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Cryptic prophages help bacteria cope with adverse environments.

Wang X, Kim Y, Ma Q, Hong SH, Pokusaeva K, Sturino JM, Wood TK - Nat Commun (2010)

Bottom Line: We find that cryptic prophages contribute significantly to resistance to sub-lethal concentrations of quinolone and β-lactam antibiotics primarily through proteins that inhibit cell division (for example, KilR of rac and DicB of Qin).Moreover, the prophages are beneficial for withstanding osmotic, oxidative and acid stresses, for increasing growth, and for influencing biofilm formation.Therefore, cryptic prophages provide multiple benefits to the host for surviving adverse environmental conditions.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemical Engineering, Texas A & M University, 220 Jack E. Brown Building, College Station, Texas 77843-3122, USA.

ABSTRACT
Phages are the most abundant entity in the biosphere and outnumber bacteria by a factor of 10. Phage DNA may also constitute 20% of bacterial genomes; however, its role is ill defined. Here, we explore the impact of cryptic prophages on cell physiology by precisely deleting all nine prophage elements (166 kbp) using Escherichia coli. We find that cryptic prophages contribute significantly to resistance to sub-lethal concentrations of quinolone and β-lactam antibiotics primarily through proteins that inhibit cell division (for example, KilR of rac and DicB of Qin). Moreover, the prophages are beneficial for withstanding osmotic, oxidative and acid stresses, for increasing growth, and for influencing biofilm formation. Prophage CPS-53 proteins YfdK, YfdO and YfdS enhanced resistance to oxidative stress, prophages e14, CPS-53 and CP4-57 increased resistance to acid, and e14 and rac proteins increased early biofilm formation. Therefore, cryptic prophages provide multiple benefits to the host for surviving adverse environmental conditions.

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Cryptic prophage genes influence stress-related phenotypes.(a) Summary of the PM results for the wild-type strain versus Δ9. The fold changes indicate the relative difference in the average slope in the growth curves multiplied by the area under the curves, which is indicative of cell respiration. From left to right, with the MIC indicated for the wild-type strain in parenthesis, quinolones include nalidixic acid (4 μg ml−1), oxolinic acid (0.9 μg ml−1), ofloxacin (0.048 μg ml−1) and novobiocin (132 μg ml−1); β-lactams include nafcillin (320 μg ml−1), azlocillin (17.6 μg ml−1), cephalothin (5.12 μg ml−1) and moxalactam (0.27 μg ml−1); osmolytes include 5% NaCl, 6% NaCl, 6% KCl and 2% sodium formate; and the other stresses include thallium acetate and potassium tellurite. All chemicals shown here were significantly repressed for Δ9 versus wild-type strain (P<0.05 using a paired t-test). Error bars indicate s.e.m. (n=3). (b) Efficiency of colony formation for Δ9 and the wild-type strain with sublethal concentrations of nalidixic acid (2 μg ml−1) and azlocillin (5 μg ml−1) as well as with 6% NaCl. Powers of 10 indicate the amount of dilution. Scale bar represents 10 mm. (c) Cell morphology for Δ9 and wild-type strain after treating with 2 μg ml−1 nalidixic acid for 2 h. Scale bar represents 10 μm.
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f3: Cryptic prophage genes influence stress-related phenotypes.(a) Summary of the PM results for the wild-type strain versus Δ9. The fold changes indicate the relative difference in the average slope in the growth curves multiplied by the area under the curves, which is indicative of cell respiration. From left to right, with the MIC indicated for the wild-type strain in parenthesis, quinolones include nalidixic acid (4 μg ml−1), oxolinic acid (0.9 μg ml−1), ofloxacin (0.048 μg ml−1) and novobiocin (132 μg ml−1); β-lactams include nafcillin (320 μg ml−1), azlocillin (17.6 μg ml−1), cephalothin (5.12 μg ml−1) and moxalactam (0.27 μg ml−1); osmolytes include 5% NaCl, 6% NaCl, 6% KCl and 2% sodium formate; and the other stresses include thallium acetate and potassium tellurite. All chemicals shown here were significantly repressed for Δ9 versus wild-type strain (P<0.05 using a paired t-test). Error bars indicate s.e.m. (n=3). (b) Efficiency of colony formation for Δ9 and the wild-type strain with sublethal concentrations of nalidixic acid (2 μg ml−1) and azlocillin (5 μg ml−1) as well as with 6% NaCl. Powers of 10 indicate the amount of dilution. Scale bar represents 10 mm. (c) Cell morphology for Δ9 and wild-type strain after treating with 2 μg ml−1 nalidixic acid for 2 h. Scale bar represents 10 μm.

Mentions: To examine the impact of deleting the nine cryptic prophages on specific aspects of E. coli physiology, we used phenotype microarrays (PMs) so that 1,240 different metabolic conditions could be rapidly assayed in a high-throughput manner13; this method both amplifies and quantifies the differences in metabolism of the strains. Using plates PM 11–13, six quinolone antibiotics (four shown in Fig. 3a and six in Supplementary Table S1) dramatically inhibited the growth of Δ9 at concentrations that are 1/2 of the minimum inhibitory concentration (MIC) for the wild-type strain. These include first generation oxolinic acid and nalidixic acid, second-generation enoxacin, lomefloxacin and ofloxacin, and the related novobiocin agent. Quinolones are broad-spectrum antibacterial agents that are becoming increasingly popular and account for 18% of the antibacterial market (2006)14.


Cryptic prophages help bacteria cope with adverse environments.

Wang X, Kim Y, Ma Q, Hong SH, Pokusaeva K, Sturino JM, Wood TK - Nat Commun (2010)

Cryptic prophage genes influence stress-related phenotypes.(a) Summary of the PM results for the wild-type strain versus Δ9. The fold changes indicate the relative difference in the average slope in the growth curves multiplied by the area under the curves, which is indicative of cell respiration. From left to right, with the MIC indicated for the wild-type strain in parenthesis, quinolones include nalidixic acid (4 μg ml−1), oxolinic acid (0.9 μg ml−1), ofloxacin (0.048 μg ml−1) and novobiocin (132 μg ml−1); β-lactams include nafcillin (320 μg ml−1), azlocillin (17.6 μg ml−1), cephalothin (5.12 μg ml−1) and moxalactam (0.27 μg ml−1); osmolytes include 5% NaCl, 6% NaCl, 6% KCl and 2% sodium formate; and the other stresses include thallium acetate and potassium tellurite. All chemicals shown here were significantly repressed for Δ9 versus wild-type strain (P<0.05 using a paired t-test). Error bars indicate s.e.m. (n=3). (b) Efficiency of colony formation for Δ9 and the wild-type strain with sublethal concentrations of nalidixic acid (2 μg ml−1) and azlocillin (5 μg ml−1) as well as with 6% NaCl. Powers of 10 indicate the amount of dilution. Scale bar represents 10 mm. (c) Cell morphology for Δ9 and wild-type strain after treating with 2 μg ml−1 nalidixic acid for 2 h. Scale bar represents 10 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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f3: Cryptic prophage genes influence stress-related phenotypes.(a) Summary of the PM results for the wild-type strain versus Δ9. The fold changes indicate the relative difference in the average slope in the growth curves multiplied by the area under the curves, which is indicative of cell respiration. From left to right, with the MIC indicated for the wild-type strain in parenthesis, quinolones include nalidixic acid (4 μg ml−1), oxolinic acid (0.9 μg ml−1), ofloxacin (0.048 μg ml−1) and novobiocin (132 μg ml−1); β-lactams include nafcillin (320 μg ml−1), azlocillin (17.6 μg ml−1), cephalothin (5.12 μg ml−1) and moxalactam (0.27 μg ml−1); osmolytes include 5% NaCl, 6% NaCl, 6% KCl and 2% sodium formate; and the other stresses include thallium acetate and potassium tellurite. All chemicals shown here were significantly repressed for Δ9 versus wild-type strain (P<0.05 using a paired t-test). Error bars indicate s.e.m. (n=3). (b) Efficiency of colony formation for Δ9 and the wild-type strain with sublethal concentrations of nalidixic acid (2 μg ml−1) and azlocillin (5 μg ml−1) as well as with 6% NaCl. Powers of 10 indicate the amount of dilution. Scale bar represents 10 mm. (c) Cell morphology for Δ9 and wild-type strain after treating with 2 μg ml−1 nalidixic acid for 2 h. Scale bar represents 10 μm.
Mentions: To examine the impact of deleting the nine cryptic prophages on specific aspects of E. coli physiology, we used phenotype microarrays (PMs) so that 1,240 different metabolic conditions could be rapidly assayed in a high-throughput manner13; this method both amplifies and quantifies the differences in metabolism of the strains. Using plates PM 11–13, six quinolone antibiotics (four shown in Fig. 3a and six in Supplementary Table S1) dramatically inhibited the growth of Δ9 at concentrations that are 1/2 of the minimum inhibitory concentration (MIC) for the wild-type strain. These include first generation oxolinic acid and nalidixic acid, second-generation enoxacin, lomefloxacin and ofloxacin, and the related novobiocin agent. Quinolones are broad-spectrum antibacterial agents that are becoming increasingly popular and account for 18% of the antibacterial market (2006)14.

Bottom Line: We find that cryptic prophages contribute significantly to resistance to sub-lethal concentrations of quinolone and β-lactam antibiotics primarily through proteins that inhibit cell division (for example, KilR of rac and DicB of Qin).Moreover, the prophages are beneficial for withstanding osmotic, oxidative and acid stresses, for increasing growth, and for influencing biofilm formation.Therefore, cryptic prophages provide multiple benefits to the host for surviving adverse environmental conditions.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemical Engineering, Texas A & M University, 220 Jack E. Brown Building, College Station, Texas 77843-3122, USA.

ABSTRACT
Phages are the most abundant entity in the biosphere and outnumber bacteria by a factor of 10. Phage DNA may also constitute 20% of bacterial genomes; however, its role is ill defined. Here, we explore the impact of cryptic prophages on cell physiology by precisely deleting all nine prophage elements (166 kbp) using Escherichia coli. We find that cryptic prophages contribute significantly to resistance to sub-lethal concentrations of quinolone and β-lactam antibiotics primarily through proteins that inhibit cell division (for example, KilR of rac and DicB of Qin). Moreover, the prophages are beneficial for withstanding osmotic, oxidative and acid stresses, for increasing growth, and for influencing biofilm formation. Prophage CPS-53 proteins YfdK, YfdO and YfdS enhanced resistance to oxidative stress, prophages e14, CPS-53 and CP4-57 increased resistance to acid, and e14 and rac proteins increased early biofilm formation. Therefore, cryptic prophages provide multiple benefits to the host for surviving adverse environmental conditions.

Show MeSH
Related in: MedlinePlus