Relatedness within the Family Pasteurellaceae as Determined by Genetic Transformation

Albritton, William L.; Setlow, Jane K.; Thomas, Myrtle L.; Sottnek, F O

doi:10.1099/00207713-36-1-103

Cited by 25 publications

(15 citation statements)

References 11 publications

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“…Note that total CFU for D7S was ϳ5 ϫ 10 8 and that for D7S-smooth was ϳ5 ϫ 10 9 . (1). This suggests that the two genomes may share the same uptake sequence.…”

Section: Identification Of Naturally Transformable a Actinomycetemcomentioning

confidence: 90%

Natural Transformation and DNA Uptake Signal Sequences in Actinobacillus actinomycetemcomitans

et al. 2002

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Actinobacillus actinomycetemcomitans is a member of the family Pasteurellaceae and a major causative agent of periodontitis. While several genera from this family are known to be competent for transformation, A. actinomycetemcomitans has yet to be fully characterized. Here we show that the competence of A. actinomycetemcomitans is remarkably similar to that of Haemophilus influenzae. In addition to having a similar frequency of transformation as H. influenzae, A. actinomycetemcomitans competence could also be induced at least 100-fold by cyclic AMP, suggesting that, as in H. influenzae, at least some competence genes are regulated by catabolite repression. Even more intriguing was the discovery of a putative A. actinomycetemcomitans DNA uptake signal sequence (USS) virtually identical to the USS of H. influenzae. Moreover, we provide evidence that this sequence functions in the same capacity as that from H. influenzae; the sequence appears to be required and sufficient for DNA uptake in a variety of assays. Finally, we have taken advantage of this system to develop a simple, highly efficient competence-based method for generating site-directed mutations in the wild-type fimbriated A. actinomycetemcomitans.Actinobacillus actinomycetemcomitans, a gram-negative, facultative, nonmotile coccobacillus, is a major causative agent of localized juvenile periodontitis and other forms of chronic periodontitis (36). Moreover, A. actinomycetemcomitans is transmissible among family members and may persist for long periods (4). A. actinomycetemcomitans can also spread from the oral cavity, causing a variety of nonoral infections (31, 36). Indeed, the genomic DNA of A. actinomycetemcomitans was identified in atherosclerotic lesions (14), suggesting a possible role of this bacterium in cardiovascular disease.Some A. actinomycetemcomitans strains are known to be naturally competent for transformation (23,30). In many bacteria, transformation occurs when cells enter the state of competence. This enables them to take up DNA and incorporate it into their genomes (8, 18). In the best-studied naturally competent gram-negative bacteria, Haemophilus influenzae, Haemophilus parainfluenzae, Neisseria gonorrhoeae, and Neisseria meningitidis, double-stranded donor DNA fragments are preferentially bound into a DNase-resistant state if they contain a short recognition sequence abundant in their own genomes, the uptake signal sequence (USS) (10, 11). Although uptake has been demonstrated elsewhere for A. actinomycetemcomitans in two preliminary studies (23, 30), a quantitative analysis has yet to be performed. In particular, neither of these studies examined any of the requirements for the induction of competence. Nor was a specific DNA uptake sequence requirement for transformation investigated.Because the function of the USS has been assumed to be exclusion of DNAs from other species, different genera were expected to use different USSs. However, only USSs from the very distantly related genera Haemophilus and Neisseria have been characteriz...

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“…Note that total CFU for D7S was ϳ5 ϫ 10 8 and that for D7S-smooth was ϳ5 ϫ 10 9 . (1). This suggests that the two genomes may share the same uptake sequence.…”

Section: Identification Of Naturally Transformable a Actinomycetemcomentioning

confidence: 90%

Natural Transformation and DNA Uptake Signal Sequences in Actinobacillus actinomycetemcomitans

et al. 2002

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“…The explanation is not simply that closely related bacteria have been incorrectly assigned to different genera. Although the phylogeny of the Pasteurellaceae is not well resolved, the average DNA sequence identity between identifiable homologs of H. influenzae and P. multocida is comparable to that between Escherichia coli and Salmonella typhimurium [71% (34)], low enough to substantially limit recombination with incoming foreign DNA (21). Not only are the USS consensus sequences in different genera identical but also most individual USS elements are shared, indicating they have been inherited from the common ancestor of these species.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary stability of DNA uptake signal sequences in the Pasteurellaceae

Bakkali

Chen

Lee

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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The DNA-uptake signal sequence (USS) of the bacterium Haemophilus influenzae is highly over-represented in its genome (1,471 copies of the core sequence AAGTGCGGT), and DNA fragments containing USS are preferentially taken up by competent cells. Because this bias favors uptake of conspecific DNA, USSs are often considered a kind of mate recognition system in bacteria, acting as species-specific barriers against uptake of unrelated DNA. However, the H. influenzae USS is highly over-represented in the genomes of three otherwise-divergent Pasteurellaceae species (Pasteurella multocida, Haemophilus somnus, and Actinobacillus actinomycetemcomitans, 927, 1,205, and 1,760 copies, respectively), suggesting that USSs do not always limit exchange. USSs in all these genomes are mainly in coding regions and show no orientation bias around the chromosome, weakening proposed USS functions in transcription termination and chromosome replication. Alignment of homologous genes was used to determine evolutionary relationships between individual USSs. Most H. influenzae USSs were found to have perfect or imperfect homologs (USS at the same location) in at least one other species, and most USSs in the other species had perfect or imperfect homologs in H. influenzae. These homologies suggest that the use of a common USS is due to inheritance of the USS-based uptake system from a common ancestor of the Pasteurellaceae, and it indicates that individual USSs can be evolutionarily stable elements of their genomes. The pattern is consistent with a molecular drive model of USS evolution, with new USSs arising by mutation and preferentially spread to new genomes by the biased DNA-uptake system. natural competence ͉ transformation ͉ Actinobacillus ͉ Haemophilus ͉ Pasteurella

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“…Albritton et al (1984Albritton et al ( , 1986 observed that the genomic DNA from Haemophilus parainfluenzae, Haemophilus aphrophilus, Haemophilus paraphrophilus, Pasteurella pneumotrophica, Pasteurella multocida and A. actinomycetemcomitans competed for homospecific transformation in H. influenzae. Hong & Dewhirst (2002) found preliminary evidence for the frequent occurrences of the USS in Haemophilus parahaemolyticus, H. parainfluenzae, Actinobacillus suis, P. multocida, Pasteurella canis and several additional Pasteurella species.…”

Section: Discussionmentioning

confidence: 99%

Genomic distribution and functions of uptake signal sequences in Actinobacillus actinomycetemcomitans

et al. 2006

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Actinobacillus actinomycetemcomitans is naturally competent for transformation, with a transformation system similar to that of Haemophilus influenzae that preferentially takes up DNA bearing uptake signal sequences (USS) with the same 9-base USS core. This study examined the function of the extended 29-base USS, which comprises a highly conserved 1st region (containing the 9-base core) and 2nd and 3rd semi-conserved AT-rich regions, in transformation of A. actinomycetemcomitans. Transformation frequency was not affected by either location (in middle or at 59 end) or quantity (one or two) of USS in donor DNA. Relative transformation efficiencies (in comparison to the positive control) were 28-67 % for linear DNA with single-base mutations in the USS 1st region, and 47 % and 73 %, respectively, for linear DNA with USS that contained either a non-consensus 2nd or a non-consensus 3rd region. Plasmids with a stand-alone 1st or a stand-alone 2nd-3rd region exhibited 21 % and 6 % relative transformation efficiencies, respectively. It was also noted that A. actinomycetemcomitans and H. influenzae were similar in the frequencies and distribution patterns of USS in their genomes. In conclusion, all three regions of the extended 29-base USS are required for optimum transformation in A. actinomycetemcomitans.

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Relatedness within the Family Pasteurellaceae as Determined by Genetic Transformation

Cited by 25 publications

References 11 publications

Natural Transformation and DNA Uptake Signal Sequences in Actinobacillus actinomycetemcomitans

Natural Transformation and DNA Uptake Signal Sequences in Actinobacillus actinomycetemcomitans

Evolutionary stability of DNA uptake signal sequences in the Pasteurellaceae

Genomic distribution and functions of uptake signal sequences in Actinobacillus actinomycetemcomitans

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