Anammox Planctomycetes have a peptidoglycan cell wall

Nature Communications

Volumn 6, Issue , 2015, Pages

  Van Teeseling, Muriel C F ^a   Mesman, Rob J ^a   Kuru, Erkin ^b   Espaillat, Akbar ^c   Cava, Felipe ^c   Brun, Yves V ^b   Vannieuwenhze, Michael S ^b   Kartal, Boran ^a,d   Van Niftrik, Laura ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b INDIANA UNIVERSITY   (United States)

^c UMEÅ UNIVERSITY   (Sweden)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOZYME; NITROGEN; PEPTIDOGLYCAN; AMMONIUM DERIVATIVE;

BACTERIUM; NITROGEN CYCLE; NITROGEN FIXATION; PEPTIDE;

ANAMMOX BACTERIUM; ARTICLE; ATMOSPHERE; BACTERIAL CELL WALL; BACTERIAL GENOME; CELL DIVISION; KUENENIA STUTTGARTIENSIS; NONHUMAN; TRANSMISSION ELECTRON MICROSCOPY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANAEROBIC GROWTH; CELL WALL; CHEMISTRY; CLASSIFICATION; CYTOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PLANCTOMYCETALES;

BACTERIA (MICROORGANISMS); CANDIDATUS KUENENIA STUTTGARTIENSIS; NEGIBACTERIA; PLANCTOMYCETES;

AMMONIUM COMPOUNDS; ANAEROBIOSIS; CELL WALL; OXIDATION-REDUCTION; PEPTIDOGLYCAN; PLANCTOMYCETALES;

EID: 84929180060     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7878     Document Type: Article

References (43)

1. Vollmer, W., Blanot, D. & De Pedro, M. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32, 149-167 (2008).
2. Wagner, M. & Horn, M. The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr. Opin. Biotechnol. 17, 241-249 (2006).
3. König, E., Schlesner, H. & Hirsch, P. Cell wall studies on budding bacteria of the Planctomyces/Pasteuria group and on a Prosthecomicrobium sp. Arch. Microbiol. 138, 200-205 (1984).
4. Liesack, W., König, H., Schlesner, H. & Hirsch, P. Chemical composition of the peptidoglycan-free cell envelopes of budding bacteria of the Pirella/ Planctomyces group. Arch. Microbiol. 145, 361-366 (1986).
5. Cayrou, C., Raoult, D. & Drancourt, M. Broad-spectrum antibiotic resisitance of Planctomycetes organisms determined by Etest. J. Antimicrob. Chemother. 65, 2119-2122 (2010).
6. McCoy, A. J. & Maurelli, A. T. Building the invisible wall: updating the chlamydial peptidoglycan anomaly. Trends Microbiol. 14, 70-77 (2006).
7. Pilhofer, M. et al. Discovery of chlamydial peptidoglycan reveals bacteria with murein sacculi but without FtsZ. Nat. Commun. 4, 2856 (2013).
8. Liechti, G. W. et al. A new metabolic cell-wall labelling method reveals peptidoglycan in Chlamydia trachomatis. Nature 506, 507-510 (2014).
9. Jogler, C. et al. Planctomycetes comparative genomics: identification of proteins likely involved in morphogenesis, cell division and signal transduction. J. Bacteriol. 194, 6419-6430 (2012).
10. Guo, M. et al. Genomic evolution of 11 type strains within family Planctomycetaceae. PLoS ONE 9, e86752 (2014).
11. Lindsay, M. R. et al. Cell compartmentalization in planctomycetes: novel types of structural organization for the bacterial cell. Arch. Microbiol. 175, 413-429 (2001).
12. Sagulenko, E. et al. Structural studies of Planctomycete Gemmata obscuriglobus support cell compartmentalization in a bacterium. PLoS ONE 9, e91344 (2014).
13. Speth, D. R., van Teeseling, M. C. F. & Jetten, M. S. M. Genomic analysis indicates the presence of an asymmetric bilayer outer membrane in Planctomycetes and Verrucomicrobia. Front. Microbiol. 3, 304 (2012).
14. Devos, D. P. Re-interpretation of the evidence for the PVC cell plan supports a Gram-negative origin. Antonie Van Leeuwenhoek 105, 271-274 (2014).
15. Devos, D. P. PVC bacteria: variation of, but not exception to, the Gramnegative cell plan. Trends Microbiol. 22, 14-20 (2014).
16. Fuerst, J. A. The planctomycetes: emerging models for microbial ecology, evolution and cell biology. Microbiology. 141, 1493-1506 (1995).
17. Fuerst, J. A. & Sagulenko, E. Keys to eukaryality: planctomycetes and ancestral evolution of cellular complexity. Front. Microbiol. 3, 167 (2012).
18. Forterre, P. & Gribaldo, S. Bacteria with a eukaryotic touch: a glimpse of ancient evolution? Proc. Natl Acad. Sci. USA 107, 12739-12740 (2010).
19. Devos, D. P. & Reynaud, E. G. Intermediate steps. Science 330, 1187-1188 (2010).
20. Santarella-Mellwig, R., Pruggnaller, S., Roos, N., Mattaj, I. W. & Devos, D. P. Three-dimensional reconstruction of bacteria with a complex endomembrane system. PLoS Biol. 11, e1001565 (2013).
21. Kartal, B. et al. Molecular mechanisms of anaerobic ammonium oxidation. Nature 479, 127-130 (2011).
22. Francis, C. A., Beman, J. M. & Kuypers, M. M. M. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archeal ammonia oxidation. ISME J. 1, 19-27 (2007).
23. Kartal, B., Kuenen, J. G. & van Loosdrecht, M. C. M. Sewage treatment with anammox. Science 328, 702-703 (2010).
24. van Niftrik, L. et al. Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria. J. Struct. Biol. 161, 401-410 (2008).
25. Neumann, S. et al. Isolation and characterization of a prokaryotic cell organelle from the anammox bacterium Kuenenia stuttgartiensis. Mol. Microbiol. 94, 794-802 (2014).
26. van Teeseling, M. C. F. et al. 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 (2014).
27. van Niftrik, L. et al. Cell division ring, a new cell division protein and vertical inheritance of a bacterial organelle in anammox planctomycetes. Mol. Microbiol. 73, 1009-1019 (2009).
28. Neumann, S., van Teeseling, M. C. F. & van Niftrik, L. in Planctomycetes: Cell Structure, Origins and Biology. (ed Fuerst, J. A.) 89-123 (Humana Press/ Springer, 2013).
29. Lombard, V., Golaconda Ramula, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490-D495 (2014).
30. Hu, Z., van Alen, T., Jetten, M. S. M. & Kartal, B. Lysozyme and Penicillin inhibit the growth of anaerobic ammonium-oxidizing Planctomycetes. Appl. Environ. Microbiol. 79, 7763-7769 (2013).
31. Al-Amoudi, A. et al. Cryo-electron microscopy of vitreous sections. EMBO J. 23, 3583-3588 (2004).
32. Johnson, L. N. & Phillips, D. C. Structure of some crystalline lysozymeinhibitor complexes determined by X-ray analysis at 6 Angstrom resolution. Nature 206, 761-763 (1965).
33. De Pedro, M. A., Quintela, J. C., Höltje, J.-V. & Schwarz, H. Murein segregation in Escherichia coli. J. Bacteriol. 179, 2823-2834 (1997).
34. Strous, M. et al. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790-794 (2006).
35. Cava, F., de Pedro, M. A., Lam, H., Davis, B. M. & Waldor, M. K. Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids. EMBO J. 30, 3442-3453 (2011).
36. Kuru, E. et al. In situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angew. Chem. Int. Ed. Engl. 51, 12519-12523 (2012).
37. Siegrist, M. S. et al. D-amino acid chemical reporters reveal peptidoglycan dynamics of an intracellular pathogen. ACS Chem. Biol. 8, 500-505 (2013).
38. Gordon, E. et al. Crystal structure of UDP-N-acetylmuramoyl-L-alanyl-Dglutamate: meso-Diaminopimelate ligase from Escherichia coli. J. Biol. Chem. 276, 10999-11006 (2000).
39. Jeske, O. et al. Planctomycetes do possess a peptidoglycan cell wall. Nat. Commun. 6: 7116 doi: 10.1038/ncomms8116 (2015).
40. Kartal, B., Geerts, W. & Jetten, M. S. M. in Methods in Enzymology Vol. 486 (ed Klotz, M. G.) 89-109 (Academic, 2011).
41. van de Graaf, A. A., de Bruijn, P., Robertson, L. A., Jetten, M. S. M. & Kuenen, J. G. Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology (UK) 142, 2187-2196 (1996).
42. Schmid, M. et al. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst. Appl. Microbiol. 23, 93-106 (2000).
43. Neef, A., Amann, R. I., Schlesner, H. & Schleifer, K. H. Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16 S rRNA-targeted probes. Microbiology. 144, 3257-3266 (1998).