Abstract
BackgroundEvolution equipped Bdellovibrio bacteriovorus predatory bacteria to invade other bacteria, digesting and replicating, sealed within them thus preventing nutrient-sharing with organisms in the surrounding environment. Bdellovibrio were previously described as “obligate predators” because only by mutations, often in gene bd0108, are 1 in ~1x107 of predatory lab strains of Bdellovibrio converted to prey-independent growth. A previous genomic analysis of B. bacteriovorus strain HD100 suggested that predatory consumption of prey DNA by lytic enzymes made Bdellovibrio less likely than other bacteria to acquire DNA by lateral gene transfer (LGT). However the Doolittle and Pan groups predicted, in silico, both ancient and recent lateral gene transfer into the B. bacteriovorus HD100 genome.ResultsTo test these predictions, we isolated a predatory bacterium from the River Tiber- a good potential source of LGT as it is rich in diverse bacteria and organic pollutants- by enrichment culturing with E. coli prey cells. The isolate was identified as B. bacteriovorus and named as strain Tiberius. Unusually, this Tiberius strain showed simultaneous prey-independent growth on organic nutrients and predatory growth on live prey. Despite the prey-independent growth, the homolog of bd0108 did not have typical prey-independent-type mutations. The dual growth mode may reflect the high carbon content of the river, and gives B. bacteriovorus Tiberius extended non-predatory contact with the other bacteria present. The HD100 and Tiberius genomes were extensively syntenic despite their different cultured-terrestrial/freshly-isolated aquatic histories; but there were significant differences in gene content indicative of genomic flux and LGT. Gene content comparisons support previously published in silico predictions for LGT in strain HD100 with substantial conservation of genes predicted to have ancient LGT origins but little conservation of AT-rich genes predicted to be recently acquired.ConclusionsThe natural niche and dual predatory, and prey-independent growth of the B. bacteriovorus Tiberius strain afforded it extensive non-predatory contact with other marine and freshwater bacteria from which LGT is evident in its genome. Thus despite their arsenal of DNA-lytic enzymes; Bdellovibrio are not always predatory in natural niches and their genomes are shaped by acquiring whole genes from other bacteria.
Highlights
Evolution equipped Bdellovibrio bacteriovorus predatory bacteria to invade other bacteria, digesting and replicating, sealed within them preventing nutrient-sharing with organisms in the surrounding environment
The 16SrRNA gene amplified from the genomic DNA of the Tiberius strain cultures gave a single uniform sequence which was used to position the bacterium on a phylogenetic tree (Additional file 1) where it clustered with Bdellovibrio bacteriovorus strains, including the type strain HD100 and the well-characterised lab strain 109J [12,13]
As we discovered experimentally that the Tiberius strain had differences to HD100 in its predatory versus prey-independent growth control, we noted genes associated with those phenotypes
Summary
Evolution equipped Bdellovibrio bacteriovorus predatory bacteria to invade other bacteria, digesting and replicating, sealed within them preventing nutrient-sharing with organisms in the surrounding environment. A previous genomic analysis of B. bacteriovorus strain HD100 suggested that predatory consumption of prey DNA by lytic enzymes made Bdellovibrio less likely than other bacteria to acquire DNA by lateral gene transfer (LGT). In “attack phase”, the small, vibroid and uniflagellate B. bacteriovorus cells collide with and invade bacterial prey wherein they replicate. Despite this provision of nutrition by prey, B. bacteriovorus retains a large 3.8 Mb genome, as the sequence of the terrestrial type-strain HD100 [1,2] shows. The gene content is large for two main reasons: Firstly, entry into and digestion of another bacterium requires coding of an arsenal of hydrolytic enzymes and sensor regulator systems. The invaded prey cell, known as the “bdelloplast”, forms a protective barrier against potential environmental insults while the Bdellovibrio replicate
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