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Open Access Research article

Genome analysis of a simultaneously predatory and prey-independent, novel Bdellovibrio bacteriovorus from the River Tiber, supports in silico predictions of both ancient and recent lateral gene transfer from diverse bacteria

Laura Hobley13, Thomas R Lerner14, Laura E Williams2, Carey Lambert1, Rob Till1, David S Milner1, Sarah M Basford1, Michael J Capeness1, Andrew K Fenton15, Robert J Atterbury16, Maximilian ATS Harris1 and R Elizabeth Sockett1*

Author affiliations

1 Centre for Genetics and Genomics, School of Biology, University of Nottingham, Medical School QMC, Derby Road, Nottingham, NG7 2UH, UK

2 Institute for Genome Sciences and Policy, Duke University, Durham, NC, 27708, USA

3 Current addresses: College of Life Sciences, University of Dundee, Dow Street, Dundee, Scotland, DD1 5EH, UK

4 Current addresses: Division of Mycobacterial Research, MRC National Institute for Medical Research, The Ridgeway, Mill Hill, London, NW7 1AA, UK

5 Current addresses: Centre for Bacterial Cell Biology, University of Newcastle, Newcastle Upon Tyne, NE2 4AX, UK

6 School of Veterinary Medicine & Science, University of Nottingham, Sutton Bonington Campus, Leicestershire, LE12 5RD, UK

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Citation and License

BMC Genomics 2012, 13:670  doi:10.1186/1471-2164-13-670

Published: 27 November 2012

Abstract

Background

Evolution 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.

Results

To 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.

Conclusions

The 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.

Keywords:
Evolutionary genetics of bacteria; Lateral gene transfer; Predatory Bdellovibrio