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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 cell growth.Growth in LB at 37 °C (a) and M9C at 30 °C (b) for Δ9 (open circle) and the wild-type strain (filled circle). Growth of the nine individual prophage deletion strains (CP4-6, open diamond; DLP12, filled diamond; e14, open hexagon; rac, inverted open triangle; Qin, filled triangle; CPS-53, inverted filled triangle; CP4-44, open square; CPZ-55, open triangle and CP4-57, filled square), Δ9 (open circle) and the wild-type strain (filled circle) in LB at 37 °C (c) and M9C lactate at 37 °C (d). Error bars indicate s.d. values (n=3).
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f2: Cryptic prophage genes influence cell growth.Growth in LB at 37 °C (a) and M9C at 30 °C (b) for Δ9 (open circle) and the wild-type strain (filled circle). Growth of the nine individual prophage deletion strains (CP4-6, open diamond; DLP12, filled diamond; e14, open hexagon; rac, inverted open triangle; Qin, filled triangle; CPS-53, inverted filled triangle; CP4-44, open square; CPZ-55, open triangle and CP4-57, filled square), Δ9 (open circle) and the wild-type strain (filled circle) in LB at 37 °C (c) and M9C lactate at 37 °C (d). Error bars indicate s.d. values (n=3).

Mentions: To assess the overall effect of harbouring nine cryptic prophages (Fig. 1) on E. coli host physiology, growth of the Δ9 strain (Table 1) was tested in nutrient-rich medium at 37 °C (to mimic conditions that E. coli should encounter in the gastrointestinal tract) and in nutrient-poor medium at 30 °C (to mimic the cooler temperatures likely to be experienced by E. coli outside the human host). The maximum specific growth rates for Δ9 were decreased slightly in both media (1.36±0.01 versus 1.46±0.02 h−1 in rich medium and 0.25±0.02 versus 0.28±0.01 h−1 in minimal medium for Δ9 and the wild-type strain, respectively); however, the prophage-deleted cells had decreased yields on these substrates (Fig. 2a,b). In addition, growth of each of the nine individual prophage-deletion strains (Table 2) was tested. Among the nine strains, growth in both media was reduced the most on removing CP4-57 (Fig. 2c,d). Hence, prophages confer the ability to grow more rapidly and to obtain higher yields on nutrients.


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 cell growth.Growth in LB at 37 °C (a) and M9C at 30 °C (b) for Δ9 (open circle) and the wild-type strain (filled circle). Growth of the nine individual prophage deletion strains (CP4-6, open diamond; DLP12, filled diamond; e14, open hexagon; rac, inverted open triangle; Qin, filled triangle; CPS-53, inverted filled triangle; CP4-44, open square; CPZ-55, open triangle and CP4-57, filled square), Δ9 (open circle) and the wild-type strain (filled circle) in LB at 37 °C (c) and M9C lactate at 37 °C (d). Error bars indicate s.d. values (n=3).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3105296&req=5

f2: Cryptic prophage genes influence cell growth.Growth in LB at 37 °C (a) and M9C at 30 °C (b) for Δ9 (open circle) and the wild-type strain (filled circle). Growth of the nine individual prophage deletion strains (CP4-6, open diamond; DLP12, filled diamond; e14, open hexagon; rac, inverted open triangle; Qin, filled triangle; CPS-53, inverted filled triangle; CP4-44, open square; CPZ-55, open triangle and CP4-57, filled square), Δ9 (open circle) and the wild-type strain (filled circle) in LB at 37 °C (c) and M9C lactate at 37 °C (d). Error bars indicate s.d. values (n=3).
Mentions: To assess the overall effect of harbouring nine cryptic prophages (Fig. 1) on E. coli host physiology, growth of the Δ9 strain (Table 1) was tested in nutrient-rich medium at 37 °C (to mimic conditions that E. coli should encounter in the gastrointestinal tract) and in nutrient-poor medium at 30 °C (to mimic the cooler temperatures likely to be experienced by E. coli outside the human host). The maximum specific growth rates for Δ9 were decreased slightly in both media (1.36±0.01 versus 1.46±0.02 h−1 in rich medium and 0.25±0.02 versus 0.28±0.01 h−1 in minimal medium for Δ9 and the wild-type strain, respectively); however, the prophage-deleted cells had decreased yields on these substrates (Fig. 2a,b). In addition, growth of each of the nine individual prophage-deletion strains (Table 2) was tested. Among the nine strains, growth in both media was reduced the most on removing CP4-57 (Fig. 2c,d). Hence, prophages confer the ability to grow more rapidly and to obtain higher yields on nutrients.

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