Comparative genomics reveals distinct host-interacting traits of three major human-associated propionibacteria

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Mak, Tim N ^a   Schmid, Monika ^b   Brzuszkiewicz, Elzbieta ^c   Zeng, Guanghong ^a   Meyer, Rikke ^a   Sfanos, Karen S ^d   Brinkmann, Volker ^b   Meyer, Thomas F ^b   Brüggemann, Holger ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cutaneous propionibacteria; Exopolysaccharide; Pilus pili; Propionibacterium acnes; Propionibacterium avidum; Propionibacterium granulosum; Surfome

Indexed keywords

ADHESIN; CHRISTIE ATKINS MUNCH PETERSEN FACTOR 1; CHRISTIE ATKINS MUNCH PETERSEN FACTOR 2; DSA1 PROTEIN; DSA2 PROTEIN; ENDOGLYCOCERAMIDASE; EXOPOLYSACCHARIDE; HYALURONATE LYASE; HYALURONIDASE; LINOLEIC ACID ISOMERASE; MEMBRANE PROTEIN; SH3 DOMAIN CONTAINING LIPOPROTEIN; SIALIDASE; SORTASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL DNA;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL GENE; BACTERIAL GENOME; BACTERIUM PILUS; CELL SURFACE; CORYNEBACTERIUM AVIDUM; ELECTRON MICROSCOPY; GENE IDENTIFICATION; GENOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROPIONIBACTERIUM; PROPIONIBACTERIUM ACNES; PROPIONIBACTERIUM GRANULOSUM; PROTEOMICS; SPECIES DIFFERENCE; COMPARATIVE GENOMIC HYBRIDIZATION; CYTOLOGY; DNA SEQUENCE; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; MICROBIOLOGY; SCANNING ELECTRON MICROSCOPY; SKIN; ULTRASTRUCTURE;

PROPIONIBACTERIUM ACNES; PROPIONIBACTERIUM AVIDUM; PROPIONIBACTERIUM GRANULOSUM;

COMPARATIVE GENOMIC HYBRIDIZATION; DNA, BACTERIAL; GENOME, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, SCANNING; PROPIONIBACTERIUM; SEQUENCE ANALYSIS, DNA; SKIN;

EID: 84884308290     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-640     Document Type: Article

References (51)

1. Poonam, Pophaly SD, Tomar SK, De S, Singh R. Multifaceted attributes of dairy propionibacteria: a review. World J Microbiol Biotechnol 2012, 28:3081-3095. 10.1007/s11274-012-1117-z, 22806746.
2. Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol 2011, 9:244-253. 10.1038/nrmicro2537, 3535073, 21407241.
3. Sharon I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF. Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res 2013, 23:111-120. 10.1101/gr.142315.112, 3530670, 22936250.
4. Furukawa A, Uchida K, Ishige Y, Ishige I, Kobayashi I, Takemura T, Yokoyama T, Iwai K, Watanabe K, Shimizu S, Ishida N, Suzuki Y, Suzuki T, Yamada T, Ito T, Eishi Y. Characterization of Propionibacterium acnes isolates from sarcoid and non-sarcoid tissues with special reference to cell invasiveness, serotype, and trigger factor gene polymorphism. Microb Pathog 2009, 46:80-87. 10.1016/j.micpath.2008.10.013, 19049821.
5. Alexeyev OA, Marklund I, Shannon B, Golovleva I, Olsson J, Andersson C, Eriksson I, Cohen R, Elgh F. Direct visualization of Propionibacterium acnes in prostate tissue by multicolor fluorescent in situ hybridization assay. J Clin Microbiol 2007, 45:3721-3728. 10.1128/JCM.01543-07, 2168516, 17881550.
6. Fassi Fehri L, Mak TN, Laube B, Brinkmann V, Ogilvie LA, Mollenkopf H, Lein M, Schmidt T, Meyer TF, Brüggemann H. Prevalence of Propionibacterium acnes in diseased prostates and its inflammatory and transforming activity on prostate epithelial cells. Int J Med Microbiol 2011, 301:69-78. 10.1016/j.ijmm.2010.08.014, 20943438.
7. McGinley KJ, Webster GF, Leyden JJ. Regional variations of cutaneous propionibacteria. Appl Environ Microbiol 1978, 35:62-66. 242779, 623473.
8. Dessinioti C, Katsambas AD. The role of Propionibacterium acnes in acne pathogenesis: facts and controversies. Clin Dermatol 2010, 28:2-7. 10.1016/j.clindermatol.2009.03.012, 20082942.
9. Perry A, Lambert P. Propionibacterium acnes: infection beyond the skin. Expert Rev Anti Infect Ther 2011, 9:1149-1156. 10.1586/eri.11.137, 22114965.
10. Mak TN, Yu SH, De Marzo AM, Brüggemann H, Sfanos KS. Multilocus sequence typing (MLST) analysis of Propionibacterium acnes isolates from radical prostatectomy specimens. Prostate 2013, 73:770-777. 10.1002/pros.22621, 23184509.
11. Panagea S, Corkill JE, Hershman MJ, Parry CM. Breast abscess caused by Propionibacterium avidum following breast reduction surgery: case report and review of the literature. J Infect 2005, 51:e253-e255. 10.1016/j.jinf.2005.04.005, 15908006.
12. Vohra A, Saiz E, Chan J, Castro J, Amaro R, Barkin J. Splenic abscess caused by Propionibacterium avidum as a complication of cardiac catheterization. Clin Infect Dis 1998, 26:770-771. 10.1086/517127, 9524868.
13. Janvier F, Delacour H, Larréché S, Abdalla S, Aubert P, Mérens A. Abdominal wall and intra-peritoneal abscess by Propionibacterium avidum as a complication of abdominal parietoplasty. Pathol Biol 2013, in press.
14. Armstrong RW, Wuerflein RD. Endocarditis due to Propionibacterium granulosum. Clin Infect Dis 1996, 23:1178-1179. 10.1093/clinids/23.5.1178, 8922825.
15. Eishi Y, Suga M, Ishige I, Kobayashi D, Yamada T, Takemura T, Takizawa T, Koike M, Kudoh S, Costabel U, Guzman J, Rizzato G, Gambacorta M, du Bois R, Nicholson AG, Sharma OP, Ando M. Quantitative analysis of mycobacterial and propionibacterial DNA in lymph nodes of Japanese and European patients with sarcoidosis. J Clin Microbiol 2002, 40:198-204. 10.1128/JCM.40.1.198-204.2002, 120089, 11773116.
16. Brüggemann H, Henne A, Hoster F, Liesegang H, Wiezer A, Strittmatter A, Hujer S, Dürre P, Gottschalk G. The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 2004, 305:671-673. 10.1126/science.1100330, 15286373.
17. Valanne S, McDowell A, Ramage G, Tunney MM, Einarsson GG, O'Hagan S, Wisdom GB, Fairley D, Bhatia A, Maisonneuve JF, Lodes M, Persing DH, Patrick S. CAMP factor homologues in Propionibacterium acnes: a new protein family differentially expressed by types I and II. Microbiology 2005, 151:1369-1379. 10.1099/mic.0.27788-0, 15870447.
18. Lodes MJ, Secrist H, Benson DR, Jen S, Shanebeck KD, Guderian J, Maisonneuve JF, Bhatia A, Persing D, Patrick S, Skeiky YA. Variable expression of immunoreactive surface proteins of Propionibacterium acnes. Microbiology 2006, 152:3667-3681. 10.1099/mic.0.29219-0, 17159220.
19. McDowell A, Gao A, Barnard E, Fink C, Murray PI, Dowson CG, Nagy I, Lambert PA, Patrick S. A novel multilocus sequence typing scheme for the opportunistic pathogen Propionibacterium acnes and characterization of type I cell surface-associated antigens. Microbiology 2011, 157:1990-2003. 10.1099/mic.0.049676-0, 21511767.
20. Nakatsuji T, Liu YT, Huang CP, Zouboulis CC, Gallo RL, Huang CM. Vaccination targeting a surface sialidase of P. acnes: implication for new treatment of acne vulgaris. PLoS One 2008, 3:e1551. 10.1371/journal.pone.0001551, 2212713, 18253498.
21. Brzuszkiewicz E, Weiner J, Wollherr A, Thürmer A, Hüpeden J, Lomholt HB, Kilian M, Gottschalk G, Daniel R, Mollenkopf HJ, Meyer TF, Brüggemann H. Comparative genomics and transcriptomics of Propionibacterium acnes. PLoS One 2011, 6:e21581. 10.1371/journal.pone.0021581, 3124536, 21738717.
22. Ordögh L, Hunyadkürti J, Vörös A, Horváth B, Szucs A, Urbán E, Kereszt A, Kondorosi E, Nagy I. Complete genome sequence of Propionibacterium avidum strain 44067, isolated from a human skin abscess. Genome Announc 2013, in press.
23. Holland C, Mak TN, Zimny-Arndt U, Schmid M, Meyer TF, Jungblut PR, Brüggemann H. Proteomic identification of secreted proteins of Propionibacterium acnes. BMC Microbiol 2010, 10:230. 10.1186/1471-2180-10-230, 3224659, 20799957.
24. Lo CW, Lai YK, Liu YT, Gallo RL, Huang CM. Staphylococcus aureus hijacks a skin commensal to intensify its virulence: immunization targeting β-hemolysin and CAMP factor. J Invest Dermatol 2011, 131:401-409. 10.1038/jid.2010.319, 3057116, 21085191.
25. Nakatsuji T, Tang DC, Zhang L, Gallo RL, Huang CM. Propionibacterium acnes CAMP factor and host acid sphingomyelinase contribute to bacterial virulence: potential targets for inflammatory acne treatment. PLoS One 2011, 6:e14797. 10.1371/journal.pone.0014797, 3075254, 21533261.
26. Yamane K, Nambu T, Yamanaka T, Mashimo C, Sugimori C, Leung KP, Fukushima H. Complete genome sequence of Rothia mucilaginosa DY-18: a clinical isolate with dense meshwork-like structures from a persistent apical periodontitis lesion. Sequencing 2010, 2010:457236.
27. Rogers EA, Das A, Ton-That H. Adhesion by pathogenic corynebacteria. Adv Exp Med Biol 2011, 715:91-103. 10.1007/978-94-007-0940-9_6, 21557059.
28. Doro F, Liberatori S, Rodríguez-Ortega MJ, Rinaudo CD, Rosini R, Mora M, Scarselli M, Altindis E, D'Aurizio R, Stella M, Margarit I, Maione D, Telford JL, Norais N, Grandi G. Surfome analysis as a fast track to vaccine discovery: identification of a novel protective antigen for Group B Streptococcus hyper virulent strain COH1. Mol Cell Proteomics 2009, 8:1728-1737. 10.1074/mcp.M800486-MCP200, 2709197, 19401597.
29. Boels IC, Beerthuyzen MM, Kosters MH, Van Kaauwen MP, Kleerebezem M, De Vos WM. Identification and functional characterization of the Lactococcus lactis rfb operon, required for dTDP-rhamnose biosynthesis. J Bacteriol 2004, 186:1239-1248. 10.1128/JB.186.5.1239-1248.2004, 344400, 14973085.
30. Annunziato PW, Wright LF, Vann WF, Silver RP. Nucleotide sequence and genetic analysis of the neuD and neuB genes in region 2 of the polysialic acid gene cluster of Escherichia coli K1. J Bacteriol 1995, 177:312-319. 176593, 7814319.
31. Freeman BC, Chen C, Beattie GA. Identification of the trehalose biosynthetic loci of Pseudomonas syringae and their contribution to fitness in the phyllosphere. Environ Microbiol 2010, 12:1486-1497.
32. Ryder C, Byrd M, Wozniak DJ. Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr Opin Microbiol 2007, 10:644-648. 10.1016/j.mib.2007.09.010, 2176169, 17981495.
33. Alhede M, Bjarnsholt T, Jensen P, Phipps RK, Moser C, Christophersen L, Christensen LD, van Gennip M, Parsek M, Høiby N, Rasmussen TB, Givskov M. Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiology 2009, 155:3500-3508. 10.1099/mic.0.031443-0, 19643762.
34. Byrd MS, Pang B, Mishra M, Swords WE, Wozniak DJ. The Pseudomonas aeruginosa exopolysaccharide Psl facilitates surface adherence and NF-kappaB activation in A549 cells. MBio 2010, 1.
35. Cabrera M, Gil I, Rodriguez D. Growth of Propionibacterium acnes strains on semisynthetic medium; antigenic polysaccharide production. Zentralbl Mikrobiol 1983, 138:391-395.
36. Cummins CS, White RH. Isolation, identification, and synthesis of 2,3-diamino-2,3-dideoxyglucuronic acid: a component of Propionibacterium acnes cell wall polysaccharide. J Bacteriol 1983, 153:1388-1393. 221789, 6826525.
37. Squaiella CC, Longhini AL, Braga EG, Mussalem JS, Ananias RZ, Yendo TM, Straus AH, Toledo MS, Takahashi HK, Hirata IY, Longo-Maugéri IM. Modulation of the type I hypersensitivity late phase reaction to OVA by Propionibacterium acnes-soluble polysaccharide. Immunol Lett 2008, 121:157-166. 10.1016/j.imlet.2008.10.005, 19014971.
38. Whale GA, Sutcliffe IC, Morrisson AR, Pretswell EL, Emmison N. Purification and characterisation of lipoglycan macroamphiphiles from Propionibacterium acnes. Antonie Van Leeuwenhoek 2004, 86:77-85.
39. Mandlik A, Swierczynski A, Das A, Ton-That H. Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol Microbiol 2007, 64:111-124. 10.1111/j.1365-2958.2007.05630.x, 2844904, 17376076.
40. Schmaler M, Jann NJ, Ferracin F, Landolt LZ, Biswas L, Götz F, Landmann R. Lipoproteins in Staphylococcus aureus mediate inflammation by TLR2 and iron-dependent growth in vivo. J Immunol 2009, 182:7110-7118. 10.4049/jimmunol.0804292, 19454708.
41. Kim J. Review of the innate immune response in acne vulgaris: activation of Toll-like receptor 2 in acne triggers inflammatory cytokine responses. Dermatology 2005, 211:193-198. 10.1159/000087011, 16205063.
42. Kim J, Ochoa MT, Krutzik SR, Takeuchi O, Uematsu S, Legaspi AJ, Brightbill HD, Holland D, Cunliffe WJ, Akira S, Sieling PA, Godowski PJ, Modlin RL. Activation of toll-like receptor 2 in acne triggers inflammatory cytokine responses. J Immunol 2002, 169:1535-1541.
43. Sakaguchi K, Okino N, Sueyoshi N, Izu H, Ito M. Cloning and expression of gene encoding a novel endoglycoceramidase of Rhodococcus sp. strain C9. J Biochem 2000, 128:145-152. 10.1093/oxfordjournals.jbchem.a022725, 10876169.
44. Sörensen M, Mak TN, Hurwitz R, Ogilvie LA, Mollenkopf HJ, Meyer TF, Brüggemann H. Mutagenesis of Propionibacterium acnes and analysis of two CAMP factor knock-out mutants. J Microbiol Methods 2010, 83:211-216. 10.1016/j.mimet.2010.09.008, 20850482.
45. Liu PF, Nakatsuji T, Zhu W, Gallo RL, Huang CM. Passive immunoprotection targeting a secreted CAMP factor of Propionibacterium acnes as a novel immunotherapeutic for acne vulgaris. Vaccine 2011, 29:3230-3238. 10.1016/j.vaccine.2011.02.036, 3388602, 21354482.
46. Liu GY, Nizet V. Extracellular virulence factors of group B Streptococci. Front Biosci 2004, 9:1794-1802. 10.2741/1296, 14977587.
47. Christie R, Atkins NE, Munch-Petersen E. A note on a lytic phenomenon shown by group B streptococci. Aust J Exp Biol 1944, 22:197-200.
48. Angiuoli SV, Gussman A, Klimke W, Cochrane G, Field D, Garrity G, Kodira CD, Kyrpides N, Madupu R, Markowitz V, Tatusova T, Thomson N, White O. Toward an online repository of Standard Operating Procedures (SOPs) for (meta) genomic annotation. OMICS 2008, 12:137-141. 10.1089/omi.2008.0017, 3196215, 18416670.
49. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. ACT: the Artemis Comparison Tool. Bioinformatics 2005, 21:3422-3423. 10.1093/bioinformatics/bti553, 15976072.
50. Langille MG, Brinkman FS. Island viewer: an integrated interface for computational identification and visualization of genomic islands. Bioinformatics 2009, 25:664-665. 10.1093/bioinformatics/btp030, 2647836, 19151094.
51. Komoriya K, Shibano N, Higano T, Azuma N, Yamaguchi S, Aizawa S. Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol Microbiol 1999, 34:767-779. 10.1046/j.1365-2958.1999.01639.x, 10564516.