In and out: an analysis of epibiotic vs periplasmic bacterial predators

Abstract

Bdellovibrio and like organisms (BALO) are obligate predators of Gram-negative bacteria, belonging to the α- and δ-proteobacteria. BALO prey using either a periplasmic or an epibiotic predatory strategy, but the genetic background underlying these phenotypes is not known. Here we compare the epibiotic Bdellovibrio exovorus and Micavibrio aeruginosavorus to the periplasmic B. bacteriovorus and Bacteriovorax marinus. Electron microscopy showed that M. aeruginosavorus, but not B. exovorus, can attach to prey cells in a non-polar manner through its longitudinal side. Both these predators were resistant to a surprisingly high number of antibiotic compounds, possibly via 26 and 19 antibiotic-resistance genes, respectively, most of them encoding efflux pumps. Comparative genomic analysis of all the BALOs revealed that epibiotic predators have a much smaller genome (ca. 2.5 Mbp) than the periplasmic predators (ca. 3.5 Mbp). Additionally, periplasmic predators have, on average, 888 more proteins, at least 60% more peptidases, and one more rRNA operon. Fifteen and 219 protein families were specific to the epibiotic and the periplasmic predators, respectively, the latter clearly forming the core of the periplasmic 'predatome', which is upregulated during the growth phase. Metabolic deficiencies of epibiotic genomes include the synthesis of inosine, riboflavin, vitamin B6 and the siderophore aerobactin. The phylogeny of the epibiotic predators suggests that they evolved by convergent evolution, with M. aeruginosavorus originating from a non-predatory ancestor while B. exovorus evolved from periplasmic predators by gene loss.

Figure 1

(a) A dividing B. exovorus JSS preying on Caulobacter crescentus; (b) M. aeruginosavorus EPB dividing, attached to a Pseudomonas corrugata prey cell; (c) two M. aeruginosavorus EPB attack-phase predators simultaneously attached to a Pseudomonas corrugata prey cell; (d) M. aeruginosavorus EPB attached to a Pseudomonas corrugata prey cell by its longitudinal side; (e) unattached M. aeruginosavorus EPB cells dividing. Bars in (a) and (e) equal 200 nm.

Figure 2

Venn diagram of the proteins in the genomes of B. bacteriovorus HD100, B. marinus SJ, M. aeruginosavorus EPB and B. exovorus JSS. Proteins were clustered using BLAST with an E-value <10⁻⁴.