Limits...
Phylogenomics and the dynamic genome evolution of the genus Streptococcus.

Richards VP, Palmer SR, Pavinski Bitar PD, Qin X, Weinstock GM, Highlander SK, Town CD, Burne RA, Stanhope MJ - Genome Biol Evol (2014)

Bottom Line: This was followed by a period of genome expansion associated with the origins of the present extant species.Multiple gene ontology terms were significantly enriched for each group, and mapping terms onto the phylogeny showed that those corresponding to genes born on branches leading to the major groups represented approximately one-fifth of those enriched.For example, proteolysis: mitis group; urea metabolism: salivarius group; carbohydrate metabolism: pyogenic group; and transcription regulation: bovis group.

View Article: PubMed Central - PubMed

Affiliation: Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University.

ABSTRACT
The genus Streptococcus comprises important pathogens that have a severe impact on human health and are responsible for substantial economic losses to agriculture. Here, we utilize 46 Streptococcus genome sequences (44 species), including eight species sequenced here, to provide the first genomic level insight into the evolutionary history and genetic basis underlying the functional diversity of all major groups of this genus. Gene gain/loss analysis revealed a dynamic pattern of genome evolution characterized by an initial period of gene gain followed by a period of loss, as the major groups within the genus diversified. This was followed by a period of genome expansion associated with the origins of the present extant species. The pattern is concordant with an emerging view that genomes evolve through a dynamic process of expansion and streamlining. A large proportion of the pan-genome has experienced lateral gene transfer (LGT) with causative factors, such as relatedness and shared environment, operating over different evolutionary scales. Multiple gene ontology terms were significantly enriched for each group, and mapping terms onto the phylogeny showed that those corresponding to genes born on branches leading to the major groups represented approximately one-fifth of those enriched. Furthermore, despite the extensive LGT, several biochemical characteristics have been retained since group formation, suggesting genomic cohesiveness through time, and that these characteristics may be fundamental to each group. For example, proteolysis: mitis group; urea metabolism: salivarius group; carbohydrate metabolism: pyogenic group; and transcription regulation: bovis group.

Show MeSH

Related in: MedlinePlus

Hierarchal clustering among genomes using presence/absence of MCL gene clusters. Approximately unbiased P values are shown on branches. Color shading for each major Streptococcus group follows figure 1.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4007547&req=5

evu048-F3: Hierarchal clustering among genomes using presence/absence of MCL gene clusters. Approximately unbiased P values are shown on branches. Color shading for each major Streptococcus group follows figure 1.

Mentions: From the perspective of gene gain/loss (turnover) for individual species, S. constellatus subsp. pharyngis is notable, as this taxon showed considerably more turnover than any other (gain = 1,408, loss = 503) (fig. 2), suggesting that perhaps this species was shifting or expanding its niche (Hao and Golding 2006; Marri et al. 2007). This high turnover was also reflected in the hierarchal clustering analysis (presence/absence of MCL gene clusters) (fig. 3) where this species was placed as an outlier to all remaining Streptococcus species. Similarly, the important human pathogens S. pyogenes and S. pneumoniae also showed high gene turnover, ranking 6th and 9th, respectively. In contrast, the two strains of S. agalactiae showed considerably less turnover ranking 21st (bovine isolate) and 40th (human isolate). The higher turnover for the bovine isolate compared with the human isolate might reflect a more recent adaptation to this environment. Similarly, S. parauberis, which was traditionally associated with the bovine environment (Williams and Collins 1990), has recently been identified as an emerging fish pathogen (Nho et al. 2011), and the fish isolate (19th) showed considerably more turnover than the bovine isolate (38th). Streptococcus suis, which remained an outlier to the mitis, sanguinis, and anginosus groups, also showed particularly high turnover (gain = 1,020, loss = 380, ranking 2nd). This species is a major porcine pathogen; however, the species has recently been identified as a particularly virulent emerging zoonotic pathogen and as an etiological agent for streptococcal toxic shock syndrome (STSS) (Lun et al. 2007). The S. suis strain included in our analysis (98HAH33) was isolated from a fatal case of STSS from an outbreak in China (Chen et al. 2007). Again, the high gene turnover for this species may reflect its recent adaptation to the human environment.Fig. 3.—


Phylogenomics and the dynamic genome evolution of the genus Streptococcus.

Richards VP, Palmer SR, Pavinski Bitar PD, Qin X, Weinstock GM, Highlander SK, Town CD, Burne RA, Stanhope MJ - Genome Biol Evol (2014)

Hierarchal clustering among genomes using presence/absence of MCL gene clusters. Approximately unbiased P values are shown on branches. Color shading for each major Streptococcus group follows figure 1.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4007547&req=5

evu048-F3: Hierarchal clustering among genomes using presence/absence of MCL gene clusters. Approximately unbiased P values are shown on branches. Color shading for each major Streptococcus group follows figure 1.
Mentions: From the perspective of gene gain/loss (turnover) for individual species, S. constellatus subsp. pharyngis is notable, as this taxon showed considerably more turnover than any other (gain = 1,408, loss = 503) (fig. 2), suggesting that perhaps this species was shifting or expanding its niche (Hao and Golding 2006; Marri et al. 2007). This high turnover was also reflected in the hierarchal clustering analysis (presence/absence of MCL gene clusters) (fig. 3) where this species was placed as an outlier to all remaining Streptococcus species. Similarly, the important human pathogens S. pyogenes and S. pneumoniae also showed high gene turnover, ranking 6th and 9th, respectively. In contrast, the two strains of S. agalactiae showed considerably less turnover ranking 21st (bovine isolate) and 40th (human isolate). The higher turnover for the bovine isolate compared with the human isolate might reflect a more recent adaptation to this environment. Similarly, S. parauberis, which was traditionally associated with the bovine environment (Williams and Collins 1990), has recently been identified as an emerging fish pathogen (Nho et al. 2011), and the fish isolate (19th) showed considerably more turnover than the bovine isolate (38th). Streptococcus suis, which remained an outlier to the mitis, sanguinis, and anginosus groups, also showed particularly high turnover (gain = 1,020, loss = 380, ranking 2nd). This species is a major porcine pathogen; however, the species has recently been identified as a particularly virulent emerging zoonotic pathogen and as an etiological agent for streptococcal toxic shock syndrome (STSS) (Lun et al. 2007). The S. suis strain included in our analysis (98HAH33) was isolated from a fatal case of STSS from an outbreak in China (Chen et al. 2007). Again, the high gene turnover for this species may reflect its recent adaptation to the human environment.Fig. 3.—

Bottom Line: This was followed by a period of genome expansion associated with the origins of the present extant species.Multiple gene ontology terms were significantly enriched for each group, and mapping terms onto the phylogeny showed that those corresponding to genes born on branches leading to the major groups represented approximately one-fifth of those enriched.For example, proteolysis: mitis group; urea metabolism: salivarius group; carbohydrate metabolism: pyogenic group; and transcription regulation: bovis group.

View Article: PubMed Central - PubMed

Affiliation: Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University.

ABSTRACT
The genus Streptococcus comprises important pathogens that have a severe impact on human health and are responsible for substantial economic losses to agriculture. Here, we utilize 46 Streptococcus genome sequences (44 species), including eight species sequenced here, to provide the first genomic level insight into the evolutionary history and genetic basis underlying the functional diversity of all major groups of this genus. Gene gain/loss analysis revealed a dynamic pattern of genome evolution characterized by an initial period of gene gain followed by a period of loss, as the major groups within the genus diversified. This was followed by a period of genome expansion associated with the origins of the present extant species. The pattern is concordant with an emerging view that genomes evolve through a dynamic process of expansion and streamlining. A large proportion of the pan-genome has experienced lateral gene transfer (LGT) with causative factors, such as relatedness and shared environment, operating over different evolutionary scales. Multiple gene ontology terms were significantly enriched for each group, and mapping terms onto the phylogeny showed that those corresponding to genes born on branches leading to the major groups represented approximately one-fifth of those enriched. Furthermore, despite the extensive LGT, several biochemical characteristics have been retained since group formation, suggesting genomic cohesiveness through time, and that these characteristics may be fundamental to each group. For example, proteolysis: mitis group; urea metabolism: salivarius group; carbohydrate metabolism: pyogenic group; and transcription regulation: bovis group.

Show MeSH
Related in: MedlinePlus