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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 and mitochondria.Bayesian tree inferred with the CAT model applied to an alignment of 13 concatenated pan-orthologous proteins. HIMB59 (marked in red) is placed within the Rhodospirillales. The SAR11 clade (marked in blue) is placed within a broad group of free-living alphaproteobacterial species that includes the Sphingomonadales, Rhodobacterales, Rhizobiales, and Caulobacterales. Numbers at nodes show PP values.
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pone-0078858-g002: Phylogenetic analysis of the Alphaproteobacteria and mitochondria.Bayesian tree inferred with the CAT model applied to an alignment of 13 concatenated pan-orthologous proteins. HIMB59 (marked in red) is placed within the Rhodospirillales. The SAR11 clade (marked in blue) is placed within a broad group of free-living alphaproteobacterial species that includes the Sphingomonadales, Rhodobacterales, Rhizobiales, and Caulobacterales. Numbers at nodes show PP values.

Mentions: Next, we examined how the inclusion of mitochondrial sequences in the tree influenced the relation of HIMB59 to the SAR11 isolates. To this end, we made a separate clustering of proteins encoded by 48 mitochondrial genomes (Table S1). These were then merged with the corresponding clusters generated from the alphaproteobacterial genomes. First, we inferred the relationships of these taxa from a concatenated set of 29 proteins that indicated monophyly of the mitochondria in single protein trees with the maximum likelihood method. HIMB59 clustered separately from the SAR11 clade in these trees irrespectively of the method used for the analysis (data not shown). From this set, we selected a smaller set of proteins that individually supported the monophyly of mitochondria with more than 70% bootstrap support and included taxa such that each alphaproteobacterial genus would be represented by at least one species. This resulted in a dataset of 177 taxa and 13 orthologous protein clusters (Table S2). In the trees inferred from these proteins, both the Bayesian (Figure 2) and the maximum likelihood analyses (Figure S2) suggested that the SAR11 clade was placed distinct from the Rickettsiales and mitochondria and positioned within the free-living Alphaproteobacteria. Importantly, the SAR11 isolates of subtypes Ia and IIIa formed a clade with 100% support, while HIMB59 was positioned within the Rhodospirillales in the Bayesian analyses (posterior probability = 1.0) or at the base of the free-living Alphaproteobacteria in the maximum likelihood analysis (bootstrap support = 80%). Thus, none of the trees that included mitochondrial taxa suggested a placement of either mitochondria or HIMB59 within or as sister groups to the SAR11 clade.


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 and mitochondria.Bayesian tree inferred with the CAT model applied to an alignment of 13 concatenated pan-orthologous proteins. HIMB59 (marked in red) is placed within the Rhodospirillales. The SAR11 clade (marked in blue) is placed within a broad group of free-living alphaproteobacterial species that includes the Sphingomonadales, 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-g002: Phylogenetic analysis of the Alphaproteobacteria and mitochondria.Bayesian tree inferred with the CAT model applied to an alignment of 13 concatenated pan-orthologous proteins. HIMB59 (marked in red) is placed within the Rhodospirillales. The SAR11 clade (marked in blue) is placed within a broad group of free-living alphaproteobacterial species that includes the Sphingomonadales, Rhodobacterales, Rhizobiales, and Caulobacterales. Numbers at nodes show PP values.
Mentions: Next, we examined how the inclusion of mitochondrial sequences in the tree influenced the relation of HIMB59 to the SAR11 isolates. To this end, we made a separate clustering of proteins encoded by 48 mitochondrial genomes (Table S1). These were then merged with the corresponding clusters generated from the alphaproteobacterial genomes. First, we inferred the relationships of these taxa from a concatenated set of 29 proteins that indicated monophyly of the mitochondria in single protein trees with the maximum likelihood method. HIMB59 clustered separately from the SAR11 clade in these trees irrespectively of the method used for the analysis (data not shown). From this set, we selected a smaller set of proteins that individually supported the monophyly of mitochondria with more than 70% bootstrap support and included taxa such that each alphaproteobacterial genus would be represented by at least one species. This resulted in a dataset of 177 taxa and 13 orthologous protein clusters (Table S2). In the trees inferred from these proteins, both the Bayesian (Figure 2) and the maximum likelihood analyses (Figure S2) suggested that the SAR11 clade was placed distinct from the Rickettsiales and mitochondria and positioned within the free-living Alphaproteobacteria. Importantly, the SAR11 isolates of subtypes Ia and IIIa formed a clade with 100% support, while HIMB59 was positioned within the Rhodospirillales in the Bayesian analyses (posterior probability = 1.0) or at the base of the free-living Alphaproteobacteria in the maximum likelihood analysis (bootstrap support = 80%). Thus, none of the trees that included mitochondrial taxa suggested a placement of either mitochondria or HIMB59 within or as sister groups to the SAR11 clade.

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.

Show MeSH