Limits...
Global analysis of host response to induction of a latent bacteriophage.

Osterhout RE, Figueroa IA, Keasling JD, Arkin AP - BMC Microbiol. (2007)

Bottom Line: Though statistically significant, most of the changes in these genes were mild, with only 140 genes showing greater than two-fold change.Overall, we observe that prophage induction has a surprisingly low impact on host physiology.This study provides the first global dynamic picture of how host processes respond to lambda phage induction.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Bioengineering and Howard Hughes Medical Institute, University of California at Berkeley, Berkeley, CA 94720, USA. reosterhout@berkeley.edu

ABSTRACT

Background: The transition from viral latency to lytic growth involves complex interactions among host and viral factors, and the extent to which host physiology is buffered from the virus during induction of lysis is not known. A reasonable hypothesis is that the virus should be evolutionarily selected to ensure host health throughout induction to minimize its chance of reproductive failure. To address this question, we collected transcriptional profiles of Escherichia coli and bacteriophage lambda throughout lysogenic induction by UV light.

Results: We observed a temporally coordinated program of phage gene expression, with distinct early, middle and late transcriptional classes. Our study confirmed known host-phage interactions of induction of the heat shock regulon, escape replication, and suppression of genes involved in cell division and initiation of replication. We identified 728 E. coli genes responsive to prophage induction, which included pleiotropic stress response pathways, the Arc and Cpx regulons, and global regulators crp and lrp. Several hundred genes involved in central metabolism, energy metabolism, translation and transport were down-regulated late in induction. Though statistically significant, most of the changes in these genes were mild, with only 140 genes showing greater than two-fold change.

Conclusion: Overall, we observe that prophage induction has a surprisingly low impact on host physiology. This study provides the first global dynamic picture of how host processes respond to lambda phage induction.

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Related in: MedlinePlus

Escherichia coli lambda lysogen DNA and average transcript levels after treatment with 10 J/m2 UV light. The x-axis is the position of genes on the E. coli chromosome. The E. coli origin is at the 0 position on the x-axis. The lambda integration site attB is indicated by the vertical line. The y-axis is the log ratio of treated to untreated cells. A). Average transcription (100 bins) along the E. coli chromosome at 20, 40, 60 minutes after exposure to UV light. B). Ratio of DNA 60 minutes after treatment with UV light relative to DNA of untreated cells.
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Figure 3: Escherichia coli lambda lysogen DNA and average transcript levels after treatment with 10 J/m2 UV light. The x-axis is the position of genes on the E. coli chromosome. The E. coli origin is at the 0 position on the x-axis. The lambda integration site attB is indicated by the vertical line. The y-axis is the log ratio of treated to untreated cells. A). Average transcription (100 bins) along the E. coli chromosome at 20, 40, 60 minutes after exposure to UV light. B). Ratio of DNA 60 minutes after treatment with UV light relative to DNA of untreated cells.

Mentions: Genes in the gal operon, adjacent to the phage integration site attB, are amplified during prophage induction in E. coli; this amplification has been attributed to increase in gene dosage due to escape replication from the prophage origin [19] and trans-acting antitermination by lambda-N [6,20]. In data presented here, transcription of gal operon genes was enhanced nearly 13-fold in lysogens relative to non-lysogens, as expected. In addition to the gal operon, we observed enhancement of transcription in a 300-kb region surrounding the prophage integration site, attB (Figure 3A). The boundaries of this region were defined by binning the average expression fold-change at defined intervals. In the attB region, 126 genes demonstrated 1.4-fold or higher up-regulation; no genes in the region were down-regulated. As distance from attB increased, the average fold-change of host genes decreased.


Global analysis of host response to induction of a latent bacteriophage.

Osterhout RE, Figueroa IA, Keasling JD, Arkin AP - BMC Microbiol. (2007)

Escherichia coli lambda lysogen DNA and average transcript levels after treatment with 10 J/m2 UV light. The x-axis is the position of genes on the E. coli chromosome. The E. coli origin is at the 0 position on the x-axis. The lambda integration site attB is indicated by the vertical line. The y-axis is the log ratio of treated to untreated cells. A). Average transcription (100 bins) along the E. coli chromosome at 20, 40, 60 minutes after exposure to UV light. B). Ratio of DNA 60 minutes after treatment with UV light relative to DNA of untreated cells.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2147009&req=5

Figure 3: Escherichia coli lambda lysogen DNA and average transcript levels after treatment with 10 J/m2 UV light. The x-axis is the position of genes on the E. coli chromosome. The E. coli origin is at the 0 position on the x-axis. The lambda integration site attB is indicated by the vertical line. The y-axis is the log ratio of treated to untreated cells. A). Average transcription (100 bins) along the E. coli chromosome at 20, 40, 60 minutes after exposure to UV light. B). Ratio of DNA 60 minutes after treatment with UV light relative to DNA of untreated cells.
Mentions: Genes in the gal operon, adjacent to the phage integration site attB, are amplified during prophage induction in E. coli; this amplification has been attributed to increase in gene dosage due to escape replication from the prophage origin [19] and trans-acting antitermination by lambda-N [6,20]. In data presented here, transcription of gal operon genes was enhanced nearly 13-fold in lysogens relative to non-lysogens, as expected. In addition to the gal operon, we observed enhancement of transcription in a 300-kb region surrounding the prophage integration site, attB (Figure 3A). The boundaries of this region were defined by binning the average expression fold-change at defined intervals. In the attB region, 126 genes demonstrated 1.4-fold or higher up-regulation; no genes in the region were down-regulated. As distance from attB increased, the average fold-change of host genes decreased.

Bottom Line: Though statistically significant, most of the changes in these genes were mild, with only 140 genes showing greater than two-fold change.Overall, we observe that prophage induction has a surprisingly low impact on host physiology.This study provides the first global dynamic picture of how host processes respond to lambda phage induction.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Bioengineering and Howard Hughes Medical Institute, University of California at Berkeley, Berkeley, CA 94720, USA. reosterhout@berkeley.edu

ABSTRACT

Background: The transition from viral latency to lytic growth involves complex interactions among host and viral factors, and the extent to which host physiology is buffered from the virus during induction of lysis is not known. A reasonable hypothesis is that the virus should be evolutionarily selected to ensure host health throughout induction to minimize its chance of reproductive failure. To address this question, we collected transcriptional profiles of Escherichia coli and bacteriophage lambda throughout lysogenic induction by UV light.

Results: We observed a temporally coordinated program of phage gene expression, with distinct early, middle and late transcriptional classes. Our study confirmed known host-phage interactions of induction of the heat shock regulon, escape replication, and suppression of genes involved in cell division and initiation of replication. We identified 728 E. coli genes responsive to prophage induction, which included pleiotropic stress response pathways, the Arc and Cpx regulons, and global regulators crp and lrp. Several hundred genes involved in central metabolism, energy metabolism, translation and transport were down-regulated late in induction. Though statistically significant, most of the changes in these genes were mild, with only 140 genes showing greater than two-fold change.

Conclusion: Overall, we observe that prophage induction has a surprisingly low impact on host physiology. This study provides the first global dynamic picture of how host processes respond to lambda phage induction.

Show MeSH
Related in: MedlinePlus