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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.

Hobley L, Lerner TR, Williams LE, Lambert C, Till R, Milner DS, Basford SM, Capeness MJ, Fenton AK, Atterbury RJ, Harris MA, Sockett RE - BMC Genomics (2012)

Bottom Line: Bdellovibrio were previously described as "obligate predators" because only by mutations, often in gene bd0108, are 1 in ~1x10(7) of predatory lab strains of Bdellovibrio converted to prey-independent growth.However the Doolittle and Pan groups predicted, in silico, both ancient and recent lateral gene transfer into the B. bacteriovorus HD100 genome.Despite the prey-independent growth, the homolog of bd0108 did not have typical prey-independent-type mutations.

View Article: PubMed Central - HTML - PubMed

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

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 ~1x10(7) 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.

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Simultaneous predatory and prey-independent growth by B. bacteriovorus Tiberius. (a) Plaques formed by lysis of prey within lawns of prey cells by B. bacteriovorus(i) HD100 clear plaque and (ii) Tiberius plaque with central colony growth. (b) Light microscopy images of serpentine prey-independently growing Tiberius cells alongside free-swimming Bdellovibrio cells and bdelloplasts. (c) Electron microscopy of Tiberius cells (i & ii) attack phase, predatory cells (iii-v) filamentous, prey-independently growing cells from the same samples as in (i & ii). (d – f) Timelapse microscopy still images (from all T= timepoint in minutes from addition of bdellovibrios to slide) from movies showing: (d) co-existence of long HI prey-independently growing cells (black arrows) and comma-shaped predatory B. bacteriovorus Tiberius invading an E. coli prey cell (white arrow); (e) evidence that the outcome of prey entry by B. bacteriovorus Tiberius results in bdellovibrio replication- one cell enters at T=0 and three leave upon prey lysis at T=300; (f) septation by binary fission of the long prey-independently growing form of B. bacteriovorus Tiberius. (g) Diagram comparing the modes of growth of B. bacteriovorus HD100 and Tiberius in both high and low nutrient conditions, showing simultaneous predatory and prey-independent growth by Tiberius in low nutrient conditions. (h) Cell pellets of predatory cells showing the white cells of B. bacteriovorus Tiberius against the yellow, carotenoid-producing, cells of strain HD100.
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Figure 1: Simultaneous predatory and prey-independent growth by B. bacteriovorus Tiberius. (a) Plaques formed by lysis of prey within lawns of prey cells by B. bacteriovorus(i) HD100 clear plaque and (ii) Tiberius plaque with central colony growth. (b) Light microscopy images of serpentine prey-independently growing Tiberius cells alongside free-swimming Bdellovibrio cells and bdelloplasts. (c) Electron microscopy of Tiberius cells (i & ii) attack phase, predatory cells (iii-v) filamentous, prey-independently growing cells from the same samples as in (i & ii). (d – f) Timelapse microscopy still images (from all T= timepoint in minutes from addition of bdellovibrios to slide) from movies showing: (d) co-existence of long HI prey-independently growing cells (black arrows) and comma-shaped predatory B. bacteriovorus Tiberius invading an E. coli prey cell (white arrow); (e) evidence that the outcome of prey entry by B. bacteriovorus Tiberius results in bdellovibrio replication- one cell enters at T=0 and three leave upon prey lysis at T=300; (f) septation by binary fission of the long prey-independently growing form of B. bacteriovorus Tiberius. (g) Diagram comparing the modes of growth of B. bacteriovorus HD100 and Tiberius in both high and low nutrient conditions, showing simultaneous predatory and prey-independent growth by Tiberius in low nutrient conditions. (h) Cell pellets of predatory cells showing the white cells of B. bacteriovorus Tiberius against the yellow, carotenoid-producing, cells of strain HD100.

Mentions: Predatory cultures of well-studied B. bacteriovorus HD100 and 109J form clear plaques on prey lawns (Figure1a (i)) and are composed solely of vibroid attack-phase cells. However, pure, predatory cultures of the Tiberius strain formed plaques on E. coli lawns each containing a central zone where a small Bdellovibrio micro-colony was seen (Figure1a (ii)). B. bacteriovorus Tiberius from the plaques and the predatory liquid cultures derived from them, contained a mix of vibroid and long serpentine morphotypes the latter with spherical regions (Figure1b and1c). The long cells resembled axenically-growing prey/host-independent (HI) Bdellovibrio, reported by Friedberg[10] and Reiner and Shilo[11]. The distinctive colony-centred plaques continued even after serial passage of the strain, derived from single plaques, predatorily, repeatedly on prey showing that pure cultures contain both cell types. That a pure strain had been isolated was backed up by examination of restriction digest and Southern blot hybridisation patterns for DNA derived from multiple cultures of the Tiberius strain (data not shown) no variation was detected which would have indicated two strains rather than one. 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 file1) where it clustered with Bdellovibrio bacteriovorus (rather than Bacteriovorax) strains, including the type strain HD100 and the well-characterised lab strain 109J[12,13].


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.

Hobley L, Lerner TR, Williams LE, Lambert C, Till R, Milner DS, Basford SM, Capeness MJ, Fenton AK, Atterbury RJ, Harris MA, Sockett RE - BMC Genomics (2012)

Simultaneous predatory and prey-independent growth by B. bacteriovorus Tiberius. (a) Plaques formed by lysis of prey within lawns of prey cells by B. bacteriovorus(i) HD100 clear plaque and (ii) Tiberius plaque with central colony growth. (b) Light microscopy images of serpentine prey-independently growing Tiberius cells alongside free-swimming Bdellovibrio cells and bdelloplasts. (c) Electron microscopy of Tiberius cells (i & ii) attack phase, predatory cells (iii-v) filamentous, prey-independently growing cells from the same samples as in (i & ii). (d – f) Timelapse microscopy still images (from all T= timepoint in minutes from addition of bdellovibrios to slide) from movies showing: (d) co-existence of long HI prey-independently growing cells (black arrows) and comma-shaped predatory B. bacteriovorus Tiberius invading an E. coli prey cell (white arrow); (e) evidence that the outcome of prey entry by B. bacteriovorus Tiberius results in bdellovibrio replication- one cell enters at T=0 and three leave upon prey lysis at T=300; (f) septation by binary fission of the long prey-independently growing form of B. bacteriovorus Tiberius. (g) Diagram comparing the modes of growth of B. bacteriovorus HD100 and Tiberius in both high and low nutrient conditions, showing simultaneous predatory and prey-independent growth by Tiberius in low nutrient conditions. (h) Cell pellets of predatory cells showing the white cells of B. bacteriovorus Tiberius against the yellow, carotenoid-producing, cells of strain HD100.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3539863&req=5

Figure 1: Simultaneous predatory and prey-independent growth by B. bacteriovorus Tiberius. (a) Plaques formed by lysis of prey within lawns of prey cells by B. bacteriovorus(i) HD100 clear plaque and (ii) Tiberius plaque with central colony growth. (b) Light microscopy images of serpentine prey-independently growing Tiberius cells alongside free-swimming Bdellovibrio cells and bdelloplasts. (c) Electron microscopy of Tiberius cells (i & ii) attack phase, predatory cells (iii-v) filamentous, prey-independently growing cells from the same samples as in (i & ii). (d – f) Timelapse microscopy still images (from all T= timepoint in minutes from addition of bdellovibrios to slide) from movies showing: (d) co-existence of long HI prey-independently growing cells (black arrows) and comma-shaped predatory B. bacteriovorus Tiberius invading an E. coli prey cell (white arrow); (e) evidence that the outcome of prey entry by B. bacteriovorus Tiberius results in bdellovibrio replication- one cell enters at T=0 and three leave upon prey lysis at T=300; (f) septation by binary fission of the long prey-independently growing form of B. bacteriovorus Tiberius. (g) Diagram comparing the modes of growth of B. bacteriovorus HD100 and Tiberius in both high and low nutrient conditions, showing simultaneous predatory and prey-independent growth by Tiberius in low nutrient conditions. (h) Cell pellets of predatory cells showing the white cells of B. bacteriovorus Tiberius against the yellow, carotenoid-producing, cells of strain HD100.
Mentions: Predatory cultures of well-studied B. bacteriovorus HD100 and 109J form clear plaques on prey lawns (Figure1a (i)) and are composed solely of vibroid attack-phase cells. However, pure, predatory cultures of the Tiberius strain formed plaques on E. coli lawns each containing a central zone where a small Bdellovibrio micro-colony was seen (Figure1a (ii)). B. bacteriovorus Tiberius from the plaques and the predatory liquid cultures derived from them, contained a mix of vibroid and long serpentine morphotypes the latter with spherical regions (Figure1b and1c). The long cells resembled axenically-growing prey/host-independent (HI) Bdellovibrio, reported by Friedberg[10] and Reiner and Shilo[11]. The distinctive colony-centred plaques continued even after serial passage of the strain, derived from single plaques, predatorily, repeatedly on prey showing that pure cultures contain both cell types. That a pure strain had been isolated was backed up by examination of restriction digest and Southern blot hybridisation patterns for DNA derived from multiple cultures of the Tiberius strain (data not shown) no variation was detected which would have indicated two strains rather than one. 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 file1) where it clustered with Bdellovibrio bacteriovorus (rather than Bacteriovorax) strains, including the type strain HD100 and the well-characterised lab strain 109J[12,13].

Bottom Line: Bdellovibrio were previously described as "obligate predators" because only by mutations, often in gene bd0108, are 1 in ~1x10(7) of predatory lab strains of Bdellovibrio converted to prey-independent growth.However the Doolittle and Pan groups predicted, in silico, both ancient and recent lateral gene transfer into the B. bacteriovorus HD100 genome.Despite the prey-independent growth, the homolog of bd0108 did not have typical prey-independent-type mutations.

View Article: PubMed Central - HTML - PubMed

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

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 ~1x10(7) 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.

Show MeSH
Related in: MedlinePlus