From the Inside Out: an Epibiotic Bdellovibrio Predator with an Expanded Genomic Complement

Abstract

Bdellovibrio and like organisms are bacteria that prey on other bacteria and are widespread in the environment. Most of the known Bdellovibrio species enter the space between the inner and outer prey membrane, where they consume their prey cells. However, one Bdellovibrio species has been described that consumes its prey from the outside. Here, we describe “ Ca. Bdellovibrio qaytius,” a novel member of the genus Bdellovibrio that also remains outside the prey cell throughout its replication cycle. Unexpectedly, the genome of “ Ca. Bdellovibrio” is much more similar to the genomes of intracellular predators than to the species with a similar life cycle. Since “ Ca. Bdellovibrio” is also a basal representative of this genus, we hypothesize that extracellular predation could be the ancestral predation strategy.

ABSTRACT

Bdellovibrio and like organisms are abundant environmental parasitoids of prokaryotes that show diverse predation strategies. The vast majority of studied Bdellovibrio bacteria and like organisms deploy intraperiplasmic replication inside the prey cell, while few isolates with smaller genomes consume their prey from the outside in an epibiotic manner. The novel parasitoid “ Candidatus Bdellovibrio qaytius” was isolated from a eutrophic freshwater pond in British Columbia, where it was a continual part of the microbial community. “ Ca. Bdellovibrio qaytius” was found to preferentially prey on the betaproteobacterium Paraburkholderia fungorum without entering the periplasm. Despite its epibiotic replication strategy, “ Ca. Bdellovibrio” encodes a large genomic complement more similar to that of complex periplasmic predators. Functional genomic annotation further revealed several biosynthesis pathways not previously found in epibiotic predators, indicating that “ Ca. Bdellovibrio” represents an intermediate phenotype and at the same time narrowing down the genomic complement specific to epibiotic predators. In phylogenetic analysis, “ Ca. Bdellovibrio qaytius” occupies a widely distributed, but poorly characterized, basal cluster within the genus Bdellovibrio. This suggests that epibiotic predation might be a common predation type in nature and that epibiotic predation could be the ancestral predation type in the genus.

IMPORTANCE Bdellovibrio and like organisms are bacteria that prey on other bacteria and are widespread in the environment. Most of the known Bdellovibrio species enter the space between the inner and outer prey membrane, where they consume their prey cells. However, one Bdellovibrio species has been described that consumes its prey from the outside. Here, we describe “ Ca. Bdellovibrio qaytius,” a novel member of the genus Bdellovibrio that also remains outside the prey cell throughout its replication cycle. Unexpectedly, the genome of “ Ca. Bdellovibrio” is much more similar to the genomes of intracellular predators than to the species with a similar life cycle. Since “ Ca. Bdellovibrio” is also a basal representative of this genus, we hypothesize that extracellular predation could be the ancestral predation strategy.