Structural studies of planctomycete Gemmata obscuriglobus support cell compartmentalisation in a bacterium

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Sagulenko, Evgeny ^a   Morgan, Garry P ^a   Webb, Richard I ^a   Yee, Benjamin ^a   Lee, Kuo Chang ^a   Fuerst, John A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FTSK PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; CELL COMPARTMENTALIZATION; CELL COMPONENT; CELL DIVISION; CELL NUCLEUS INCLUSION BODY; CELL STRUCTURE; GEMMATA; GEMMATA OBSCURIGLOBUS; IMMUNOGOLD STAINING; NONHUMAN; PROTEIN LOCALIZATION; RIBOPLASM; CELL WALL; INTRACELLULAR SPACE; METABOLISM; PLANCTOMYCETALES; PROTEIN TRANSPORT; ULTRASTRUCTURE;

BACTERIAL PROTEINS; CELL COMPARTMENTATION; CELL WALL; INTRACELLULAR SPACE; PLANCTOMYCETALES; PROTEIN TRANSPORT;

EID: 84898444747     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091344     Document Type: Article

References (53)

1. Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, et al. (2001) Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 175: 413-429. (Pubitemid 32646349)
2. Jogler C, Glockner FO, Kolter R (2011) Characterization of Planctomyces limnophilus and development of genetic tools for its manipulation establish it as a model species for the phylum Planctomycetes . Appl Environ Microbiol 77: 5826-5829.
3. Fuerst JA, Webb RI (1991) Membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus. Proc Natl Acad Sci U S A 88: 8184-8188. (Pubitemid 21915321)
4. Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9: 403-413.
5. Fuerst JA (2005) Intracellular compartmentation in planctomycetes. Annu Rev Microbiol 59: 299-328.
6. Yee B, Sagulenko E, Morgan GP, Webb RI, Fuerst JA (2012) Electron tomography of the nucleoid of Gemmata obscuriglobus reveals complex liquid crystalline cholesteric structure. Front Microbiol 3: 326.
7. Santarella-Mellwig R, Pruggnaller S, Roos N, Mattaj IW, Devos DP (2013) Three-dimensional reconstruction of bacteria with a complex endomembrane system. PLoS Biol 11: e1001565.
8. Acehan D, Santarella-Mellwig R, Devos DP (2013) A bacterial tubulovesicular network. J Cell Sci.
9. Devos DP (2013) Re-interpretation of the evidence for the PVC cell plan supports a Gram-negative origin. Antonie Van Leeuwenhoek.
10. Stackebrandt E, Wehmeyer U, Liesack W (1986) 16S ribosomal RNA- and cell wall analysis of Gemmata obscuriglobus, a new member of the order Planctomycetales. FEMS Microbiol Lett 37: 289-292. (Pubitemid 17204762)
11. Giovannoni SJ, Godchaux W, 3rd, Schabtach E, Castenholz RW (1987) Cell wall and lipid composition of Isosphaera pallida, a budding eubacterium from hot springs. J Bacteriol 169: 2702-2707. (Pubitemid 17104335)
12. Liesack W, Konig H, Schlesner H, Hirsch P (1986) Chemical composition of the peptidoglycan-free cell envelopes of budding bacteria of the Pirella /Planctomyces group. Arch Microbiol 145: 361-366. (Pubitemid 16030979)
13. Wang L, Lutkenhaus J (1998) FtsK is an essential cell division protein that is localized to the septum and induced as part of the SOS response. Mol Microbiol 29: 731-740. (Pubitemid 28365460)
14. Addinall SG, Bi E, Lutkenhaus J (1996) FtsZ ring formation in fts mutants. J Bacteriol 178: 3877-3884. (Pubitemid 26227205)
15. Ben-Yehuda S, Losick R (2002) Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109: 257-266. (Pubitemid 34518263)
16. Thanedar S, Margolin W (2004) FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr Biol 14: 1167-1173. (Pubitemid 38893979)
17. Wang SC, West L, Shapiro L (2006) The bifunctional FtsK protein mediates chromosome partitioning and cell division in Caulobacter. J Bacteriol 188: 1497-1508. (Pubitemid 43228683)
18. Lee KC, Webb RI, Fuerst JA (2009) The cell cycle of the planctomycete Gemmata obscuriglobus with respect to cell compartmentalization. BMC Cell Biol 10: 4.
19. Kuznetsov YG, Klose T, Rossmann M, McPherson A (2013) Morphogenesis of mimivirus and its viral factories: an atomic force microscopy study of infected cells. J Virol 87: 11200-11213.
20. Rachel R, Wyschkony I, Riehl S, Huber H (2002) The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 1: 9-18. (Pubitemid 38871626)
21. Huber H, Kuper U, Daxer S, Rachel R (2012) The unusual cell biology of the hyperthermophilic Crenarchaeon Ignicoccus hospitalis. Antonie Van Leeuwenhoek 102: 203-219.
22. Kuper U, Meyer C, Muller V, Rachel R, Huber H (2010) Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon Ignicoccus hospitalis. Proc Natl Acad Sci U S A 107: 3152-3156.
23. Sutcliffe IC (2010) A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18: 464-470.
24. Beveridge TJ (1999) Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181: 4725-4733.
25. Devos DP (2014) PVC bacteria: variation of, but not exception to, the Gram-negative cell plan. Trends Microbiol 22: 14-20.
26. Acehan D, Santarella-Mellwig R, Devos DP (2014) A bacterial tubulovesicular network. J Cell Sci 127: 277-280.
27. Devos DP (2014) Re-interpretation of the evidence for the PVC cell plan supports a Gram-negative origin. Antonie Van Leeuwenhoek 105: 271-274.
28. Engelhardt H (2007) Are S-layers exoskeletons? The basic function of protein surface layers revisited. J Struct Biol 160: 115-124.
29. Matias VR, Beveridge TJ (2005) Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol Microbiol 56: 240-251. (Pubitemid 40461502)
30. van Teeseling MC, de Almeida NM, Klingl A, Speth DR, Op den Camp HJ, et al. (2014) A new addition to the cell plan of anammox bacteria: "Candidatus Kuenenia stuttgartiensis" has a protein surface layer as the outermost layer of the cell. J Bacteriol 196: 80-89.
31. Amat F, Comolli LR, Nomellini JF, Moussavi F, Downing KH, et al. (2010) Analysis of the intact surface layer of Caulobacter crescentus by cryo-electron tomography. J Bacteriol 192: 5855-5865.
32. Goley ED, Yeh YC, Hong SH, Fero MJ, Abeliuk E, et al. (2011) Assembly of the Caulobacter cell division machine. Mol Microbiol 80: 1680-1698.
33. Speth DR, van Teeseling MC, Jetten MS (2012) Genomic analysis indicates the presence of an asymmetric bilayer outer membrane in planctomycetes and verrucomicrobia. Front Microbiol 3: 304.
34. Lonhienne TG, Sagulenko E, Webb RI, Lee KC, Franke J, et al. (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci U S A 107: 12883-12888.
35. Hobot JA, Carlemalm E, Villiger W, Kellenberger E (1984) Periplasmic gel: new concept resulting from the reinvestigation of bacterial cell envelope ultrastructure by new methods. J Bacteriol 160: 143-152. (Pubitemid 14022809)
36. Fuerst JA, Sagulenko E (2010) Protein uptake by bacteria: An endocytosis-like process in the planctomycete Gemmata obscuriglobus. Commun Integr Biol 3: 572-575.
37. Lindsay MR, Webb RI, Fuerst JA (1997) Pirellulosomes: A new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula . Microbiology-Uk 143: 739-748. (Pubitemid 27192751)
38. Santarella-Mellwig R, Franke J, Jaedicke A, Gorjanacz M, Bauer U, et al. (2010) The compartmentalized bacteria of the planctomycetes-verrucomicrobia- chlamydiae superphylum have membrane coat-like proteins. PLoS Biol 8: e1000281.
39. Devos DP (2013) PVC bacteria: variation of, but not exception to, the Gram-negative cell plan. Trends Microbiol.
40. Pilhofer M, Rappl K, Eckl C, Bauer AP, Ludwig W, et al. (2008) Characterization and evolution of cell division and cell wall synthesis genes in the bacterial phyla Verrucomicrobia, Lentisphaerae, Chlamydiae, and Planctomycetes and phylogenetic comparison with rRNA genes. J Bacteriol 190: 3192-3202. (Pubitemid 351581415)
41. Bernander R, Ettema TJ (2010) FtsZ-less cell division in archaea and bacteria. Curr Opin Microbiol 13: 747-752.
42. Bisicchia P, Steel B, Mariam Debela MH, Lowe J, Sherratt D (2013) The N-terminal membrane-spanning domain of the Escherichia coli DNA translocase FtsK hexamerizes at midcell. MBio 4: e00800-00813.
43. Dubarry N, Barre FX (2010) Fully efficient chromosome dimer resolution in Escherichia coli cells lacking the integral membrane domain of FtsK. EMBO J 29: 597-605.
44. Hale CA, de Boer PA (2002) ZipA is required for recruitment of FtsK, FtsQ, FtsL, and FtsN to the septal ring in Escherichia coli. J Bacteriol 184: 2552-2556. (Pubitemid 34311151)
45. Sherratt D (2013) Plasmid partition: sisters drifting apart. EMBO J 32: 1208-1210.
46. Fuerst JA (2013) The PVC superphylum: exceptions to the bacterial definition? Antonie Van Leeuwenhoek 104: 451-466.
47. Forterre P, Gribaldo S (2010) Bacteria with a eukaryotic touch: a glimpse of ancient evolution? Proc Natl Acad Sci U S A 107: 12739-12740.
48. Fuerst JA, Sagulenko E (2012) Keys to eukaryality: planctomycetes and ancestral evolution of cellular complexity. Front Microbiol 3: 167.
49. Fuerst JA, Sagulenko E (2013) Nested bacterial boxes: nuclear and other intracellular compartments in planctomycetes. J Mol Microbiol Biotechnol 23: 95-103.
50. Fuerst JA, Sagulenko E (2013) Towards understanding the molecular mechanism of the endocytosis-like process in the bacterium Gemmata obscuriglobus. Biochim Biophys Acta. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research doi: 10.1016/j.bbamcr.2013.10.002.
51. Dacks JB, Poon PP, Field MC (2008) Phylogeny of endocytic components yields insight into the process of nonendosymbiotic organelle evolution. Proc Natl Acad Sci U S A 105: 588-593. (Pubitemid 351171752)
52. Neumann N, Lundin D, Poole AM (2010) Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS One 5: e13241.
53. Schlesner H (1994) The development of media suitable for the microorganisms morphologically resembling Planctomyces spp, Pirellula spp, and other Planctomycetales from various aquatic habitats using dilute media. Systematic and Applied Microbiology 17: 135-145.