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New implications on genomic adaptation derived from the Helicobacter pylori genome comparison.

Lara-Ramírez EE, Segura-Cabrera A, Guo X, Yu G, García-Pérez CA, Rodríguez-Pérez MA - PLoS ONE (2011)

Bottom Line: Helicobacter pylori has a reduced genome and lives in a tough environment for long-term persistence.Hence, pseudogenes could be a reservoir of adaptation materials and the HPN mutations could be favorable to H. pylori adaptation, leading to HPN accumulation on the genomes, which corresponds to a special feature of Helicobacter species: extremely high HPN composition of genome.Our research demonstrated that both genome content and structure of H. pylori have been highly adapted to its particular life style.

View Article: PubMed Central - PubMed

Affiliation: Centro de Biotecnología Genómica, Instituto Politécnico Nacional, Reynosa, México.

ABSTRACT

Background: Helicobacter pylori has a reduced genome and lives in a tough environment for long-term persistence. It evolved with its particular characteristics for biological adaptation. Because several H. pylori genome sequences are available, comparative analysis could help to better understand genomic adaptation of this particular bacterium.

Principal findings: We analyzed nine H. pylori genomes with emphasis on microevolution from a different perspective. Inversion was an important factor to shape the genome structure. Illegitimate recombination not only led to genomic inversion but also inverted fragment duplication, both of which contributed to the creation of new genes and gene family, and further, homological recombination contributed to events of inversion. Based on the information of genomic rearrangement, the first genome scaffold structure of H. pylori last common ancestor was produced. The core genome consists of 1186 genes, of which 22 genes could particularly adapt to human stomach niche. H. pylori contains high proportion of pseudogenes whose genesis was principally caused by homopolynucleotide (HPN) mutations. Such mutations are reversible and facilitate the control of gene expression through the change of DNA structure. The reversible mutations and a quasi-panmictic feature could allow such genes or gene fragments frequently transferred within or between populations. Hence, pseudogenes could be a reservoir of adaptation materials and the HPN mutations could be favorable to H. pylori adaptation, leading to HPN accumulation on the genomes, which corresponds to a special feature of Helicobacter species: extremely high HPN composition of genome.

Conclusion: Our research demonstrated that both genome content and structure of H. pylori have been highly adapted to its particular life style.

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Related in: MedlinePlus

Sketch map of genomic structure in an inversion.Each arrow-formed block represents a gene open reading frame (ORF). The solid block indicates a pair of inverted repeats. The density from pale to dark shows the nucleotide identity degree of various regions between these two inverted repeats in which the dark region means identical. Small black lines indicate other genomic sequences. The letters within the blocks are the names of genes.
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pone-0017300-g004: Sketch map of genomic structure in an inversion.Each arrow-formed block represents a gene open reading frame (ORF). The solid block indicates a pair of inverted repeats. The density from pale to dark shows the nucleotide identity degree of various regions between these two inverted repeats in which the dark region means identical. Small black lines indicate other genomic sequences. The letters within the blocks are the names of genes.

Mentions: The first introduction of inverted sequence can lead to the formation of a family of outer membrane proteins. In strain 26695, there are a pair of inverted repeat fragments, 2144 bp including HP0722 (omp16) on the sequence strand and 2163 bp including HP0725 (omp17) on the complementary strand. These two ORFs encode outer membrane protein with 1187 bp identical at the last half part of gene. The two genes, ansB (L-asparaginase II) and dcuA (anaerobic C4-dicarboxylate transporter) are located between them. The organization from different H. pylori strains are shown as Figure 4. The order of ansB and dcuA on the genomes shows, with no doubt, the presence of inversion in some strains between the inverted sequences. The strains B38 (HELPY_0642), Shi470 (HPSH_03230), and 51 (KHP_0602) have only one homolog at the similar position to HP0722 and the following genes are in the same order as dcuA-ansB. So the fragment including HP0722 is the original and the sequence containing HP0725 was the duplication while dcuA-ansB should thus be the original gene order in contrast to the inverted form as ansB-dcuA, as occurred in strains 26695, 52 and P12. In strains P12 and 52, the whole fragments of repeats are almost identical within a genome (only 1 bp deleted in one fragment in P12), which could be the consequence of recent duplication. Phylogenic analysis showed that the inverted repeat sequences at two sites within a genome have been diversified in some strains (Figure 4). The identical sequences are located at the last half part of gene but the first half part, close to the inversion junction, have been changed to great extent in various regions (Figure 5), indicating that the recombination had been involved in this region and thus a family of proteins were created. The diversification of paralogs after duplication could be similar to the case of homA and homB shown in the recent report [49]. On the other hand, the borders of inversion are the inverted repeats, as the case of 5S rDNA inversion mentioned above, indicating that these inversions could be realized by homologous recombination through inverted repeats. We further compared the junction sequences of the inverted repeats and found that the exterior border sequences (16–21 bp) of the junctions could be the same from different strains but never in the same strain (more than 70% of identity) even though the repeats within a genome are identical, suggesting that the inverted repeat could be introduced by illegitimate recombination. To this sense, the process of inversion could be the first introduction of the inverted repeat to a new site by illegitimate recombination and then the occurrence of inversion between two inverted repeats. It can also explain why the strains with inverted repeats (strains J99, G27, and HPAG1) still kept the same gene order between the inverted regions as the strains without the inverted repeats (strains 51, Shi470 and B38): only occurred the inverted duplication and the inversion did not happen yet. Of course, an extreme case could occur that the inversions happen in even number of times.


New implications on genomic adaptation derived from the Helicobacter pylori genome comparison.

Lara-Ramírez EE, Segura-Cabrera A, Guo X, Yu G, García-Pérez CA, Rodríguez-Pérez MA - PLoS ONE (2011)

Sketch map of genomic structure in an inversion.Each arrow-formed block represents a gene open reading frame (ORF). The solid block indicates a pair of inverted repeats. The density from pale to dark shows the nucleotide identity degree of various regions between these two inverted repeats in which the dark region means identical. Small black lines indicate other genomic sequences. The letters within the blocks are the names of genes.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3046158&req=5

pone-0017300-g004: Sketch map of genomic structure in an inversion.Each arrow-formed block represents a gene open reading frame (ORF). The solid block indicates a pair of inverted repeats. The density from pale to dark shows the nucleotide identity degree of various regions between these two inverted repeats in which the dark region means identical. Small black lines indicate other genomic sequences. The letters within the blocks are the names of genes.
Mentions: The first introduction of inverted sequence can lead to the formation of a family of outer membrane proteins. In strain 26695, there are a pair of inverted repeat fragments, 2144 bp including HP0722 (omp16) on the sequence strand and 2163 bp including HP0725 (omp17) on the complementary strand. These two ORFs encode outer membrane protein with 1187 bp identical at the last half part of gene. The two genes, ansB (L-asparaginase II) and dcuA (anaerobic C4-dicarboxylate transporter) are located between them. The organization from different H. pylori strains are shown as Figure 4. The order of ansB and dcuA on the genomes shows, with no doubt, the presence of inversion in some strains between the inverted sequences. The strains B38 (HELPY_0642), Shi470 (HPSH_03230), and 51 (KHP_0602) have only one homolog at the similar position to HP0722 and the following genes are in the same order as dcuA-ansB. So the fragment including HP0722 is the original and the sequence containing HP0725 was the duplication while dcuA-ansB should thus be the original gene order in contrast to the inverted form as ansB-dcuA, as occurred in strains 26695, 52 and P12. In strains P12 and 52, the whole fragments of repeats are almost identical within a genome (only 1 bp deleted in one fragment in P12), which could be the consequence of recent duplication. Phylogenic analysis showed that the inverted repeat sequences at two sites within a genome have been diversified in some strains (Figure 4). The identical sequences are located at the last half part of gene but the first half part, close to the inversion junction, have been changed to great extent in various regions (Figure 5), indicating that the recombination had been involved in this region and thus a family of proteins were created. The diversification of paralogs after duplication could be similar to the case of homA and homB shown in the recent report [49]. On the other hand, the borders of inversion are the inverted repeats, as the case of 5S rDNA inversion mentioned above, indicating that these inversions could be realized by homologous recombination through inverted repeats. We further compared the junction sequences of the inverted repeats and found that the exterior border sequences (16–21 bp) of the junctions could be the same from different strains but never in the same strain (more than 70% of identity) even though the repeats within a genome are identical, suggesting that the inverted repeat could be introduced by illegitimate recombination. To this sense, the process of inversion could be the first introduction of the inverted repeat to a new site by illegitimate recombination and then the occurrence of inversion between two inverted repeats. It can also explain why the strains with inverted repeats (strains J99, G27, and HPAG1) still kept the same gene order between the inverted regions as the strains without the inverted repeats (strains 51, Shi470 and B38): only occurred the inverted duplication and the inversion did not happen yet. Of course, an extreme case could occur that the inversions happen in even number of times.

Bottom Line: Helicobacter pylori has a reduced genome and lives in a tough environment for long-term persistence.Hence, pseudogenes could be a reservoir of adaptation materials and the HPN mutations could be favorable to H. pylori adaptation, leading to HPN accumulation on the genomes, which corresponds to a special feature of Helicobacter species: extremely high HPN composition of genome.Our research demonstrated that both genome content and structure of H. pylori have been highly adapted to its particular life style.

View Article: PubMed Central - PubMed

Affiliation: Centro de Biotecnología Genómica, Instituto Politécnico Nacional, Reynosa, México.

ABSTRACT

Background: Helicobacter pylori has a reduced genome and lives in a tough environment for long-term persistence. It evolved with its particular characteristics for biological adaptation. Because several H. pylori genome sequences are available, comparative analysis could help to better understand genomic adaptation of this particular bacterium.

Principal findings: We analyzed nine H. pylori genomes with emphasis on microevolution from a different perspective. Inversion was an important factor to shape the genome structure. Illegitimate recombination not only led to genomic inversion but also inverted fragment duplication, both of which contributed to the creation of new genes and gene family, and further, homological recombination contributed to events of inversion. Based on the information of genomic rearrangement, the first genome scaffold structure of H. pylori last common ancestor was produced. The core genome consists of 1186 genes, of which 22 genes could particularly adapt to human stomach niche. H. pylori contains high proportion of pseudogenes whose genesis was principally caused by homopolynucleotide (HPN) mutations. Such mutations are reversible and facilitate the control of gene expression through the change of DNA structure. The reversible mutations and a quasi-panmictic feature could allow such genes or gene fragments frequently transferred within or between populations. Hence, pseudogenes could be a reservoir of adaptation materials and the HPN mutations could be favorable to H. pylori adaptation, leading to HPN accumulation on the genomes, which corresponds to a special feature of Helicobacter species: extremely high HPN composition of genome.

Conclusion: Our research demonstrated that both genome content and structure of H. pylori have been highly adapted to its particular life style.

Show MeSH
Related in: MedlinePlus