Comparative and Phylogenomic Evidence That the Alphaproteobacterium HIMB59 Is Not a Member of the Oceanic SAR11 Clade

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.