Translational frameshifting in the control of transposition in bacteria

Chandler, Michaël; Fayet, Olivier

doi:10.1111/j.1365-2958.1993.tb01140.x

Cited by 212 publications

(157 citation statements)

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“…Firstly, five IS elements (13)(14)(25)(26)(41)(42) exhibited characteristic features of the IS3 family, which is widespread in L. lactis. They contained two consecutive and partially overlapping reading frames that could generate a fusion protein by programmed translational frameshifting (Chandler & Fayet, 1993). Secondly, eight IS elements, four of them truncated (ORFs 4, 6, 18, 28, 32, 39, 54 and 65) belonged to the IS6 family, which is also widespread in L. lactis.…”

Section: Is Elements and Transposasesmentioning

confidence: 99%

Sequence analysis of the mobilizable lactococcal plasmid pGdh442 encoding glutamate dehydrogenase activity

2007

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A novel plasmid named pGdh442 had previously been isolated from a plant Lactococcus lactis strain. This plasmid encodes two interesting properties with applications in the dairy industry: a glutamate dehydrogenase activity that stimulates amino acid conversion to aroma compounds, and cadmium/zinc resistance that can be used as a selectable marker. Moreover, this plasmid can be transferred naturally to other strains, but appears to be incompatible with certain other lactococcal plasmids. During this study, the complete sequence of pGdh442 (68 319 bp) was determined and analysed. This plasmid contains 67 ORFs that include 20 IS elements that may have mediated transfer events between L. lactis and other genera living in the same biotope, such as Streptococcus, Pediococcus and Lactobacillus. Even though it is a low-copy-number plasmid, it is relatively stable due to a theta replication mode and the presence of two genes involved in its maintenance system. However, pGdh442 is incompatible with pSK08-derived protease/lactose plasmids because both possess the same replication and partition system. pGdh442 is not self-transmissible, but can be naturally transmitted via mobilization by conjugative elements carried by the chromosome or by other plasmids, such as the 712-type sex factor, which is widely distributed in L. lactis. In addition to several genes already found on other L. lactis plasmids, such as the oligopeptide transport and utilization genes, pGdh442 also carries several genes not yet identified in L. lactis. Finally, it does not carry genes that would trigger concern over its presence in human food. INTRODUCTIONLactococcus lactis is a lactic acid bacterium (LAB) widely used as a starter culture for the production of various fermented dairy products. Although this bacterium is commonly found in milk, it is also naturally present on plants and on parts of the bodies of cows (Nomura et al., 2006;Salama et al., 1995;Teuber, 1995). Typically, Lactococcus strains possess an abundance of plasmid DNA. Many large L. lactis plasmids are self-transmissible or mobilizable by conjugative elements carried by the chromosome or plasmids of the host strain (Gasson et al., 1995). Through their natural transfer, these plasmids increase the probability of the gene moving between bacteria, and enable strains to acquire a wide variety of new genetic traits. They thus endow their hosts with many traits which offer a selective advantage to colonize specific biotopes. For example, the majority of dairy strains have adapted to growth in milk by acquiring plasmids that encode lactose catabolism (De Vos & Gasson, 1989), casein degradation (Kok, 1990), citrate utilization (Kempler & McKay, 1979) and oligopeptide transport (Yu et al., 1996). In addition, strains isolated from plant and animal environments, which contain a wide variety of cytotoxic compounds, have developed appropriate protection mechanisms (Putman et al., 2000), such as multidrug resistance, nisin resistance and heavy metal resistance (Dougherty et al., 1998;Liu et al.,...

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Section: Is Elements and Transposasesmentioning

confidence: 99%

Sequence analysis of the mobilizable lactococcal plasmid pGdh442 encoding glutamate dehydrogenase activity

2007

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“…Transposition of IS911 has been investigated in some detail (Ton Hoang et al, 1997 and references therein), and a cell-free system allowing transposasemediated intramolecular recombination has been developed (Polard et al, 1996). One feature of IS911 and other members of the IS3 family is that the transposase is generated by a programmed ¹1 translational frameshift from two consecutive open reading frames (see Chandler and Fayet, 1993). One of these, orfA, encodes a helixturn-helix motif, which might confer the ability to recognize and bind to the ends of the element, while the second, orf B, encodes a DD(35)E motif known to be part of the catalytic centre of many enzymes of this type (see Polard and Chandler, 1995a;Grindley and Leschziner, 1995;Rice et al, 1996;Andrake and Skalka, 1996).…”

Section: Introductionmentioning

confidence: 99%

IS911‐mediated intramolecular transposition is naturally temperature sensitive

Haren

Bétermier

Polard

et al. 1997

Molecular Microbiology

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SummaryIt is shown here that the bacterial insertion sequence IS911 exhibits a temperature-sensitive transposition phenotype. Previous results have demonstrated that elevated levels of the IS911 transposase OrfAB generate significant quantities of a figure-eight form, created by cleavage and circularization of one of the transposon strands, and of an excised circular form, in which both transposon strands have been circularized. We show here that the level of both types of molecule observed in vivo was greatly reduced at 42ЊC compared with 37ЊC. On the other hand, reducing the temperature to 30ЊC resulted in a significant increase in production. Transposition activity at this temperature was sufficiently high to permit detection in vivo of an excised circular form of a defective single IS911 chromosomal copy when OrfAB is supplied in trans. A similar temperature-activity profile is observed for a cell-free reaction that uses partially purified OrfAB and generates the figure-eight form uniquely. Moreover, two point mutants of OrfAB were obtained, which render the reactions partially temperature resistant both in vivo and in vitro. These results suggest that some property of transposase itself is sensitive to elevated temperatures.

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“…Although the integration mechanism of this prophage-like element is unknown, it presumably involves a protein of the integrase family (required for the phage DNA integration into the host chromosome through site-specific recombination). It should be pointed out that the expression of many of the transposases that catalyze the insertion of IS (Insertion Sequence) copies into new chromosomal locations is controlled by translational frameshifting (Chandler and Fayet 1993). Because of the numerous frameshift points, this B. subtilis region probably contains traces of the phage integrase gene.…”

Section: Detection Of Several Authentic Frameshiftsmentioning

confidence: 99%

“…In the case of E. coli, at least two programmed translational frameshifts are well documented: (1) The expression of the prfB gene (encoding the peptide release factor 2) involves an autogenous regulatory loop in which expression of the gene by translational frameshifting is negatively regulated by the gene product (Craigen et al 1985); (2) a frameshift in the dnaX gene (encoding DNA polymerase III) allows the expression of alternative enzyme activities, as a result of the production of the and ␥ subunits, respectively (Blinkowa and Walker 1990;Flower and McHenry 1990;Tsuchihashi and Kornberg 1990). Several programmed translational frameshifts have been identified in bacteriophages and bacterial insertion sequences (Chandler and Fayet 1993). Analysis of the +1 and ‫1מ‬ frameshifting systems identifies three paradigms: (1) doublet decoding of aminoacyl-tRNA; (2) out-of-frame binding of aminoacyl-tRNA; and (3) slippage of peptidyl-tRNA (Farabaugh 1996).…”

Section: Cold Spring Harbor Laboratory Press On May 11 2018 -Publishmentioning

confidence: 99%

Detecting and Analyzing DNA Sequencing Errors: Toward a Higher Quality of the Bacillus subtilis Genome Sequence

Médigue

Rose²,

Viari³

et al. 1999

Genome Res.

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During the determination of a DNA sequence, the introduction of artifactual frameshifts and/or in-frame stop codons in putative genes can lead to misprediction of gene products. Detection of such errors with a method based on protein similarity matching is only possible when related sequences are available in databases. Here, we present a method to detect frameshift errors in DNA sequences that is based on the intrinsic properties of the coding sequences. It combines the results of two analyses, the search for translational initiation/termination sites and the prediction of coding regions. This method was used to screen the complete Bacillus subtilis genome sequence and the regions flanking putative errors were resequenced for verification. This procedure allowed us to correct the sequence and to analyze in detail the nature of the errors. Interestingly, in several cases in-frame termination codons or frameshifts were not sequencing errors but confirmed to be present in the chromosome, indicating that the genes are either nonfunctional (pseudogenes) or subject to regulatory processes such as programmed translational frameshifts. The method can be used for checking the quality of the sequences produced by any prokaryotic genome sequencing project.Despite progress in DNA-sequencing techniques, currently used protocols result in different sources of errors. High-performance automated sequencing machines have been developed and substantially reduce the introduction of human errors. However, systematic error due to gel compression for example, still remain difficult to avoid. Most of these errors involve singlebase substitutions and have limited effect on the overall quality of the final sequence. Sometimes, they can generate artifactual insertions and deletions of bases (indels) that produce frameshifts in deduced coding regions, and thereby cause errors in predicted protein sequences and compromise the interpretation of the chromosome sequence.Several computational tools have been developed to avoid many of the pitfalls of error accumulation during DNA sequencing (White et al. 1993;Richterich 1998). Various related methods address the question of detecting frameshift errors in DNA sequence data. They are based on the comparison of the conceptual translations of the DNA sequences in all six reading frames, to each sequence of a protein databank (Posfai and Roberts 1992;Claverie 1993;Guan and Uberbacher 1996;Brown et al. 1998). Frameshifts are thus inferred from the comparison of the protein sequences, and consequently, error detection relies on the presence of closely related protein sequences in databanks. To overcome this drawback, Fichant and Quentin (1995) have developed a tool, called FSED (Frameshift Errors Detection), which is based on discrimination of the coding frame from the two other frames. Their method rests on the result of a correspondence analysis performed on the nonoverlapping tri-or hexa-nucleotides in the three frames of a coding sequence (CDS). Because, by construction, this algorithm only work...

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Translational frameshifting in the control of transposition in bacteria

Cited by 212 publications

References 30 publications

Sequence analysis of the mobilizable lactococcal plasmid pGdh442 encoding glutamate dehydrogenase activity

Sequence analysis of the mobilizable lactococcal plasmid pGdh442 encoding glutamate dehydrogenase activity

IS911‐mediated intramolecular transposition is naturally temperature sensitive

Detecting and Analyzing DNA Sequencing Errors: Toward a Higher Quality of the Bacillus subtilis Genome Sequence

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