Common Cell Shape Evolution of Two Nasopharyngeal Pathogens
The nasopharynx hosts an important microbial community that comprises some well-known pathogens such as Neisseria meningitidis and Moraxella catarrhalis. In some circumstances, it also represents the portal of entry of systemic infections such as septicemia and meningitis, or infections of the respiratory system, middle ear, eye, central nervous system and joints of humans, caused by N. meningitidis and M. catarrhalis, respectively. In this article, we demonstrated that both bacteria underwent a similar cell shape evolution that resulted in a transition from a bacillus to a coccus. This was consequently accompanied by a change, similar for both bacteria, in the structure of the PG, the major bacterial cell shape determinant and also a strongly recognized molecule by the immune system. In our efforts in understanding the evolutionary events that led to the cell shape transition in N. meningitidis, we identified two genetic deletion events required for the shape transition, i.e. of yacF (zapD) and the cell elongation machinery. Furthermore, we delineated the importance of YacF (ZapD) in the coordination of the cell elongation and division. Finally, we suggest that this transition was selected to reduce the cell surface sensible to immune attacks and to redistribute surface appendages, such as pili, to acquire new properties of cell adhesion or movement necessary for the proper colonization of the nasopharynx.
Vyšlo v časopise:
Common Cell Shape Evolution of Two Nasopharyngeal Pathogens. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005338
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005338
Souhrn
The nasopharynx hosts an important microbial community that comprises some well-known pathogens such as Neisseria meningitidis and Moraxella catarrhalis. In some circumstances, it also represents the portal of entry of systemic infections such as septicemia and meningitis, or infections of the respiratory system, middle ear, eye, central nervous system and joints of humans, caused by N. meningitidis and M. catarrhalis, respectively. In this article, we demonstrated that both bacteria underwent a similar cell shape evolution that resulted in a transition from a bacillus to a coccus. This was consequently accompanied by a change, similar for both bacteria, in the structure of the PG, the major bacterial cell shape determinant and also a strongly recognized molecule by the immune system. In our efforts in understanding the evolutionary events that led to the cell shape transition in N. meningitidis, we identified two genetic deletion events required for the shape transition, i.e. of yacF (zapD) and the cell elongation machinery. Furthermore, we delineated the importance of YacF (ZapD) in the coordination of the cell elongation and division. Finally, we suggest that this transition was selected to reduce the cell surface sensible to immune attacks and to redistribute surface appendages, such as pili, to acquire new properties of cell adhesion or movement necessary for the proper colonization of the nasopharynx.
Zdroje
1. Girardin SE, Boneca IG, Carneiro LA, Antignac A, Jehanno M, Viala J, et al. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science. 2003;300(5625):1584–7. Epub 2003/06/07. 12791997
2. Girardin SE, Travassos LH, Herve M, Blanot D, Boneca IG, Philpott DJ, et al. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem. 2003;278(43):41702–8. Epub 2003/07/23. 12871942
3. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem. 2003;278(11):8869–72. Epub 2003/01/16. 12527755
4. Inohara N, Ogura Y, Fontalba A, Gutierrez O, Pons F, Crespo J, et al. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J Biol Chem. 2003;278(8):5509–12. Epub 2003/01/07. C200673200 [pii]. 12514169
5. Holtje JV. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev. 1998;62(1):181–203. Epub 1998/04/08. 9529891
6. Tamames J, Gonzalez-Moreno M, Mingorance J, Valencia A, Vicente M. Bringing gene order into bacterial shape. Trends Genet. 2001;17(3):124–6. Epub 2001/02/28. 11226588
7. Young KD. Bacterial shape. Mol Microbiol. 2003;49(3):571–80. Epub 2003/08/14. 12914007
8. Cava F, de Pedro MA. Peptidoglycan plasticity in bacteria: emerging variability of the murein sacculus and their associated biological functions. Curr Opin Microbiol. 2014;18:46–53. doi: 10.1016/j.mib.2014.01.004 24607990
9. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev. 2008;32(2):234–58. Epub 2008/02/13. doi: 10.1111/j.1574-6976.2008.00105.x 18266856
10. Typas A, Banzhaf M, Gross CA, Vollmer W. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nature reviews Microbiology. 2012;10(2):123–36. Epub 2011/12/29.
11. Erickson HP, Anderson DE, Osawa M. FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev. 2011;74(4):504–28. Epub 2010/12/02.
12. Liu G, Tang CM, Exley RM. Non-pathogenic Neisseria: members of an abundant, multi-habitat, diverse genus. Microbiology. 2015. Epub 2015/03/31.
13. Adeolu M, Gupta RS. Phylogenomics and molecular signatures for the order Neisseriales: proposal for division of the order Neisseriales into the emended family Neisseriaceae and Chromobacteriaceae fam. nov. Antonie van Leeuwenhoek. 2013;104(1):1–24. Epub 2013/04/12. doi: 10.1007/s10482-013-9920-6 23575986
14. Guibourdenche M, Popoff MY, Riou JY. Deoxyribonucleic acid relatedness among Neisseria gonorrhoeae, N. meningitidis, N. lactamica, N. cinerea and "Neisseria polysaccharea". Ann Inst Pasteur Microbiol. 1986;137B(2):177–85. Epub 1986/09/01. 3120761
15. Best GK, Durham NN. Vancomycin adsorption to Bacillus subtilis cell walls. Arch Biochem Biophys. 1965;111(3):685–91. Epub 1965/09/01. 4955576
16. Veyrier F, Pletzer D, Turenne C, Behr MA. Phylogenetic detection of horizontal gene transfer during the step-wise genesis of Mycobacterium tuberculosis. BMC Evol Biol. 2009;9:196. Epub 2009/08/12. doi: 10.1186/1471-2148-9-196 19664275
17. Durand-Heredia J, Rivkin E, Fan G, Morales J, Janakiraman A. Identification of ZapD as a cell division factor that promotes the assembly of FtsZ in Escherichia coli. J Bacteriol. 194(12):3189–98. Epub 2012/04/17. doi: 10.1128/JB.00176-12 22505682
18. Bovre K, Holten E. Neisseria elongata sp.nov., a rod-shaped member of the genus Neisseria. Re-evaluation of cell shape as a criterion in classification. J Gen Microbiol. 1970;60(1):67–75. Epub 1970/01/01. 5488467
19. Zarantonelli ML, Skoczynska A, Antignac A, El Ghachi M, Deghmane AE, Szatanik M, et al. Penicillin resistance compromises Nod1-dependent proinflammatory activity and virulence fitness of neisseria meningitidis. Cell Host Microbe. 2013;13(6):735–45. Epub 2013/06/19. doi: 10.1016/j.chom.2013.04.016 23768497
20. Werts C, le Bourhis L, Liu J, Magalhaes JG, Carneiro LA, Fritz JH, et al. Nod1 and Nod2 induce CCL5/RANTES through the NF-kappaB pathway. European journal of immunology. 2007;37(9):2499–508. Epub 2007/08/21. 17705131
21. Wheeler R. VFJ, Werts C., Boneca I.G. Peptidoglycan and Nod Receptor. Glycoscience: Biology and Medicine. 2015:737–49.
22. Guilhen C, Taha MK, Veyrier FJ. Role of transition metal exporters in virulence: the example of Neisseria meningitidis. Front Cell Infect Microbiol. 2013;3:102. Epub 2014/01/07. doi: 10.3389/fcimb.2013.00102 24392357
23. Francis F, Ramirez-Arcos S, Salimnia H, Victor C, Dillon JR. Organization and transcription of the division cell wall (dcw) cluster in Neisseria gonorrhoeae. Gene. 2000;251(2):141–51. Epub 2000/07/06. 10876091
24. van der Ploeg R, Verheul J, Vischer NO, Alexeeva S, Hoogendoorn E, Postma M, et al. Colocalization and interaction between elongasome and divisome during a preparative cell division phase in Escherichia coli. Mol Microbiol. 2013;87(5):1074–87. Epub 2013/02/08. doi: 10.1111/mmi.12150 23387922
25. Young KD. Bacterial morphology: why have different shapes? Curr Opin Microbiol. 2007;10(6):596–600. Epub 2007/11/06. 17981076
26. Wagner JK, Setayeshgar S, Sharon LA, Reilly JP, Brun YV. A nutrient uptake role for bacterial cell envelope extensions. Proc Natl Acad Sci U S A. 2006;103(31):11772–7. Epub 2006/07/25. 16861302
27. Justice SS, Hunstad DA, Cegelski L, Hultgren SJ. Morphological plasticity as a bacterial survival strategy. Nat Rev Microbiol. 2008;6(2):162–8. Epub 2007/12/25. 18157153
28. Young KD. The selective value of bacterial shape. Microbiol Mol Biol Rev. 2006;70(3):660–703. Epub 2006/09/09. 16959965
29. Dalia AB, Weiser JN. Minimization of bacterial size allows for complement evasion and is overcome by the agglutinating effect of antibody. Cell Host Microbe. 2011;10(5):486–96. Epub 2011/11/22. doi: 10.1016/j.chom.2011.09.009 22100164
30. Veyrier FJ, Williams AH, Mesnage S, Schmitt C, Taha MK, Boneca IG. De-O-acetylation of peptidoglycan regulates glycan chain extension and affects in vivo survival of Neisseria meningitidis. Mol Microbiol. 2013;87(5):1100–12. Epub 2013/02/05. doi: 10.1111/mmi.12153 23373517
31. Guan R, Brown PH, Swaminathan CP, Roychowdhury A, Boons GJ, Mariuzza RA. Crystal structure of human peptidoglycan recognition protein I alpha bound to a muramyl pentapeptide from Gram-positive bacteria. Protein Sci. 2006;15(5):1199–206. Epub 2006/04/28. 16641493
32. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. Type VI secretion delivers bacteriolytic effectors to target cells. Nature. 2011;475(7356):343–7. Epub 2011/07/22. doi: 10.1038/nature10244 21776080
33. Ieva R, Alaimo C, Delany I, Spohn G, Rappuoli R, Scarlato V. CrgA is an inducible LysR-type regulator of Neisseria meningitidis, acting both as a repressor and as an activator of gene transcription. J Bacteriol. 2005;187(10):3421–30. Epub 2005/05/04. 15866928
34. Veyrier FJ, Boneca IG, Cellier MF, Taha MK. A novel metal transporter mediating manganese export (MntX) regulates the Mn to Fe intracellular ratio and Neisseria meningitidis virulence. PLoS Pathog. 2011;7(9):e1002261. Epub 2011/10/08. doi: 10.1371/journal.ppat.1002261 21980287
35. Glauner B. Separation and quantification of muropeptides with high-performance liquid chromatography. Analytical biochemistry. 1988;172(2):451–64. Epub 1988/08/01. 3056100
36. Antignac A, Rousselle JC, Namane A, Labigne A, Taha MK, Boneca IG. Detailed structural analysis of the peptidoglycan of the human pathogen Neisseria meningitidis. J Biol Chem. 2003;278(34):31521–8. Epub 2003/06/12. 12799361
37. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004;5:113. Epub 2004/08/21. doi: 10.1186/1471-2105-5-113 15318951
38. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. Epub 2004/03/23. 15034147
39. 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. Epub 2010/07/16. doi: 10.1186/1471-2148-10-210 20626897
40. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74. Epub 2014/11/06. doi: 10.1093/molbev/msu300 25371430
41. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402. Epub 1997/09/01. 9254694
42. Yao J, Lin H, Doddapaneni H, Civerolo EL. nWayComp: a genome-wide sequence comparison tool for multiple strains/species of phylogenetically related microorganisms. In silico biology. 2007;7(2):195–200. Epub 2007/08/11. 17688445
43. von Mering C, Huynen M, Jaeggi D, Schmidt S, Bork P, Snel B. STRING: a database of predicted functional associations between proteins. Nucleic Acids Res. 2003;31(1):258–61. Epub 2003/01/10. 12519996
44. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000;28(1):33–6. Epub 1999/12/11. 10592175
45. Alyahya SA, Alexander R, Costa T, Henriques AO, Emonet T, Jacobs-Wagner C. RodZ, a component of the bacterial core morphogenic apparatus. Proc Natl Acad Sci U S A. 2009;106(4):1239–44. Epub 2009/01/24. doi: 10.1073/pnas.0810794106 19164570
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 7
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Functional Constraint Profiling of a Viral Protein Reveals Discordance of Evolutionary Conservation and Functionality
- Reversible Oxidation of a Conserved Methionine in the Nuclear Export Sequence Determines Subcellular Distribution and Activity of the Fungal Nitrate Regulator NirA
- Modeling Implicates in Nephropathy: Evidence for Dominant Negative Effects and Epistasis under Anemic Stress
- Nutritional Control of DNA Replication Initiation through the Proteolysis and Regulated Translation of DnaA