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Sequencing and comparative genome analysis of two pathogenic Streptococcus gallolyticus subspecies: genome plasticity, adaptation and virulence.

Lin IH, Liu TT, Teng YT, Wu HL, Liu YM, Wu KM, Chang CH, Hsu MT - PLoS ONE (2011)

Bottom Line: We have also predicted putative cell-surface associated proteins that could play a role in adherence to host tissues, leading to persistent infections causing sub-acute and chronic diseases in humans.This study showed evidence that the S. gallolyticus still possesses genes making it suitable in a rumen environment, whereas the ability for S. pasteurianus to live in rumen is reduced.The genome heterogeneity and genetic diversity among the two biotypes, especially membrane and lipoproteins, most likely contribute to the differences in the pathogenesis of the two S. gallolyticus biotypes and the type of disease an infected patient eventually develops.

View Article: PubMed Central - PubMed

Affiliation: Institute of BioMedical Informatics, National Yang-Ming University, Taipei, Taiwan.

ABSTRACT
Streptococcus gallolyticus infections in humans are often associated with bacteremia, infective endocarditis and colon cancers. The disease manifestations are different depending on the subspecies of S. gallolyticus causing the infection. Here, we present the complete genomes of S. gallolyticus ATCC 43143 (biotype I) and S. pasteurianus ATCC 43144 (biotype II.2). The genomic differences between the two biotypes were characterized with comparative genomic analyses. The chromosome of ATCC 43143 and ATCC 43144 are 2,36 and 2,10 Mb in length and encode 2246 and 1869 CDS respectively. The organization and genomic contents of both genomes were most similar to the recently published S. gallolyticus UCN34, where 2073 (92%) and 1607 (86%) of the ATCC 43143 and ATCC 43144 CDS were conserved in UCN34 respectively. There are around 600 CDS conserved in all Streptococcus genomes, indicating the Streptococcus genus has a small core-genome (constitute around 30% of total CDS) and substantial evolutionary plasticity. We identified eight and five regions of genome plasticity in ATCC 43143 and ATCC 43144 respectively. Within these regions, several proteins were recognized to contribute to the fitness and virulence of each of the two subspecies. We have also predicted putative cell-surface associated proteins that could play a role in adherence to host tissues, leading to persistent infections causing sub-acute and chronic diseases in humans. This study showed evidence that the S. gallolyticus still possesses genes making it suitable in a rumen environment, whereas the ability for S. pasteurianus to live in rumen is reduced. The genome heterogeneity and genetic diversity among the two biotypes, especially membrane and lipoproteins, most likely contribute to the differences in the pathogenesis of the two S. gallolyticus biotypes and the type of disease an infected patient eventually develops.

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Circular representation of protein conservation of (a) S. gallolyticus ATCC 43143 and (b) S. pasteurianus ATCC 43144.From the outside in, the outer two circles showed the open reading frames (ORFs) oriented in the forward (red) and reverse (blue) directions respectively. The third and forth circles marked the homology with other sequenced bacteria and streptococci respectively, with darker the line denoting more genomes having the putative protein orthologs and whiter lines otherwise. The fifth and sixth circle shows the degree of protein sequence homology with UCN34 and the other S. gallolyticus strain (ATCC 43144 in figure 4a and ATCC 43143 in figure 4b) respectively, with a color-scale running from the most similar in red to least similarity in green. The seventh circle shows the normalized codon usage values of the ORFs, with a color-scale running from the higher values in red to lower values in green. The location of transposases, Tn elements and phage proteins are marked by lime colored lines. Strain-specific regions (regions of genomic plasticity) are marked by bold numbers.
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pone-0020519-g004: Circular representation of protein conservation of (a) S. gallolyticus ATCC 43143 and (b) S. pasteurianus ATCC 43144.From the outside in, the outer two circles showed the open reading frames (ORFs) oriented in the forward (red) and reverse (blue) directions respectively. The third and forth circles marked the homology with other sequenced bacteria and streptococci respectively, with darker the line denoting more genomes having the putative protein orthologs and whiter lines otherwise. The fifth and sixth circle shows the degree of protein sequence homology with UCN34 and the other S. gallolyticus strain (ATCC 43144 in figure 4a and ATCC 43143 in figure 4b) respectively, with a color-scale running from the most similar in red to least similarity in green. The seventh circle shows the normalized codon usage values of the ORFs, with a color-scale running from the higher values in red to lower values in green. The location of transposases, Tn elements and phage proteins are marked by lime colored lines. Strain-specific regions (regions of genomic plasticity) are marked by bold numbers.

Mentions: Comparison in a genomic scale revealed high conservation in both the sequence and gene order of the ATCC 43143, ATCC 43144 and UCN34 genomes (Figure 3). At the same time, strain-specific regions, also known as regions of genomic plasticity (RGPs) were also identified (Figure 4). Sequence comparison against all of the other sequenced streptococcal genomes showed 91% of the CDS in ATCC 43413 and 80% in ATCC 43144 were orthologous to UCN34. Protein conservation is lower compared with other streptococci, with no more than 60% ATCC 43413 CDS and 70% ATCC 43144 CDS conserved in any single Streptococcus species (Table S1 and Figure S1). There are 600 ATCC 43143 CDS and 585 ATCC 43143 CDS that are conserved in all sequenced streptococci. A list of 108 conserved CDS that are completely identical in peptide sequence in ATCC 43143, ATCC 43144 and UCN34 is provided in Table S2. The average number of CDS in Streptococcus is roughly 2000 genes; hence the streptococci core-genome consists about 30% of the total predicted proteome. There are 99 (4%) ATCC 43143 CDS and 116 (6%) ATCC 43144 CDS not conserved in any sequenced streptococci (Table S3 and S4). The numbers rose to 410 (18%) in ATCC 43143 CDS and 217 (12%) in ATCC 43144 CDS when conservation in UCN34 was not considered, suggests the S. gallolyticus genomes contained more subspecies-specific genes than S. pasteurianus.


Sequencing and comparative genome analysis of two pathogenic Streptococcus gallolyticus subspecies: genome plasticity, adaptation and virulence.

Lin IH, Liu TT, Teng YT, Wu HL, Liu YM, Wu KM, Chang CH, Hsu MT - PLoS ONE (2011)

Circular representation of protein conservation of (a) S. gallolyticus ATCC 43143 and (b) S. pasteurianus ATCC 43144.From the outside in, the outer two circles showed the open reading frames (ORFs) oriented in the forward (red) and reverse (blue) directions respectively. The third and forth circles marked the homology with other sequenced bacteria and streptococci respectively, with darker the line denoting more genomes having the putative protein orthologs and whiter lines otherwise. The fifth and sixth circle shows the degree of protein sequence homology with UCN34 and the other S. gallolyticus strain (ATCC 43144 in figure 4a and ATCC 43143 in figure 4b) respectively, with a color-scale running from the most similar in red to least similarity in green. The seventh circle shows the normalized codon usage values of the ORFs, with a color-scale running from the higher values in red to lower values in green. The location of transposases, Tn elements and phage proteins are marked by lime colored lines. Strain-specific regions (regions of genomic plasticity) are marked by bold numbers.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3102119&req=5

pone-0020519-g004: Circular representation of protein conservation of (a) S. gallolyticus ATCC 43143 and (b) S. pasteurianus ATCC 43144.From the outside in, the outer two circles showed the open reading frames (ORFs) oriented in the forward (red) and reverse (blue) directions respectively. The third and forth circles marked the homology with other sequenced bacteria and streptococci respectively, with darker the line denoting more genomes having the putative protein orthologs and whiter lines otherwise. The fifth and sixth circle shows the degree of protein sequence homology with UCN34 and the other S. gallolyticus strain (ATCC 43144 in figure 4a and ATCC 43143 in figure 4b) respectively, with a color-scale running from the most similar in red to least similarity in green. The seventh circle shows the normalized codon usage values of the ORFs, with a color-scale running from the higher values in red to lower values in green. The location of transposases, Tn elements and phage proteins are marked by lime colored lines. Strain-specific regions (regions of genomic plasticity) are marked by bold numbers.
Mentions: Comparison in a genomic scale revealed high conservation in both the sequence and gene order of the ATCC 43143, ATCC 43144 and UCN34 genomes (Figure 3). At the same time, strain-specific regions, also known as regions of genomic plasticity (RGPs) were also identified (Figure 4). Sequence comparison against all of the other sequenced streptococcal genomes showed 91% of the CDS in ATCC 43413 and 80% in ATCC 43144 were orthologous to UCN34. Protein conservation is lower compared with other streptococci, with no more than 60% ATCC 43413 CDS and 70% ATCC 43144 CDS conserved in any single Streptococcus species (Table S1 and Figure S1). There are 600 ATCC 43143 CDS and 585 ATCC 43143 CDS that are conserved in all sequenced streptococci. A list of 108 conserved CDS that are completely identical in peptide sequence in ATCC 43143, ATCC 43144 and UCN34 is provided in Table S2. The average number of CDS in Streptococcus is roughly 2000 genes; hence the streptococci core-genome consists about 30% of the total predicted proteome. There are 99 (4%) ATCC 43143 CDS and 116 (6%) ATCC 43144 CDS not conserved in any sequenced streptococci (Table S3 and S4). The numbers rose to 410 (18%) in ATCC 43143 CDS and 217 (12%) in ATCC 43144 CDS when conservation in UCN34 was not considered, suggests the S. gallolyticus genomes contained more subspecies-specific genes than S. pasteurianus.

Bottom Line: We have also predicted putative cell-surface associated proteins that could play a role in adherence to host tissues, leading to persistent infections causing sub-acute and chronic diseases in humans.This study showed evidence that the S. gallolyticus still possesses genes making it suitable in a rumen environment, whereas the ability for S. pasteurianus to live in rumen is reduced.The genome heterogeneity and genetic diversity among the two biotypes, especially membrane and lipoproteins, most likely contribute to the differences in the pathogenesis of the two S. gallolyticus biotypes and the type of disease an infected patient eventually develops.

View Article: PubMed Central - PubMed

Affiliation: Institute of BioMedical Informatics, National Yang-Ming University, Taipei, Taiwan.

ABSTRACT
Streptococcus gallolyticus infections in humans are often associated with bacteremia, infective endocarditis and colon cancers. The disease manifestations are different depending on the subspecies of S. gallolyticus causing the infection. Here, we present the complete genomes of S. gallolyticus ATCC 43143 (biotype I) and S. pasteurianus ATCC 43144 (biotype II.2). The genomic differences between the two biotypes were characterized with comparative genomic analyses. The chromosome of ATCC 43143 and ATCC 43144 are 2,36 and 2,10 Mb in length and encode 2246 and 1869 CDS respectively. The organization and genomic contents of both genomes were most similar to the recently published S. gallolyticus UCN34, where 2073 (92%) and 1607 (86%) of the ATCC 43143 and ATCC 43144 CDS were conserved in UCN34 respectively. There are around 600 CDS conserved in all Streptococcus genomes, indicating the Streptococcus genus has a small core-genome (constitute around 30% of total CDS) and substantial evolutionary plasticity. We identified eight and five regions of genome plasticity in ATCC 43143 and ATCC 43144 respectively. Within these regions, several proteins were recognized to contribute to the fitness and virulence of each of the two subspecies. We have also predicted putative cell-surface associated proteins that could play a role in adherence to host tissues, leading to persistent infections causing sub-acute and chronic diseases in humans. This study showed evidence that the S. gallolyticus still possesses genes making it suitable in a rumen environment, whereas the ability for S. pasteurianus to live in rumen is reduced. The genome heterogeneity and genetic diversity among the two biotypes, especially membrane and lipoproteins, most likely contribute to the differences in the pathogenesis of the two S. gallolyticus biotypes and the type of disease an infected patient eventually develops.

Show MeSH
Related in: MedlinePlus