Lack of a Surface Layer in Tannerella Forsythia Mutants Deficient in the Type IX Secretion System

Overview

Journal Microbiology (Reading)

Specialty Microbiology

Date 2014 Jul 16

PMID 25023245

Citations 35

Authors

Yuka Narita

Keiko Sato

Hideharu Yukitake

Mikio Shoji

Daisuke Nakane

Keiji Nagano

Fuminobu Yoshimura

Mariko Naito

Koji Nakayama

Affiliations

Soon will be listed here.

Abstract

Tannerella forsythia, a Gram-negative anaerobic bacterium, is an important pathogen in periodontal disease. This bacterium possesses genes encoding all known components of the type IX secretion system (T9SS). T. forsythia mutants deficient in genes orthologous to the T9SS-encoding genes porK, porT and sov were constructed. All porK, porT and sov single mutants lacked the surface layer (S-layer) and expressed less-glycosylated versions of the S-layer glycoproteins TfsA and TfsB. In addition, these mutants exhibited decreased haemagglutination and increased biofilm formation. Comparison of the proteins secreted by the porK and WT strains revealed that the secretion of several proteins containing C-terminal domain (CTD)-like sequences is dependent on the porK gene. These results indicate that the T9SS is functional in T. forsythia and contributes to the translocation of CTD proteins to the cell surface or into the extracellular milieu.

Citing Articles

The type IX secretion system: Insights into its function and connection to glycosylation in .

Song W, Zhuang X, Tan Y, Qi Q, Lu X Eng Microbiol. 2024; 2(3):100038.

PMID: 39629027 PMC: 11611037. DOI: 10.1016/j.engmic.2022.100038.

Identification of nanaomycin A and its analogs by a newly established screening method for functional inhibitors of the type IX secretion system in Porphyromonas gingivalis.

Sasaki Y, Matsuo T, Watanabe Y, Iwatsuki M, Inahashi Y, Nishida S J Antibiot (Tokyo). 2024; 78(2):90-105.

PMID: 39578618 DOI: 10.1038/s41429-024-00790-8.

Ecological, beneficial, and pathogenic functions of the Type 9 Secretion System.

Rocha S, Shah D, Shrivastava A Microb Biotechnol. 2024; 17(6):e14516.

PMID: 38924452 PMC: 11205867. DOI: 10.1111/1751-7915.14516.

Structural and functional insights into the C-terminal signal domain of the Bacteroidetes type-IX secretion system.

Mizgalska D, Rodriguez-Banqueri A, Veillard F, Ksiazek M, Goulas T, Guevara T Open Biol. 2024; 14(6):230448.

PMID: 38862016 PMC: 11285876. DOI: 10.1098/rsob.230448.

Screening and characterization of aptamers recognizing the periodontal pathogen Tannerella forsythia.

Mizgalska D, Malicki S, Golda A, Chruscicka-Smaga B, Potempa J FEBS Open Bio. 2024; 14(3):498-504.

PMID: 38308430 PMC: 10909966. DOI: 10.1002/2211-5463.13772.

References

Potempa J, Sroka A, Imamura T, Travis J . Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes. Curr Protein Pept Sci. 2003; 4(6):397-407. DOI: 10.2174/1389203033487036. View

Veith P, OBrien-Simpson N, Tan Y, Djatmiko D, Dashper S, Reynolds E . Outer membrane proteome and antigens of Tannerella forsythia. J Proteome Res. 2009; 8(9):4279-92. DOI: 10.1021/pr900372c. View

Chagnot C, Zorgani M, Astruc T, Desvaux M . Proteinaceous determinants of surface colonization in bacteria: bacterial adhesion and biofilm formation from a protein secretion perspective. Front Microbiol. 2013; 4:303. PMC: 3796261. DOI: 10.3389/fmicb.2013.00303. View

Sharma A . Virulence mechanisms of Tannerella forsythia. Periodontol 2000. 2010; 54(1):106-16. PMC: 2934765. DOI: 10.1111/j.1600-0757.2009.00332.x. View

Takemoto T, Kurihara H, Dahlen G . Characterization of Bacteroides forsythus isolates. J Clin Microbiol. 1997; 35(6):1378-81. PMC: 229752. DOI: 10.1128/jcm.35.6.1378-1381.1997. View

O-Brien-Simpson N, Veith P, Dashper S, Reynolds E . Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr Protein Pept Sci. 2003; 4(6):409-26. DOI: 10.2174/1389203033487009. View

Nakane D, Sato K, Wada H, McBride M, Nakayama K . Helical flow of surface protein required for bacterial gliding motility. Proc Natl Acad Sci U S A. 2013; 110(27):11145-50. PMC: 3704026. DOI: 10.1073/pnas.1219753110. View

Posch G, Pabst M, Brecker L, Altmann F, Messner P, Schaffer C . Characterization and scope of S-layer protein O-glycosylation in Tannerella forsythia. J Biol Chem. 2011; 286(44):38714-38724. PMC: 3207478. DOI: 10.1074/jbc.M111.284893. View

Fletcher C, Coyne M, Villa O, Chatzidaki-Livanis M, Comstock L . A general O-glycosylation system important to the physiology of a major human intestinal symbiont. Cell. 2009; 137(2):321-31. PMC: 2772059. DOI: 10.1016/j.cell.2009.02.041. View

10.

Holt S, Ebersole J . Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000. 2005; 38:72-122. DOI: 10.1111/j.1600-0757.2005.00113.x. View

11.

Sekot G, Posch G, Oh Y, Zayni S, Mayer H, Pum D . Analysis of the cell surface layer ultrastructure of the oral pathogen Tannerella forsythia. Arch Microbiol. 2012; 194(6):525-39. PMC: 3354324. DOI: 10.1007/s00203-012-0792-3. View

12.

Sleytr U, Beveridge T . Bacterial S-layers. Trends Microbiol. 1999; 7(6):253-60. DOI: 10.1016/s0966-842x(99)01513-9. View

13.

Posch G, Pabst M, Neumann L, Coyne M, Altmann F, Messner P . "Cross-glycosylation" of proteins in Bacteroidales species. Glycobiology. 2012; 23(5):568-77. PMC: 3608352. DOI: 10.1093/glycob/cws172. View

14.

OToole G, Kolter R . Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol. 1998; 28(3):449-61. DOI: 10.1046/j.1365-2958.1998.00797.x. View

15.

McBride M, Zhu Y . Gliding motility and Por secretion system genes are widespread among members of the phylum bacteroidetes. J Bacteriol. 2012; 195(2):270-8. PMC: 3553832. DOI: 10.1128/JB.01962-12. View

16.

Boot H, Pouwels P . Expression, secretion and antigenic variation of bacterial S-layer proteins. Mol Microbiol. 1996; 21(6):1117-23. DOI: 10.1046/j.1365-2958.1996.711442.x. View

17.

Shoji M, Yukitake H, Sato K, Shibata Y, Naito M, Aduse-Opoku J . Identification of an O-antigen chain length regulator, WzzP, in Porphyromonas gingivalis. Microbiologyopen. 2013; 2(3):383-401. PMC: 3684754. DOI: 10.1002/mbo3.84. View

18.

Shimotahira N, Oogai Y, Kawada-Matsuo M, Yamada S, Fukutsuji K, Nagano K . The surface layer of Tannerella forsythia contributes to serum resistance and oral bacterial coaggregation. Infect Immun. 2013; 81(4):1198-206. PMC: 3639587. DOI: 10.1128/IAI.00983-12. View

19.

Karim A, Kulczycka M, Kantyka T, Dubin G, Jabaiah A, Daugherty P . A novel matrix metalloprotease-like enzyme (karilysin) of the periodontal pathogen Tannerella forsythia ATCC 43037. Biol Chem. 2009; 391(1):105-17. PMC: 2884989. DOI: 10.1515/BC.2010.009. View

20.

Yoneda M, Hirofuji T, Anan H, Matsumoto A, Hamachi T, Nakayama K . Mixed infection of Porphyromonas gingivalis and Bacteroides forsythus in a murine abscess model: involvement of gingipains in a synergistic effect. J Periodontal Res. 2001; 36(4):237-43. DOI: 10.1034/j.1600-0765.2001.036004237.x. View