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Synthesis and function of Actinomyces naeslundii T14V type 1 fimbriae require the expression of additional fimbria-associated genes

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Yeung, M K, Ragsdale, P A·1997·Infection and Immunity
DOI 10.1128/iai.65.7.2629-2639.1997PMC PMC175372
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Abstract

The nucleotide sequence of the chromosomal DNA flanking the Actinomyces naeslundii (formerly A. viscosus) T14V type 1 fimbrial structural subunit gene (fimP) was determined. Six open reading frames (ORFs), in the order 5' ORF3, ORF2, ORF1,fimP, ORF4, ORF5, ORF6 3', were identified. ORF1 encoded a protein of 408 amino acid residues (Mr = 39,270) and had significant sequence homology with the A. naeslundii T14V type 1 and A. naeslundii WVU45 type 2 fimbrial structural subunits. An in-frame fusion of ORF1 to the malE gene of the expression vector, pMAL-c2, yielded a protein that was immunostained with antibodies raised against the maltose binding protein and A. naeslundii T14V whole bacteria. Digestion of the fusion protein with factor Xa released a protein (apparent molecular mass of 34 kDa) that was immunostained only with the antibody directed against A. naeslundii T14V whole bacterial cells. Integration plasmids carrying a kanamycin resistance gene (kan) that was used to substitute for ORF1 or for DNA fragments internal to the coding region of the other five ORFs were used to transform A. naeslundii T14V. Neither type 1 fimbriae nor the 65-kDa fimbrial structural subunit was detected in mutants obtained by allelic replacement of ORF1 or ORF2. Mutants obtained by allelic replacement of ORF3 or ORF4 expressed only the 65-kDa fimbrial structural subunit. These mutants did not bind, in vitro, to proline-rich proteins that serve as the receptors for Actinomyces type 1 fimbriae. In contrast, a mutant in which the integration plasmid DNA had been inserted at a site close to the carboxyl terminus of ORF6 expressed type 1 fimbriae and had adherence properties similar to those observed in the wild-type strain. These results demonstrate the existence of additional genes near fimP that are likely to be involved in the synthesis and function of cell surface fimbriae of A. naeslundii T14V.

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  • Disruption of orf4 caused FimP and Orf1 subunits to accumulate in the envelope and prevented fimbrial structure assembly.

    “A similar result was observed when orf4 was disrupted; FimP and Orf1 subunits accumulated in the envelope, and the fimbrial structure was not assembled [59].”

    From Protein sorting to the cell wall envelope of Gram-positive bacteria (2004) · cites this paper as [59]

    In “Potential role of the putative ORFs in fimbria synthesis and function” (page not provided), the ORF4-disrupted mutant expressed the 65-kDa fimbrial structural subunit; the Discussion reports that it lacked assembled fimbriae. The paper does not report accumulation of FimP or Orf1 in the envelope, and says that only the 65-kDa subunit was detected in this mutant. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • orf1 and fimP encode protein products whose primary sequences display striking similarity to the topogenic sequences of cell wall-anchored surface proteins of S. aureus.

    “orf1 and fimP encode protein products whose primary sequences display striking similarity to the topogenic sequences of cell wall-anchored surface proteins of S. aureus.”

    From Protein sorting to the cell wall envelope of Gram-positive bacteria (2004) · cites this paper as [59]

    In ‘Analysis of DNA sequences flanking fimP’ (page not available), the paper reports high similarity between the ORF1 product and the fimP-encoded fimbrial subunit, including a membrane-anchoring LPXTG sequence common to several gram-positive surface proteins. It does not identify S. aureus proteins as the comparison or report striking similarity to their topogenic sequences specifically. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • An operon encompassing seven open reading frames was identified with the gene order (5' to 3' coding sequence): orf3-orf2-orf1-fimP-orf4-orf5-orf6.

    “An operon encompassing seven open reading frames was identified with the gene order (5V to 3V coding sequence): orf3-orf2-orf1-fimP-orf4-orf5-orf6.”

    From Protein sorting to the cell wall envelope of Gram-positive bacteria (2004) · cites this paper as [59]

    In ‘Analysis of DNA sequences flanking fimP’ (page not available), the paper identifies six putative ORFs in the same orientation as fimP; the plasmid descriptions in Table 1 place ORF3, ORF2 and ORF1 upstream of fimP, while the sequence description places ORF4–ORF6 downstream. This supports the seven-ORF arrangement, but the cited passages do not establish that all seven form one operon. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Studies by Yeung and Ragsdale revealed chromosomal regions that are involved in the biogenesis of A. naeslundii T14V type I fimbriae.

    “Studies by Yeung and Ragsdale [59] revealed chromosomal regions that are involved in the biogenesis of A. naeslundii T14V type I fimbriae.”

    From Protein sorting to the cell wall envelope of Gram-positive bacteria (2004) · cites this paper as [59]

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Authors
Yeung, M. K., & Ragsdale, P. A.
Affiliations
The University of Texas at San Antonio Health Science Center (US)
Venue
Infection and Immunity
Publisher
American Society for Microbiology
Published
1997-07
Volume
65
Issue
7
Pages
2629-2639
ISSN
  • 0019-9567 (ISSN-L)
  • 1098-5522
DOI
10.1128/iai.65.7.2629-2639.1997
PMC
PMC175372
OpenAlex
W1893249720
Cited by
62
References
56
Citations by year
2024: 1 · 2022: 1 · 2020: 3 · 2018: 1 · 2016: 2 · 2015: 1 · 2014: 5 · 2013: 1 · 2012: 3
FWCI
0.95
Type
journal article
Language
en
Open access
Licence
journals.asm.org/non-commercial-tdm-license (tdm)
Locations
  • Infection and Immunity (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (5r01de011102-09)
  • National Institute of Dental and Craniofacial Research (DE-11102)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Health Sciences › Medicine › Pharmacology › Microbial Natural Products and Biosynthesis
Keywords
Actinomyces naeslundii, type 1 fimbriae, FIMP, ORF1, ORF2, ORF3, ORF4, ORF6, bacterial adhesion, proline-rich proteins, allelic replacement
MeSH terms
Amino Acid Sequence, Bacterial Proteins, Base Sequence, DNA, Bacterial, Genes, Bacterial, Kanamycin Resistance, Molecular Sequence Data, Fimbriae, Bacterial, Open Reading Frames, Actinomyces viscosus

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