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Comparative and phylogenomic evidence that the alphaproteobacterium HIMB59 is not a member of the oceanic SAR11 clade.

Viklund J, Martijn J, Ettema TJ, Andersson SG - PLoS ONE (2013)

Bottom Line: By placing the comparison in the context of the evolution of the Alphaproteobacteria, we found that none of the measures of genomic similarity supports a clustering of HIMB59 and SAR11 to the exclusion of other Alphaproteobacteria.Finally, in contrast to earlier reports, we observed no sequence similarity between the hypervariable region HVR2 in the SAR11 genomes and the region located at the corresponding position in the HIMB59 genome.Based on these observations, we conclude that the alphaproteobacterium HIMB59 is not monophyletic with the SAR11 strains and that genome streamlining has evolved multiple times independently in Alphaproteobacteria adapted to the upper surface waters of the oceans.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Evolution, Biomedical Centre, Science for Life Laboratory, Uppsala, Sweden.

ABSTRACT
SAR11 is a globally abundant group of Alphaproteobacteria in the oceans that is taxonomically not well defined. It has been suggested SAR11 should be classified into the novel order Pelagibacterales. Features such as conservation of gene content and synteny have been taken as evidence that also the divergent member HIMB59 should be included in the order. However, this proposition is controversial since phylogenetic analyses have questioned the monophyly of this grouping. Here, we performed phylogenetic analyses and reinvestigated the genomic similarity of SAR11 and HIMB59. Our phylogenetic analysis confirmed that HIMB59 is not a sister group to the other SAR11 strains. By placing the comparison in the context of the evolution of the Alphaproteobacteria, we found that none of the measures of genomic similarity supports a clustering of HIMB59 and SAR11 to the exclusion of other Alphaproteobacteria. First, pairwise sequence similarity measures for the SAR11 and HIMB59 genomes were within the range observed for unrelated pairs of Alphaproteobacteria. Second, pairwise comparisons of gene contents revealed a higher similarity of SAR11 to several other alphaproteobacterial genomes than to HIMB59. Third, the SAR11 genomes are not more similar in gene order to the HIMB59 genome than what they are to several other alphaproteobacterial genomes. Finally, in contrast to earlier reports, we observed no sequence similarity between the hypervariable region HVR2 in the SAR11 genomes and the region located at the corresponding position in the HIMB59 genome. Based on these observations, we conclude that the alphaproteobacterium HIMB59 is not monophyletic with the SAR11 strains and that genome streamlining has evolved multiple times independently in Alphaproteobacteria adapted to the upper surface waters of the oceans.

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Phylogenetic analysis of the Alphaproteobacteria.Bayesian tree inferred with the CAT model applied to an alignment of 150 concatenated pan-orthologous proteins. HIMB59 (marked in red) clusters with the Rickettsiales. The SAR11 clade (marked in blue) is placed within a broad group of free-living alphaproteobacterial species that includes the Spingomonadales, Rhodobacterales, Rhizobiales, and Caulobacterales. Numbers at nodes show PP values.
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pone-0078858-g001: Phylogenetic analysis of the Alphaproteobacteria.Bayesian tree inferred with the CAT model applied to an alignment of 150 concatenated pan-orthologous proteins. HIMB59 (marked in red) clusters with the Rickettsiales. The SAR11 clade (marked in blue) is placed within a broad group of free-living alphaproteobacterial species that includes the Spingomonadales, Rhodobacterales, Rhizobiales, and Caulobacterales. Numbers at nodes show PP values.

Mentions: Phylogenomic analyses of Alphaproteobacteria indicate that HIMB59 is not affiliated with SAR11. To re-examine the relationship of HIMB59 to the SAR11 genomes, we repeated our previous phylogenetic analysis of alphaproteobacterial genomes [12], and included several isolates of the SAR11 clade. As representatives of subtype Ia of the SAR11 clade we selected HTCC1062, HTCC7211 and HIMB5, and as representatives of subtype IIIa we included HIMB114 and IMCC9063 (Table 1). This resulted in a dataset of 135 alphaproteobacterial genomes that were clustered into orthologous clusters (OC) using orthoMCL (Table S1). We first constructed a phylogeny based on an alignment of a concatenated dataset of 150 proteins (Figure 1; Figure S1). As in our previous analyses [12], we noted that the placement of the SAR11 clade was sensitive to the method used to infer the phylogeny. With the Bayesian method and the CAT model the SAR11 clade clustered with the free-living Alphaproteobacteria (Figure 1), whereas it clustered with the Rickettsiales with the maximum likelihood method (Figure S1). Also the placement of HIMB59 was sensitive to the use of method such that it clustered with the SAR11 strains in the maximum likelihood trees (Figure S1), but was placed distinct from the SAR11 group with the Bayesian method (Figure 1).


Comparative and phylogenomic evidence that the alphaproteobacterium HIMB59 is not a member of the oceanic SAR11 clade.

Viklund J, Martijn J, Ettema TJ, Andersson SG - PLoS ONE (2013)

Phylogenetic analysis of the Alphaproteobacteria.Bayesian tree inferred with the CAT model applied to an alignment of 150 concatenated pan-orthologous proteins. HIMB59 (marked in red) clusters with the Rickettsiales. The SAR11 clade (marked in blue) is placed within a broad group of free-living alphaproteobacterial species that includes the Spingomonadales, Rhodobacterales, Rhizobiales, and Caulobacterales. Numbers at nodes show PP values.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3815206&req=5

pone-0078858-g001: Phylogenetic analysis of the Alphaproteobacteria.Bayesian tree inferred with the CAT model applied to an alignment of 150 concatenated pan-orthologous proteins. HIMB59 (marked in red) clusters with the Rickettsiales. The SAR11 clade (marked in blue) is placed within a broad group of free-living alphaproteobacterial species that includes the Spingomonadales, Rhodobacterales, Rhizobiales, and Caulobacterales. Numbers at nodes show PP values.
Mentions: Phylogenomic analyses of Alphaproteobacteria indicate that HIMB59 is not affiliated with SAR11. To re-examine the relationship of HIMB59 to the SAR11 genomes, we repeated our previous phylogenetic analysis of alphaproteobacterial genomes [12], and included several isolates of the SAR11 clade. As representatives of subtype Ia of the SAR11 clade we selected HTCC1062, HTCC7211 and HIMB5, and as representatives of subtype IIIa we included HIMB114 and IMCC9063 (Table 1). This resulted in a dataset of 135 alphaproteobacterial genomes that were clustered into orthologous clusters (OC) using orthoMCL (Table S1). We first constructed a phylogeny based on an alignment of a concatenated dataset of 150 proteins (Figure 1; Figure S1). As in our previous analyses [12], we noted that the placement of the SAR11 clade was sensitive to the method used to infer the phylogeny. With the Bayesian method and the CAT model the SAR11 clade clustered with the free-living Alphaproteobacteria (Figure 1), whereas it clustered with the Rickettsiales with the maximum likelihood method (Figure S1). Also the placement of HIMB59 was sensitive to the use of method such that it clustered with the SAR11 strains in the maximum likelihood trees (Figure S1), but was placed distinct from the SAR11 group with the Bayesian method (Figure 1).

Bottom Line: By placing the comparison in the context of the evolution of the Alphaproteobacteria, we found that none of the measures of genomic similarity supports a clustering of HIMB59 and SAR11 to the exclusion of other Alphaproteobacteria.Finally, in contrast to earlier reports, we observed no sequence similarity between the hypervariable region HVR2 in the SAR11 genomes and the region located at the corresponding position in the HIMB59 genome.Based on these observations, we conclude that the alphaproteobacterium HIMB59 is not monophyletic with the SAR11 strains and that genome streamlining has evolved multiple times independently in Alphaproteobacteria adapted to the upper surface waters of the oceans.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Evolution, Biomedical Centre, Science for Life Laboratory, Uppsala, Sweden.

ABSTRACT
SAR11 is a globally abundant group of Alphaproteobacteria in the oceans that is taxonomically not well defined. It has been suggested SAR11 should be classified into the novel order Pelagibacterales. Features such as conservation of gene content and synteny have been taken as evidence that also the divergent member HIMB59 should be included in the order. However, this proposition is controversial since phylogenetic analyses have questioned the monophyly of this grouping. Here, we performed phylogenetic analyses and reinvestigated the genomic similarity of SAR11 and HIMB59. Our phylogenetic analysis confirmed that HIMB59 is not a sister group to the other SAR11 strains. By placing the comparison in the context of the evolution of the Alphaproteobacteria, we found that none of the measures of genomic similarity supports a clustering of HIMB59 and SAR11 to the exclusion of other Alphaproteobacteria. First, pairwise sequence similarity measures for the SAR11 and HIMB59 genomes were within the range observed for unrelated pairs of Alphaproteobacteria. Second, pairwise comparisons of gene contents revealed a higher similarity of SAR11 to several other alphaproteobacterial genomes than to HIMB59. Third, the SAR11 genomes are not more similar in gene order to the HIMB59 genome than what they are to several other alphaproteobacterial genomes. Finally, in contrast to earlier reports, we observed no sequence similarity between the hypervariable region HVR2 in the SAR11 genomes and the region located at the corresponding position in the HIMB59 genome. Based on these observations, we conclude that the alphaproteobacterium HIMB59 is not monophyletic with the SAR11 strains and that genome streamlining has evolved multiple times independently in Alphaproteobacteria adapted to the upper surface waters of the oceans.

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