Size-independent symmetric division in extraordinarily long cells

Nature Communications

Volumn 5, Issue , 2014, Pages

  Pende, Nika ^a   Leisch, Nikolaus ^b   Gruber Vodicka, Harald R ^a   Heindl, Niels R ^b   Ott, Jörg ^a   Den Blaauwen, Tanneke ^c   Bulgheresi, Silvia ^a,d  

^a UNIVERSITY OF VIENNA   (Austria)

^b MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d Medical University of Vienna   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; BACTERIAL DNA; BACTERIAL PROTEIN; CYTOSKELETON PROTEIN; FTSZ PROTEIN, BACTERIA; RNA 16S;

BACTERIUM; CYTOLOGY; DNA; IMMUNE SYSTEM; MORPHOMETRY; SYMMETRY; ULTRASTRUCTURE;

ARTICLE; BACTERIAL CELL; CELL DIVISION; CELL SIZE; EUBOSTRICHUS DIANEAE; EUBOSTRICHUS FERTILIS; GAMMAPROTEOBACTERIA; IMMUNOCYTOCHEMISTRY; MORPHOMETRICS; NEMATODE; NONHUMAN; ULTRASTRUCTURE; ANIMAL; AQUATIC SPECIES; BACTERIAL GENE; BACTERIUM ADHERENCE; BIOLOGICAL MODEL; CLASSIFICATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENETICS; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; SYMBIOSIS;

BACTERIA (MICROORGANISMS); EUBOSTRICHUS; GAMMAPROTEOBACTERIA; NEMATODA;

ANIMALS; AQUATIC ORGANISMS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CELL DIVISION; CYTOSKELETAL PROTEINS; DNA, BACTERIAL; GAMMAPROTEOBACTERIA; GENE EXPRESSION; GENES, BACTERIAL; IN SITU HYBRIDIZATION, FLUORESCENCE; MICROSCOPY, ELECTRON, SCANNING; MODELS, GENETIC; NEMATODA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

EID: 84923353153     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5803     Document Type: Article

References (60)

1. Goley, E. D. Tiny cells meet big questions: a closer look at bacterial cell biology. Mol. Biol. Cell 24, 1099-1102 (2013)
2. Silver, L. Challenges of antibacterial discovery. Clin. Microbiol. Rev. 24, 71-109 (2011)
3. Chien, A. C., Hill, N. S. &Levin, P. A. Cell size control in bacteria. Curr. Biol. 22, R340-R349 (2012)
4. Marshall, W. F. et al. What determines cell size? BMC Biol. 10, 101 (2012)
5. Errington, J., Daniel, R. A. &Scheffers, D. J. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67, 52-65 (2003)
6. Pierucci, O., Helmstetter, C. E., Rickert, M., Weinberger, M. &Leonard, A. C. Overexpression of the dnaA gene in Escherichia coli B/r: chromosome and minichromosome replication in the presence of rifampin. J. Bacteriol. 169, 1871-1877 (1987)
7. Sargent, M. G. Control of cell length in Bacillus subtilis. J. Bacteriol. 123, 7-19 (1975)
8. Weart, R. B. et al. A metabolic sensor governing cell size in bacteria. Cell 130, 335-347 (2007)
9. Trueba, F. J. &Woldringh, C. L. Changes in cell diameter during the division cycle of Escherichia coli. J. Bacteriol. 142, 869-878 (1980)
10. Zaritsky, A., Woldringh, C. L., Helmstetter, C. E. &Grover, N. B. Dimensional rearrangement of Escherichia coli B/r cells during a nutritional shift-down. J. Gen. Microbiol. 139, 2711-2714 (1993)
11. Hill, N. S., Buske, P. J. &Levin, P. A. A moonlighting enzyme links Escherichia coli cell size with cenral metabolism. PLoS Genet. 9, e1003663 (2013)
12. Grover, N. B. &Woldringh, C. L. Dimensional regulation of cell-cycle events in Escherichia coli during steady-state growth. Microbiology 147, 171-181 (2001)
13. Angert, E. R. &Clements, K. D. Initiation of intracellular offspring in Epulopiscium. Mol. Microbiol. 51, 827-835 (2004)
14. Schulz, H. N. &Jorgensen, B. B. Big bacteria. Annu. Rev. Microbiol. 55, 105-137 (2001)
15. Ott, J. A., Leisch, N. &Gruber-Vodicka, H. R. Eubostrichus fertilis n. sp., a new marine nematode (Desmodoridae, Stilbonematinae) with an extraordinary reproductive potential from Belize, Central America. Nematology doi:10.1163/15685411-00002807 in the press
16. Hopper, B. E. &Cefalu, R. C. Free-living marine nematodes from Biscayne-Bay, Florida. V. Stilbonematinae: contributions to the taxonomy and morphology of the genus Eubostrichus Greeff and related genera. Trans. Am. Microsc. Soc. 92, 578-591 (1973)
17. Polz, M., Felbeck, H., Novak, R., Nebelsick, M. &Ott, J. Chemoautotrophic, sulphur-oxidizing symbiotic bacteria on marine nematodes: morphological and biochemical characterization. Microb. Ecol. 24, 313-329 (1992)
18. Himmel, D., Maurin, L. C., Gros, O. &Mansot, J. L. Raman microspectrometry sulphur detection and characterization in the marine ectosymbiotic nematode Eubostrichus dianae (Desmodoridae, Stilbonematidae) Biol. Cell. 101, 43-54 (2009)
19. Maurin, L. C., Himmel, D., Mansot, J. L. &Gros, O. Raman microspectrometry as a powerful tool for a quick screening of thiotrophy: an application on mangrove swamp meiofauna of Guadeloupe (F.W.I.) Mar. Environ. Res. 69, 382-389 (2010)
20. Polz, M. F., Harbison, C. &Cavanaugh, C. M. Diversity and heterogeneity of epibiotic bacterial communities on the marine nematode Eubostrichus dianae. Appl. Environ. Microbiol. 65, 4271-4275 (1999)
21. Berger, E. C., Urbancik, W. &Ott, J. A. Eubostrichus topiarius sp.n. a new free-living marine species of Stilbonematinae (Nematoda: Desmodoridae) from a shallow subtidal sand bottom. Nematologica 42, 521-536 (1996)
22. Ott, J. A. A new symbiotic, marine nematode Adelphos rolandi gen.n. sp.n. (Stilbonematinae), from the Caribbean Sea. Ann. Nat. Hist. Mus. Wien 99, 417-422 (1997)
23. Heindl, N. R. et al. First detection of thiotrophic symbiont phylotypes in the pelagic marine environment. FEM Microbiol. Ecol. 77, 223-227 (2011)
24. Polz, M. F. et al. Phylogenetic analysis of a highly specific association between ectosymbiotic, sulphur-oxidizing bacteria and a marine nematode. Appl. Environ. Microbiol. 60, 4461-4467 (1994)
25. Bayer, C. et al. Molecular characterization of the symbionts associated with marine nematodes of the genus Robbea. Environ. Microbiol. Rep. 1, 136-144 (2009)
26. Bulgheresi, S. et al. Sequence variability of the pattern recognition receptor Mermaid mediates specificity of marine nematode symbioses. ISME J. 5, 986-998 (2011)
27. Bi, E. F. &Lutkenhaus, J. FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161-164 (1991)
28. Addinall, S. G. &Holland, B. The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J. Mol. Biol. 318, 219-236 (2002)
29. den Blaauwen, T., de Pedro, M. A., Nguyen-Disteche, M. &Ayala, J. A. Morphogenesis of rod-shaped sacculi. FEMS Microbiol. Rev. 32, 321-344 (2008)
30. Adams, D. W. &Errington, J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat. Rev. Microbiol. 7, 642-653 (2009)
31. Leisch, N. et al. Growth in width and FtsZ ring longitudinal positioning in a gammaproteobacterial symbiont. Curr. Biol. 22, R831-R832 (2012)
32. RayChaudhuri, D., Gordon, G. S. &Wright, A. How does a bacterium find its middle? Nat. Struct. Biol. 7, 997-999 (2000)
33. De Boer, P., Crossley, R. E. &Rothfield, L. I. Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J. Bacteriol. 174, 63-70 (1992)
34. Mergaert, P. et al. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc. Natl Acad. Sci. USA 103, 5230-5235 (2006)
35. Nardon, P. &Wicker, C. La symbiose chez le genre Sitophilus (Coleoptere Curculionide): principaux aspects morphologiques, physiologiques et genetiques [bacterie symbiotique]. Annee Biol. 20, 327-373 (1981)
36. Wu, D. et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4, e188 (2006)
37. Mendell, J. E., Clements, K. D., Choat, J. H. &Angert, E. R. Extreme polyploidy in a large bacterium. Proc. Natl Acad. Sci. USA 105, 6730-6734 (2008)
38. Van de Velde, W. et al. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327, 1122-1126 (2010)
39. Login, F. H. et al. Antimicrobial peptides keep insect endosymbionts under control. Science 334, 362-365 (2011)
40. Miller, D. A., Suen, G., Clements, K. D. &Angert, E. R. The genomic basis for the evolution of a novel form of cellular reproduction in the bacterium Epulopiscium. BMC Genomics 13, 265 (2012)
41. Angert, E. R. DNA replication and genomic architecture of very large bacteria. Annu. Rev. Microbiol. 66, 197-212 (2012)
42. Wang, X., Montero Llopis, P. &Rudner, D. Organization and segregation of bacterial chromosomes. Nat. Rev. Genet. 14, 191-203 (2013)
43. Kampfer, S., Sturmbauer, C. &Ott, J. A. Phylogenetic analysis of rDNA sequences from adenophorean nematodes and implications for the adenophorea-secernentea controversy. Invertebr. Biol. 117, 29-36 (1998)
44. Schizas, N. V., Street, G. T., Coull, B. C., Chandler, G. T. &Quattro, J. M. An efficient DNA extraction method for small metazoans. Mol. Mar. Biol. Biotechnol. 6, 381-383 (1997)
45. Juretschko, S. et al. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl. Environ. Microbiol. 64, 3042-3051 (1998)
46. Kane, M. D., Poulsen, L. K. &Stahl, D. A. Monitoring the enrichment and isolation of sulfate-reducing bacteria by using oligonucleotide hybridization probes designed from environmentally derived 16S rRNA sequences. Appl. Environ. Microbiol. 59, 682-686 (1993)
47. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. &Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990)
48. Katoh, K., Kuma, K.-I., Toh, H. &Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511-518 (2005)
49. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690 (2006)
50. Ronquist, F. &Huelsenbeck, J. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574 (2003)
51. Stamatakis, A., Hoover, P. &Rougemont, J. A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol. 57, 758-771 (2008)
52. Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371 (2004)
53. Pruesse, E. et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188-7196 (2007)
54. Cole, J. et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37, D141 D145 (2009)
55. Manz, W., Amann, R., Ludwig, W., Wagner, M. &Schleifer, K.-H. Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst. Appl. Microbiol. 15, 593-600 (1992)
56. Amann, R. I., Krumholz, L. &Stahl, D. A. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J. Bacteriol. 172, 762-770 (1990)
57. Brosius, J., Palmer, M. L., Kennedy, P. J. &Noller, H. F. Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc. Natl Acad. Sci. USA 75, 4801-4805 (1978)
58. Schneider, C. A., Rasband, W. S. &Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012)
59. van der Ploeg, R. et al. Colocalization and interaction between elongasome and divisome during a preparative cell division phase in Escherichia coli. Mol. Microbiol. 87, 1074-1087 (2013)
60. Marie, D., Vaulot, D. &Partensky, F. Application of the novel nucleic acid dyes YOYO-1, YO-PRO-1, and PicoGreen for flow cytometric analysis of marine prokaryotes. Appl. Environ. Microbiol. 62, 1649-1655 (1996)