The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta-proteobacteria

Abstract

Anaeromyxobacter dehalogenans strain 2CP-C is a versaphilic delta-Proteobacterium distributed throughout many diverse soil and sediment environments. 16S rRNA gene phylogenetic analysis groups A. dehalogenans together with the myxobacteria, which have distinguishing characteristics including strictly aerobic metabolism, sporulation, fruiting body formation, and surface motility. Analysis of the 5.01 Mb strain 2CP-C genome substantiated that this organism is a myxobacterium but shares genotypic traits with the anaerobic majority of the delta-Proteobacteria (i.e., the Desulfuromonadales). Reflective of its respiratory versatility, strain 2CP-C possesses 68 genes coding for putative c-type cytochromes, including one gene with 40 heme binding motifs. Consistent with its relatedness to the myxobacteria, surface motility was observed in strain 2CP-C and multiple types of motility genes are present, including 28 genes for gliding, adventurous (A-) motility and 17 genes for type IV pilus-based motility (i.e., social (S-) motility) that all have homologs in Myxococcus xanthus. Although A. dehalogenans shares many metabolic traits with the anaerobic majority of the delta-Proteobacteria, strain 2CP-C grows under microaerophilic conditions and possesses detoxification systems for reactive oxygen species. Accordingly, two gene clusters coding for NADH dehydrogenase subunits and two cytochrome oxidase gene clusters in strain 2CP-C are similar to those in M. xanthus. Remarkably, strain 2CP-C possesses a third NADH dehydrogenase gene cluster and a cytochrome cbb(3) oxidase gene cluster, apparently acquired through ancient horizontal gene transfer from a strictly anaerobic green sulfur bacterium. The mosaic nature of the A. dehalogenans strain 2CP-C genome suggests that the metabolically versatile, anaerobic members of the delta-Proteobacteria may have descended from aerobic ancestors with complex lifestyles.

Figure 1. 16S rRNA gene-based phylogenetic tree of the delta-Proteobacteria indicates that A. dehalogenans strain 2CP-C is deeply nested in the order Myxococcales.

Neighbor-joining bootstrap values (500 replicates) are indicated at each branch. Class, order, and suborder designations are indicated on the right side.

Figure 2. The Anaeromyxobacter dehalogenans strain 2CP-C complete genome with genes color-coded to indicate putative ancestry.

Genome positions are indicated on the outside of the circle. The color legend refers to the two outer circles. The outer circle indicates predicted coding regions on the plus strand colored according to the organism that carries a gene with greatest sequence similarity. The second circle indicates predicted coding regions on the minus strand also color coded by gene similarity. The third circle (black) shows variation in G+C content with the average G+C value as the center line. The innermost circle (green and purple) depicts GC skew with the average GC skew as the center line.

Figure 3. Phenetic, enzyme-based classification groups A. dehalogenans strain 2CP-C with aerobic organisms (red box).

The blue dashed line box indicates the anaerobic delta-Proteobacteria included in the analysis. Bootstrap values are indicated at each node.

Figure 4. A. dehalogenans strain 2CP-C colony edges magnified 100-fold bear evidence of gliding motility.

Flares characteristic of gliding motility began forming after 2 days of incubation.

Figure 5. Distribution of heme-binding motifs in c-type cytochrome genes varies according to respiratory versatility and correlates with aerobic, facultative, or strict anaerobic lifestyle: aerobic bacteria, metal reducers, and obligate anaerobes.

Escherichia coli (Ecoli), Bdellovibrio bacteriovorus (Bdbac), Myxococcus xanthus (Mxan), Shewanella oneidensis (Sheon), Anaeromyxobacter dehalogenans (Adeh), Geobacter sulfurreducens (Gsulf), Geobacter metallireducens (Gmet), Geobacter lovleyi (Glov), Desulfovibrio vulgaris (Dvul), Pelodictyon luteolum (Plut), Chlorobium phaeobacteroides (Cpha), and Dehalococcoides species strain BAV1 (Dehal).