The first world swimming championships of roseobacters—Phylogenomic insights into an exceptional motility phenotype

Abstract

Many marine Alphaproteobacteria of the Roseobacter group show a characteristic swim-or-stick lifestyle, for which motility is a crucial trait. Three phylogenetically distinct flagellar gene clusters (FGCs) have been identified in Rhodobacteraceae that have been named fla1, fla2 and fla3 according to their relative abundance. In addition to the flagellar-dependent swimming and swarming motility, pilus-dependent twitching mediates bacterial locomotion. Furthermore, filament independent modes of motility, namely gliding and sliding, have been described for various microorganisms. However, no mode of motility other than swimming has so far been described for roseobacters. In the present study, we investigated motility, distribution of flagellar systems and the phylogeny of 120 genome-sequenced Rhodobacteraceae. The phylogenetically broad taxon sampling that included 114 type strains revealed the presence of at least ten distinct clades that were statistically well supported. The investigation of the actual physiological capacity for swimming motility on soft agar plates showed that only about half of the 120 tested strains were motile under the tested conditions. Seven strains developed a conspicuous dendritic motility phenotype that was reminiscent of the swarming motility in Pseudomonas aeruginosa. The observed dendritic motility in two strains (i.e. Sulfitobacter pseudonitzschiae DSM 26842 and Roseovarius pacificus DSM 29589) was particularly surprising because they did not harbor any genes of the FGC. Accordingly, it was concluded that this form of dendritic motility was independent of a flagellum. A comparative genomics approach allowed a remarkable number of pilus-related candidate genes to be identified for this novel type of motility in Rhodobacteraceae.