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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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Related in: MedlinePlus

Whole genome comparison of the B. bacteriovorus Tiberius and HD100 strains. DNAplotter[16] was used to compare the genomes of the (A) Tiberius and (B) HD100 strains. The circles represent (from outer to inner): CDS on plus strand; CDS on minus strand; tRNAs (pink) and rRNA operons (navy); regions of homology between the two genomes (blue); % GC plot (yellow=above average, purple=below average); and GC skew ([G-C]/[G+C]).
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Figure 2: Whole genome comparison of the B. bacteriovorus Tiberius and HD100 strains. DNAplotter[16] was used to compare the genomes of the (A) Tiberius and (B) HD100 strains. The circles represent (from outer to inner): CDS on plus strand; CDS on minus strand; tRNAs (pink) and rRNA operons (navy); regions of homology between the two genomes (blue); % GC plot (yellow=above average, purple=below average); and GC skew ([G-C]/[G+C]).

Mentions: Despite the differences in predatory versus prey-independent lifestyle regulation and terrestrial versus aquatic environments; there was extensive synteny (Figure2 and Additional file5), approximate conservation of genome size (3,988,594 bp, 3,738 protein coding genes for B. bacteriovorus Tiberius versus 3,782,950 bp, 3,587 protein coding genes for B. bacteriovorus HD100), codon usage and conservation of the number and loci of rRNA and tRNA genes (bar one tRNA gene) (Figure2). There were however differences in genomic content which were analysed further.


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)

Whole genome comparison of the B. bacteriovorus Tiberius and HD100 strains. DNAplotter[16] was used to compare the genomes of the (A) Tiberius and (B) HD100 strains. The circles represent (from outer to inner): CDS on plus strand; CDS on minus strand; tRNAs (pink) and rRNA operons (navy); regions of homology between the two genomes (blue); % GC plot (yellow=above average, purple=below average); and GC skew ([G-C]/[G+C]).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Whole genome comparison of the B. bacteriovorus Tiberius and HD100 strains. DNAplotter[16] was used to compare the genomes of the (A) Tiberius and (B) HD100 strains. The circles represent (from outer to inner): CDS on plus strand; CDS on minus strand; tRNAs (pink) and rRNA operons (navy); regions of homology between the two genomes (blue); % GC plot (yellow=above average, purple=below average); and GC skew ([G-C]/[G+C]).
Mentions: Despite the differences in predatory versus prey-independent lifestyle regulation and terrestrial versus aquatic environments; there was extensive synteny (Figure2 and Additional file5), approximate conservation of genome size (3,988,594 bp, 3,738 protein coding genes for B. bacteriovorus Tiberius versus 3,782,950 bp, 3,587 protein coding genes for B. bacteriovorus HD100), codon usage and conservation of the number and loci of rRNA and tRNA genes (bar one tRNA gene) (Figure2). There were however differences in genomic content which were analysed further.

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