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17 pages, 3021 KiB

Open AccessArticle

Low Host Abundance and High Temperature Determine Switching from Lytic to Lysogenic Cycles in Planktonic Microbial Communities in a Tropical Sea (Red Sea)

by Ruba Abdulrahman Ashy and Susana Agustí

Viruses 2020, 12(7), 761; https://0-doi-org.brum.beds.ac.uk/10.3390/v12070761 - 15 Jul 2020

Cited by 12 | Viewed by 3552

Abstract

The lytic and lysogenic life cycles of marine phages are influenced by environmental conditions such as solar radiation, temperature, and host abundance. Temperature can regulate phage infection, but its role is difficult to discern in oligotrophic waters where there is typically low host [...] Read more.

The lytic and lysogenic life cycles of marine phages are influenced by environmental conditions such as solar radiation, temperature, and host abundance. Temperature can regulate phage infection, but its role is difficult to discern in oligotrophic waters where there is typically low host abundance and high temperatures. Here, we study the temporal variability of viral dynamics and the occurrence of lysogeny using mitomycin C in a eutrophic coastal lagoon in the oligotrophic Red Sea, which showed strong seasonality in terms of temperature (22.1–33.3 °C) and large phytoplankton blooms. Viral abundances ranged from 2.2 × 10⁶ to 1.5 × 10⁷ viruses mL⁻¹ and were closely related to chlorophyll a (chl a) concentration. Observed high virus-to-bacterium ratio (VBR) (4–79; 16 ± 4 (SE)) suggests that phages exerted a tight control of their hosts as indicated by the significant decrease in bacterial abundance with increasing virus concentration. Heterotrophic bacterial abundance also showed a significant decrease with increasing temperature. However, viral abundance was not related to temperature changes and the interaction of water temperature, suggesting an indirect effect of temperature on decreased host abundance, which was observed at the end of the summertime. From the estimated burst size (BS), we observed lysogeny (undetectable to 29.1%) at low percentages of 5.0% ± 1.2 (SE) in half of the incubations with mitomycin C, while it increased to 23.9% ± 2.8 (SE) when the host abundance decreased. The results suggest that lytic phages predominate, switching to a moderate proportion of temperate phages when the host abundance reduces. Full article

(This article belongs to the Special Issue Phage Ecology)

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18 pages, 2978 KiB

Open AccessArticle

Isolation and Characterization of Bacteriophages That Infect Citrobacter rodentium, a Model Pathogen for Intestinal Diseases

by Carolina M. Mizuno, Tiffany Luong, Robert Cederstrom, Mart Krupovic, Laurent Debarbieux and Dwayne R. Roach

Viruses 2020, 12(7), 737; https://0-doi-org.brum.beds.ac.uk/10.3390/v12070737 - 08 Jul 2020

Cited by 12 | Viewed by 3551

Abstract

Enteropathogenic Escherichia coli (EPEC) is a major pathogen for diarrheal diseases among children. Antibiotics, when used appropriately, are effective; however, their overuse and misuse have led to the rise of antibiotic resistance worldwide. Thus, there are renewed efforts into the development of phage [...] Read more.

Enteropathogenic Escherichia coli (EPEC) is a major pathogen for diarrheal diseases among children. Antibiotics, when used appropriately, are effective; however, their overuse and misuse have led to the rise of antibiotic resistance worldwide. Thus, there are renewed efforts into the development of phage therapy as an alternative antibacterial therapy. Because EPEC in vivo models have shortcomings, a surrogate is used to study the mouse pathogen Citrobacter rodentium in animal models. In this study, two new phages CrRp3 and CrRp10, which infect C. rodentium, were isolated and characterized. CrRp3 was found to be a new species within the genus Vectrevirus, and CrRp10 is a new strain within the species Escherichia virus Ime09, in the genus Tequatrovirus. Both phages appear to have independently evolved from E. coli phages, rather than other Citrobacter spp. phages. Neither phage strain carries known genes associated with bacterial virulence, antibiotic resistance, or lysogeny. CrRp3 is more potent, having a 24-fold faster adsorption rate and shorter lytic cycle when compared to the same properties of CrRp10. However, a lysis curve analysis revealed that CrRp10 prevented growth of C. rodentium for 18 h, whereas resistance developed against CrRp3 within 9 h. We also show that hypoxic (5% oxygen) conditions decreased CrRp3 ability to control bacterial densities in culture. In contrast, low oxygen conditions did not affect CrRp10 ability to replicate on C. rodentium. Together, CrRp10 is likely to be the better candidate for future phage therapy investigations. Full article

(This article belongs to the Special Issue Phage Ecology)

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14 pages, 829 KiB

Open AccessArticle

The Single-Stranded RNA Bacteriophage Qβ Adapts Rapidly to High Temperatures: An Evolution Experiment

by Md. Tanvir Hossain, Toma Yokono and Akiko Kashiwagi

Viruses 2020, 12(6), 638; https://0-doi-org.brum.beds.ac.uk/10.3390/v12060638 - 12 Jun 2020

Cited by 2 | Viewed by 2564

Abstract

Single-stranded (ss)RNA viruses are thought to evolve rapidly due to an inherently high mutation rate. However, it remains unclear how ssRNA viruses adapt to novel environments and/or how many and what types of substitutions are needed to facilitate this evolution. In this study, [...] Read more.

Single-stranded (ss)RNA viruses are thought to evolve rapidly due to an inherently high mutation rate. However, it remains unclear how ssRNA viruses adapt to novel environments and/or how many and what types of substitutions are needed to facilitate this evolution. In this study, we followed the adaptation of the ssRNA bacteriophage Qβ using thermally adapted Escherichia coli as a host, which can efficiently grow at temperatures between 37.2 and 45.3 °C. This made it possible to evaluate Qβ adaptation to the highest known temperature that supports growth, 45.3 °C. We found that Qβ was capable of replication at this temperature; within 114 days (~1260 generations), we detected more than 34 novel point mutations in the genome of the thermally adapted Qβ population, representing 0.8% of the total Qβ genome. In addition, we returned the 45.3 °C-adapted Qβ populations to 37.2 °C and passaged them for 8 days (~124 generations). We found that the reverse-adapted Qβ population showed little to no decrease in fitness. These results indicate that Qβ can evolve in response to increasing temperatures in a short period of time with the accumulation of point mutations. Full article

(This article belongs to the Special Issue Phage Ecology)

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14 pages, 2042 KiB

Open AccessArticle

Application of Adaptive Evolution to Improve the Stability of Bacteriophages during Storage

by Kelvin K. Kering, Xiaoxu Zhang, Raphael Nyaruaba, Junping Yu and Hongping Wei

Viruses 2020, 12(4), 423; https://0-doi-org.brum.beds.ac.uk/10.3390/v12040423 - 09 Apr 2020

Cited by 26 | Viewed by 4921

Abstract

Phage stability is important for the successful application of bacteriophages as alternative antibacterial agents. Considering that temperature is a critical factor in phage stability, this study aimed to explore the possibility of improving long-term phage stability through adaptive evolution to elevated temperature. Evolution [...] Read more.

Phage stability is important for the successful application of bacteriophages as alternative antibacterial agents. Considering that temperature is a critical factor in phage stability, this study aimed to explore the possibility of improving long-term phage stability through adaptive evolution to elevated temperature. Evolution of three wild-type ancestral phages (Myoviridae phage Wc4 and Podoviridae phages CX5 and P-PSG-11) was induced by subjecting the phages to heat treatment at 60 °C for five cycles. The adapted phages showed better stability than the wild-type ancestral phages when subjected to heat treatment at 60 °C for 1 h and after 60 days of storage at 37 °C. However, the adapted phages could not withstand thermal treatment at 70 °C for 1 h. The infectivity and the lytic properties of the phages were not changed by the evolution process. Whole-genome sequencing revealed that single substitutions in the tail tubular proteins were the only changes observed in the genomes of the adapted phages. This study demonstrates that adaptive evolution could be used as a general method for enhancing the thermal stability of phages without affecting their lytic activity. Sequencing results showed that bacteriophages may exist as a population with minor heterogeneous mutants, which might be important to understand the ecology of phages in different environments. Full article

(This article belongs to the Special Issue Phage Ecology)

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21 pages, 784 KiB

Open AccessArticle

Promises and Pitfalls of In Vivo Evolution to Improve Phage Therapy

by James J. Bull, Bruce R. Levin and Ian J. Molineux

Viruses 2019, 11(12), 1083; https://0-doi-org.brum.beds.ac.uk/10.3390/v11121083 - 21 Nov 2019

Cited by 22 | Viewed by 4015

Abstract

Phage therapy is the use of bacterial viruses (phages) to treat bacterial infections, a medical intervention long abandoned in the West but now experiencing a revival. Currently, therapeutic phages are often chosen based on limited criteria, sometimes merely an ability to plate on [...] Read more.

Phage therapy is the use of bacterial viruses (phages) to treat bacterial infections, a medical intervention long abandoned in the West but now experiencing a revival. Currently, therapeutic phages are often chosen based on limited criteria, sometimes merely an ability to plate on the pathogenic bacterium. Better treatment might result from an informed choice of phages. Here we consider whether phages used to treat the bacterial infection in a patient may specifically evolve to improve treatment on that patient or benefit subsequent patients. With mathematical and computational models, we explore in vivo evolution for four phage properties expected to influence therapeutic success: generalized phage growth, phage decay rate, excreted enzymes to degrade protective bacterial layers, and growth on resistant bacteria. Within-host phage evolution is strongly aligned with treatment success for phage decay rate but only partially aligned for phage growth rate and growth on resistant bacteria. Excreted enzymes are mostly not selected for treatment success. Even when evolution and treatment success are aligned, evolution may not be rapid enough to keep pace with bacterial evolution for maximum benefit. An informed use of phages is invariably superior to naive reliance on within-host evolution. Full article

(This article belongs to the Special Issue Phage Ecology)

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20 pages, 6525 KiB

Open AccessArticle

A Novel Benthic Phage Infecting Shewanella with Strong Replication Ability

by Zengmeng Wang, Jiulong Zhao, Long Wang, Chengcheng Li, Jianhui Liu, Lihua Zhang and Yongyu Zhang

Viruses 2019, 11(11), 1081; https://0-doi-org.brum.beds.ac.uk/10.3390/v11111081 - 19 Nov 2019

Cited by 12 | Viewed by 3678

Abstract

The coastal sediments were considered to contain diverse phages playing important roles in driving biogeochemical cycles based on genetic analysis. However, till now, benthic phages in coastal sediments were very rarely isolated, which largely limits our understanding of their biological characteristics. Here, we [...] Read more.

The coastal sediments were considered to contain diverse phages playing important roles in driving biogeochemical cycles based on genetic analysis. However, till now, benthic phages in coastal sediments were very rarely isolated, which largely limits our understanding of their biological characteristics. Here, we describe a novel lytic phage (named Shewanella phage S0112) isolated from the coastal sediments of the Yellow Sea infecting a sediment bacterium of the genus Shewanella. The phage has a very high replication capability, with the burst size of ca. 1170 phage particles per infected cell, which is 5–10 times higher than that of most phages isolated before. Meanwhile, the latent period of this phage is relatively longer, which might ensure adequate time for phage replication. The phage has a double-stranded DNA genome comprising 62,286 bp with 102 ORFs, ca. 60% of which are functionally unknown. The expression products of 16 ORF genes, mainly structural proteins, were identified by LC-MS/MS analysis. Besides the general DNA metabolism and structure assembly genes in the phage genome, there is a cluster of auxiliary metabolic genes that may be involved in 7-cyano-7-deazaguanine (preQ₀) biosynthesis. Meanwhile, a pyrophosphohydrolase (MazG) gene being considered as a regulator of programmed cell death or involving in host stringer responses is inserted in this gene cluster. Comparative genomic and phylogenetic analysis both revealed a great novelty of phage S0112. This study represents the first report of a benthic phage infecting Shewanella, which also sheds light on the phage–host interactions in coastal sediments. Full article

(This article belongs to the Special Issue Phage Ecology)

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19 pages, 7042 KiB

Open AccessArticle

A Quest of Great Importance-Developing a Broad Spectrum Escherichia coli Phage Collection

by Joanna Kaczorowska, Eoghan Casey, Horst Neve, Charles M.A.P. Franz, Jean-Paul Noben, Gabriele A. Lugli, Marco Ventura, Douwe van Sinderen and Jennifer Mahony

Viruses 2019, 11(10), 899; https://0-doi-org.brum.beds.ac.uk/10.3390/v11100899 - 26 Sep 2019

Cited by 8 | Viewed by 4299

Abstract

Shigella ssp. and enterotoxigenic Escherichia coli are the most common etiological agents of diarrheal diseases in malnourished children under five years of age in developing countries. The ever-growing issue of antibiotic resistance and the potential negative impact of antibiotic use on infant commensal [...] Read more.

Shigella ssp. and enterotoxigenic Escherichia coli are the most common etiological agents of diarrheal diseases in malnourished children under five years of age in developing countries. The ever-growing issue of antibiotic resistance and the potential negative impact of antibiotic use on infant commensal microbiota are significant challenges to current therapeutic approaches. Bacteriophages (or phages) represent an alternative treatment that can be used to treat specific bacterial infections. In the present study, we screened water samples from both environmental and industrial sources for phages capable of infecting E. coli laboratory strains within our collection. Nineteen phages were isolatedand tested for their ability to infect strains within the ECOR collection and E. coli O157:H7 Δstx. Furthermore, since coliphages have been reported to cross-infect certain Shigella spp., we also evaluated the ability of the nineteen phages to infect a representative Shigella sonnei strain from our collection. Based on having distinct (although overlapping in some cases) host ranges, ten phage isolates were selected for genome sequence and morphological characterization. Together, these ten selected phages were shown to infect most of the ECOR library, with 61 of the 72 strains infected by at least one phage from our collection. Genome analysis of the ten phages allowed classification into five previously described genetic subgroups plus one previously underrepresented subgroup. Full article

(This article belongs to the Special Issue Phage Ecology)

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Review

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40 pages, 4440 KiB

Open AccessReview

Look Who’s Talking: T-Even Phage Lysis Inhibition, the Granddaddy of Virus-Virus Intercellular Communication Research

by Stephen T. Abedon

Viruses 2019, 11(10), 951; https://0-doi-org.brum.beds.ac.uk/10.3390/v11100951 - 16 Oct 2019

Cited by 41 | Viewed by 8606

Abstract

That communication can occur between virus-infected cells has been appreciated for nearly as long as has virus molecular biology. The original virus communication process specifically was that seen with T-even bacteriophages—phages T2, T4, and T6—resulting in what was labeled as a lysis inhibition. [...] Read more.

That communication can occur between virus-infected cells has been appreciated for nearly as long as has virus molecular biology. The original virus communication process specifically was that seen with T-even bacteriophages—phages T2, T4, and T6—resulting in what was labeled as a lysis inhibition. Another proposed virus communication phenomenon, also seen with T-even phages, can be described as a phage-adsorption-induced synchronized lysis-inhibition collapse. Both are mediated by virions that were released from earlier-lysing, phage-infected bacteria. Each may represent ecological responses, in terms of phage lysis timing, to high local densities of phage-infected bacteria, but for lysis inhibition also to locally reduced densities of phage-uninfected bacteria. With lysis inhibition, the outcome is a temporary avoidance of lysis, i.e., a lysis delay, resulting in increased numbers of virions (greater burst size). Synchronized lysis-inhibition collapse, by contrast, is an accelerated lysis which is imposed upon phage-infected bacteria by virions that have been lytically released from other phage-infected bacteria. Here I consider some history of lysis inhibition, its laboratory manifestation, its molecular basis, how it may benefit expressing phages, and its potential ecological role. I discuss as well other, more recently recognized examples of virus-virus intercellular communication. Full article

(This article belongs to the Special Issue Phage Ecology)

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