Stetter R Rachel 1997 Cultivation of hyperthermophilic archaea in capillary tubes resulting in improved preservation of fine structures Arch Microbiol 168 373 379
40. I Rosenshine R Tchelet M Mevarech 1989 The mechanism of DNA transfer in the mating system of an archaebacterium Science 245 1387 1389
41. A Scheffel M Gruska D Faivre A Linaroudis JM Plitzko D Schüler 2006 An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria Nature 440 110 114
42. YD Stierhof BM Humbel R Hermann MT Otten H Schwarz 1992 Direct visualization and silver enhancement of ultrasmall antibody-bound gold particles on immunolabeled ultrathin resin sections Scanning Microsc 6 1009 1012
43. P Walther A Ziegler 2002 Freeze-substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water J Microscopy 208 3 10
44. X Wang J Lutkenhaus 1993 The FtsZ protein of Bacillus subtilis is localized at the division site and has GTPase activity that is dependent upon FtsZ concentration Mol Microbiol 9 435 442
45. E Waters MJ Hohn I Ahel DE Graham MD Adams M Barnstead KY Beeson L Bibbs R Bolanos M Keller K Kretz X Lin E Mathur J Ni M Podar TH Richardson GS Sutton M Simon D Soll KO Stetter JM Short M Noorderwier 2003 The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism Proc Natl Acad Sci USA 100 12984 12988
46. H Wickert W Göttler G Krohne M Lanzer 2004 Maurer's cleft organization in the cytoplasm of Plasmodium falciparum-infected erythrocytes: new insights from three-dimensional reconstruction of serial ultrathin sections Eur J Cell Biol 83 567 582