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26 pages, 21730 KiB

Open AccessArticle

Genome Characterization and Infectivity Potential of Vibriophage-ϕLV6 with Lytic Activity against Luminescent Vibrios of Penaeus vannamei Shrimp Aquaculture

by Manikantha Benala, Murugadas Vaiyapuri, Visnuvinayagam Sivam, Karthika Raveendran, Mukteswar Prasad Mothadaka and Madhusudana Rao Badireddy

Viruses 2023, 15(4), 868; https://doi.org/10.3390/v15040868 - 28 Mar 2023

Cited by 3 | Viewed by 1730

Abstract

Shrimp aquaculture, especially during the hatchery phase, is prone to economic losses due to infections caused by luminescent vibrios. In the wake of antimicrobial resistance (AMR) in bacteria and the food safety requirements of farmed shrimp, aqua culturists are seeking alternatives to antibiotics [...] Read more.

Shrimp aquaculture, especially during the hatchery phase, is prone to economic losses due to infections caused by luminescent vibrios. In the wake of antimicrobial resistance (AMR) in bacteria and the food safety requirements of farmed shrimp, aqua culturists are seeking alternatives to antibiotics for shrimp health management, and bacteriophages are fast emerging as natural and bacteria-specific antimicrobial agents. This study analyzed the whole genome of vibriophage-ϕLV6 that showed lytic activity against six luminescent vibrios isolated from the larval tanks of P. vannamei shrimp hatcheries. The Vibriophage-ϕLV6 genome was 79,862 bp long with 48% G+C content and 107 ORFs that coded for 31 predicted protein functions, 75 hypothetical proteins, and a tRNA. Pertinently, the vibriophage-ϕLV6 genome harbored neither AMR determinants nor virulence genes, indicating its suitability for phage therapy. There is a paucity of whole genome-based information on vibriophages that lyse luminescent vibrios, and this study adds pertinent data to the database of V. harveyi infecting phage genomes and, to our knowledge, is the first vibriophage genome report from India. Transmission electron microscopy (TEM) of vibriophage-ϕLV6 revealed an icosahedral head (~73 nm) and a long, flexible tail (~191 nm) suggesting siphovirus morphology. The vibriophage-ϕLV6 phage at a multiplicity of infection (MOI) of 80 inhibited the growth of luminescent V. harveyi at 0.25%, 0.5%, 1%, 1.5%, 2%, 2.5%, and 3% salt gradients. In vivo experiments conducted with post-larvae of shrimp showed that vibriophage-ϕLV6 reduced luminescent vibrio counts and post-larval mortalities in the phage-treated tank compared to the bacteria-challenged tank, suggesting the potentiality of vibriophage-ϕLV6 as a promising candidate in treating luminescent vibriosis in shrimp aquaculture. The vibriophage-ϕLV6 survived for 30 days in salt (NaCl) concentrations ranging from 5 ppt to 50 ppt and was stable at 4 °C for 12 months. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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12 pages, 2203 KiB

Open AccessArticle

Characterization of Three Different Endolysins Effective against Gram-Negative Bacteria

by Tae-Hwan Jeong, Hye-Won Hong, Min Soo Kim, Miryoung Song and Heejoon Myung

Viruses 2023, 15(3), 679; https://doi.org/10.3390/v15030679 - 04 Mar 2023

Cited by 6 | Viewed by 2170

Abstract

Genes encoding endolysins were identified and cloned from three different Escherichia coli bacteriophages, 10-24(13), PBEC30, and PBEC56. Putative antimicrobial peptide (AMP)-like C-terminal alpha helix structures with amphipathic natures were predicted from the three endolysins. Each gene was cloned and expressed as hexahistidine-tagged forms, [...] Read more.

Genes encoding endolysins were identified and cloned from three different Escherichia coli bacteriophages, 10-24(13), PBEC30, and PBEC56. Putative antimicrobial peptide (AMP)-like C-terminal alpha helix structures with amphipathic natures were predicted from the three endolysins. Each gene was cloned and expressed as hexahistidine-tagged forms, and the products were purified and characterized. The purified endolysins exhibited antibacterial activities against a variety of Gram-negative bacteria including Escherichia coli, Pseudomonas aeruginosa, Acinetobacter baumannii, and Klebsiella pneumonia. Their antibacterial activities were improved by N-terminal fusion with an antimicrobial peptide, cecropin A. Minimum inhibitory concentrations (MIC) were as low as 4 μg/mL, depending on the targeted strain. The endolysins’ enzymatic activities were not affected by changes in pH at ranges from 5 to 10 and were stable at temperatures between 4 and 65 °C. The in vivo efficacies of the three endolysins were also demonstrated using Galleria melonella for infection models. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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16 pages, 1330 KiB

Open AccessArticle

Co-Delivery of the Human NY-ESO-1 Tumor-Associated Antigen and Alpha-GalactosylCeramide by Filamentous Bacteriophages Strongly Enhances the Expansion of Tumor-Specific CD8+ T Cells

by Roberta Manco, Luciana D’Apice, Maria Trovato, Lucia Lione, Erika Salvatori, Eleonora Pinto, Mirco Compagnone, Luigi Aurisicchio, Piergiuseppe De Berardinis and Rossella Sartorius

Viruses 2023, 15(3), 672; https://doi.org/10.3390/v15030672 - 02 Mar 2023

Cited by 1 | Viewed by 1730

Abstract

Tumor-associated antigens (TAAs) represent attractive targets in the development of anti-cancer vaccines. The filamentous bacteriophage is a safe and versatile delivery nanosystem, and recombinant bacteriophages expressing TAA-derived peptides at a high density on the viral coat proteins improve TAA immunogenicity, triggering effective in [...] Read more.

Tumor-associated antigens (TAAs) represent attractive targets in the development of anti-cancer vaccines. The filamentous bacteriophage is a safe and versatile delivery nanosystem, and recombinant bacteriophages expressing TAA-derived peptides at a high density on the viral coat proteins improve TAA immunogenicity, triggering effective in vivo anti-tumor responses. To enhance the efficacy of the bacteriophage as an anti-tumor vaccine, we designed and generated phage particles expressing a CD8+ peptide derived from the human cancer germline antigen NY-ESO-1 decorated with the immunologically active lipid alpha-GalactosylCeramide (α-GalCer), a potent activator of invariant natural killer T (iNKT) cells. The immune response to phage expressing the human TAA NY-ESO-1 and delivering α-GalCer, namely fdNY-ESO-1/α-GalCer, was analyzed either in vitro or in vivo, using an HLA-A2 transgenic mouse model (HHK). By using NY-ESO-1-specific TCR-engineered T cells and iNKT hybridoma cells, we observed the efficacy of the fdNY-ESO-1/α-GalCer co-delivery strategy at inducing activation of both the cell subsets. Moreover, in vivo administration of fdNY-ESO-1 decorated with α-GalCer lipid in the absence of adjuvants strongly enhances the expansion of NY-ESO-1-specific CD8+ T cells in HHK mice. In conclusion, the filamentous bacteriophage delivering TAA-derived peptides and the α-GalCer lipid may represent a novel and promising anti-tumor vaccination strategy. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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19 pages, 7581 KiB

Open AccessArticle

Pseudomonas Phage ZCPS1 Endolysin as a Potential Therapeutic Agent

by Fatma Abdelrahman, Rutuja Gangakhedkar, Gokul Nair, Gamal El-Didamony, Ahmed Askora, Vikas Jain and Ayman El-Shibiny

Viruses 2023, 15(2), 520; https://doi.org/10.3390/v15020520 - 13 Feb 2023

Cited by 7 | Viewed by 3383

Abstract

The challenge of antibiotic resistance has gained much attention in recent years due to the rapid emergence of resistant bacteria infecting humans and risking industries. Thus, alternatives to antibiotics are being actively searched for. In this regard, bacteriophages and their enzymes, such as [...] Read more.

The challenge of antibiotic resistance has gained much attention in recent years due to the rapid emergence of resistant bacteria infecting humans and risking industries. Thus, alternatives to antibiotics are being actively searched for. In this regard, bacteriophages and their enzymes, such as endolysins, are a very attractive alternative. Endolysins are the lytic enzymes, which are produced during the late phase of the lytic bacteriophage replication cycle to target the bacterial cell walls for progeny release. Here, we cloned, expressed, and purified LysZC1 endolysin from Pseudomonas phage ZCPS1. The structural alignment, molecular dynamic simulation, and CD studies suggested LysZC1 to be majorly helical, which is highly similar to various phage-encoded lysozymes with glycoside hydrolase activity. Our endpoint turbidity reduction assay displayed the lytic activity against various Gram-positive and Gram-negative pathogens. Although in synergism with EDTA, LysZC1 demonstrated significant activity against Gram-negative pathogens, it demonstrated the highest activity against Bacillus cereus. Moreover, LysZC1 was able to reduce the numbers of logarithmic-phase B. cereus by more than 2 log₁₀ CFU/mL in 1 h and also acted on the stationary-phase culture. Remarkably, LysZC1 presented exceptional thermal stability, pH tolerance, and storage conditions, as it maintained the antibacterial activity against its host after nearly one year of storage at 4 °C and after being heated at temperatures as high as 100 °C for 10 min. Our data suggest that LysZC1 is a potential candidate as a therapeutic agent against bacterial infection and an antibacterial bio-control tool in food preservation technology. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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19 pages, 4961 KiB

Open AccessArticle

Development and Evaluation of Bacteriophage Cocktail to Eradicate Biofilms Formed by an Extensively Drug-Resistant (XDR) Pseudomonas aeruginosa

by Medhavi Vashisth, Anu Bala Jaglan, Shikha Yashveer, Priya Sharma, Priyanka Bardajatya, Nitin Virmani, Bidhan Chand Bera, Rajesh Kumar Vaid and Taruna Anand

Viruses 2023, 15(2), 427; https://doi.org/10.3390/v15020427 - 02 Feb 2023

Cited by 4 | Viewed by 2049

Abstract

Extensive and multiple drug resistance in P. aeruginosa combined with the formation of biofilms is responsible for its high persistence in nosocomial infections. A sequential method to devise a suitable phage cocktail with a broad host range and high lytic efficiency against a [...] Read more.

Extensive and multiple drug resistance in P. aeruginosa combined with the formation of biofilms is responsible for its high persistence in nosocomial infections. A sequential method to devise a suitable phage cocktail with a broad host range and high lytic efficiency against a biofilm forming XDR P. aeruginosa strain is presented here. Out of a total thirteen phages isolated against P. aeruginosa, five were selected on the basis of their high lytic spectra assessed using spot assay and productivity by efficiency of plating assay. Phages, after selection, were tested individually and in combinations of two-, three-, four-, and five-phage cocktails using liquid infection model. Out of total 22 combinations tested, the cocktail comprising four phages viz. φPA170, φPA172, φPA177, and φPA180 significantly inhibited the bacterial growth in liquid infection model (p < 0.0001). The minimal inhibitory dose of each phage in a cocktail was effectively reduced to >10 times than the individual dose in the inhibition of XDR P. aeruginosa host. Field emission-scanning electron microscopy was used to visualize phage cocktail mediated eradication of 4-day-old multi-layers of XDR P. aeruginosa biofilms from urinary catheters and glass cover slips, and was confirmed by absence of any viable cells. Differential bacterial inhibition was observed with different phage combinations where multiple phages were found to enhance the cocktail’s lytic range, but the addition of too many phages reduced the overall inhibition. This study elaborates an effective and sequential method for the preparation of a phage cocktail and evaluates its antimicrobial potential against biofilm forming XDR strains of P. aeruginosa. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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13 pages, 1677 KiB

Open AccessArticle

Development and Characterization of Phage Display-Derived Monoclonal Antibodies to the S2 Domain of Spike Proteins of Wild-Type SARS-CoV-2 and Multiple Variants

by Ji Woong Kim, Ah Hyun Cho, Ha Gyeong Shin, Sung Hoon Jang, Su Yeon Cho, Ye Rim Lee and Sukmook Lee

Viruses 2023, 15(1), 174; https://doi.org/10.3390/v15010174 - 06 Jan 2023

Cited by 3 | Viewed by 2551

Abstract

The rapid emergence of new severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants has resulted in the ongoing global coronavirus disease 2019 (COVID-19) pandemic. Thus, the rapid development of a platform to detect a broad range of SARS-CoV-2 variants is essential for successful [...] Read more.

The rapid emergence of new severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants has resulted in the ongoing global coronavirus disease 2019 (COVID-19) pandemic. Thus, the rapid development of a platform to detect a broad range of SARS-CoV-2 variants is essential for successful COVID-19 management. In this study, four SARS-CoV-2 spike protein-specific single-chain variable fragments (scFvs) were isolated from a synthetic antibody library using phage display technology. Following the conversion of these scFvs into monoclonal antibodies (mAbs) (K104.1–K104.4) and production and purification of the mAbs, the antibody pair (K104.1 and K104.2) that exhibited the highest binding affinity (K104.1 and K104.2, 1.3 nM and 1.9 nM) was selected. Biochemical analyses revealed that this antibody pair specifically bound to different sites on the S2 subunit of the spike protein. Furthermore, we developed a highly sensitive sandwich immunoassay using this antibody pair that accurately and quantitatively detected the spike proteins of wild-type SARS-CoV-2 and multiple variants, including Alpha, Beta, Gamma, Delta, Kappa, and Omicron, in the picomolar range. Conclusively, the novel phage display-derived mAbs we have developed may be useful for the rapid and efficient detection of the fast-evolving SARS-CoV-2. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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18 pages, 5756 KiB

Open AccessArticle

Broad-Spectrum Salmonella Phages PSE-D1 and PST-H1 Controls Salmonella in Foods

by Yajie Cao, Runwen Ma, Ziyong Li, Xinyu Mao, Yinan Li, Yuxin Wu, Leping Wang, Kaiou Han, Lei Li, Dongxin Ma, Yuqing Zhou, Xun Li and Xiaoye Wang

Viruses 2022, 14(12), 2647; https://doi.org/10.3390/v14122647 - 27 Nov 2022

Cited by 7 | Viewed by 1605

Abstract

Food contamination by Salmonella can lead to serious foodborne diseases that constantly threaten public health. Innovative and effective strategies are needed to control foodborne pathogenic contamination since the incidence of foodborne diseases has increased gradually. In the present study, two broad-spectrum phages named [...] Read more.

Food contamination by Salmonella can lead to serious foodborne diseases that constantly threaten public health. Innovative and effective strategies are needed to control foodborne pathogenic contamination since the incidence of foodborne diseases has increased gradually. In the present study, two broad-spectrum phages named Salmonella phage PSE-D1 and Salmonella phage PST-H1 were isolated from sewage in China. Phages PSE-D1 and PST-H1 were obtained by enrichment with Salmonella enterica subsp. enterica serovar Enteritidis (S. Enteritidis) CVCC1806 and Salmonella enterica subsp. enterica serovar Typhimurium (S. Typhimurium) CVCC3384, respectively. They were able to lyse Salmonella, E. coli and K. pneumoniae and exhibited broad host range. Further study demonstrated that PSE-D1 and PST-H1 showed high pH and thermal tolerances. Phage PSE-D1 belongs to the Jiaodavirus genus, Tevenvirinae subfamily, while phage PST-H1 belongs to the Jerseyvirus genus, Guernseyvirinae subfamily according to morphology and phylogeny. The results of genome analysis showed that PSE-D1 and PST-H1 lack virulence and drug-resistance genes. The effects of PSE-D1 and PST-H1 on controlling S. Enteritidis CVCC1806 and S. Typhimurium CVCC3384 contamination in three kinds of foods (eggshells, sausages and milk) were further investigated, respectively. Our results showed that, compared to phage-free groups, PSE-D1 and PST-H1 inhibited the growth of their host strain significantly. A significant reduction of host bacteria titers (1.5 and 1.9 log₁₀ CFU/sample, p < 0.001) on eggshells was observed under PSE-D1 and PST-H1 treatments, respectively. Furthermore, administration of PSE-D1 and PST-H1 decreased the counts of bacteria by 1.1 and 1.2 log₁₀ CFU/cm² (p < 0.001) in sausages as well as 1.5 and 1.8 log₁₀ CFU/mL (p < 0.001) in milk, respectively. Interesting, the bacteriostasis efficacy of both phages exhibited more significantly at 4 °C than that at 28 °C in eggshells and milk and sausages. In sum, the purpose of our research was evaluating the counteracting effect of phage PSE-D1 and PST-H1 on the spread of Salmonella on contaminated foods products. Our results suggested that these two phage-based biocontrol treatments are promising strategies for controlling pathogenic Salmonella contaminated food. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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13 pages, 2557 KiB

Open AccessArticle

Development of Antimicrobial Paper Coatings Containing Bacteriophages and Silver Nanoparticles for Control of Foodborne Pathogens

by Thanh Tung Lai, Thi Thanh Ha Pham, Marijn van Lingen, Gabrielle Desaulniers, Guy Njamen, Balázs Tolnai, Tarik Jabrane, Sylvain Moineau and Simon Barnabé

Viruses 2022, 14(11), 2478; https://doi.org/10.3390/v14112478 - 09 Nov 2022

Viewed by 1630

Abstract

In this study, a novel antimicrobial formula that incorporates Listeria bacteriophage P100 and silver nanoparticles into an alginate matrix was successfully developed. Paper coated with the antimicrobial formula inhibited the growth of Listeria monocytogenes. The effects of alginate concentration on the formation of [...] Read more.

In this study, a novel antimicrobial formula that incorporates Listeria bacteriophage P100 and silver nanoparticles into an alginate matrix was successfully developed. Paper coated with the antimicrobial formula inhibited the growth of Listeria monocytogenes. The effects of alginate concentration on the formation of silver nanoparticles, silver concentration on the infectivity of phages, and of low alginate concentrations on the sustained release of silver and phages were explored. The highest antimicrobial activity of the alginate–silver coating was achieved with an alginate concentration of 1%. Adding phage P100 (10⁹ PFU/mL) into the alginate–silver coating led to a synergic effect that resulted in a 5-log reduction in L. monocytogenes. A bioactive paper was then developed by coating a base paper with the antimicrobial formula at different coating weights, followed by infrared drying. The higher coating weight was a crucial factor for the maintenance of phage infectivity throughout the coating and drying processes. Phages incorporated into the alginate matrix remained functional even after high-temperature infrared drying. Taken together, an optimized coating matrix is critical in improving the antimicrobial performance of bioactive paper as well as maintaining phage infectivity during the paper manufacturing process. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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11 pages, 1943 KiB

Open AccessArticle

Thermosensitive Hydrogel Wound Dressing Loaded with Bacteriophage Lysin LysP53

by Changchang Li, Raphael Nyaruaba, Xiaowei Zhao, Heng Xue, Yuhong Li, Hang Yang and Hongping Wei

Viruses 2022, 14(9), 1956; https://doi.org/10.3390/v14091956 - 03 Sep 2022

Cited by 9 | Viewed by 2404

Abstract

Wound infections are prone to attacks from infectious pathogens, including multidrug resistant bacteria that render conventional antimicrobials ineffective. Recently, lysins have been proposed as alternatives to conventional antimicrobials to tackle the menace of multidrug resistance pathogens. The coupling of lysins with a material [...] Read more.

Wound infections are prone to attacks from infectious pathogens, including multidrug resistant bacteria that render conventional antimicrobials ineffective. Recently, lysins have been proposed as alternatives to conventional antimicrobials to tackle the menace of multidrug resistance pathogens. The coupling of lysins with a material that will cover the wound may prove beneficial in both protecting and treating wound infections. Hence, in this study, a Gram-negative lysin, LysP53, was coupled with a thermosensitive hydrogel, poloxamer P407, and its efficacy to treat wound infection was tested. In vitro, the addition of LysP53 to the poloxamer did not affect its thermosensitive characteristics, nor did it affect the hydrogel structure. Moreover, the lysin hydrogel could hydrolyze the peptidoglycan, demonstrating that it may have bactericidal activity. Up to 10.4% of LysP53 was released from the hydrogel gradually within 24 h, which led to a 4-log reduction of stationary phase Acinetobacter baumannii. Lastly, the lysin hydrogel was found safe with no cytotoxic effects observed in cells. Ex vivo, LysP53 hydrogel could inhibit bacterial growth on a pig skin decolonization model, with 3-log differences compared to non-treated groups. Overall, our results suggest that lysin-loaded hydrogels may provide a novel solution to treat wound infections caused by resistant bacteria. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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15 pages, 2541 KiB

Open AccessArticle

Bacteriophage-Based Detection of Staphylococcus aureus in Human Serum

by Matthew Brown, Alex Hall, Henriett Zahn, Marcia Eisenberg and Stephen Erickson

Viruses 2022, 14(8), 1748; https://doi.org/10.3390/v14081748 - 10 Aug 2022

Cited by 4 | Viewed by 1685

Abstract

Bacteriophages have been investigated for clinical utility, both as diagnostic tools and as therapeutic interventions. In order to be applied successfully, a detailed understanding of the influence of the human matrix on the interaction between bacteriophage and the host bacterium is required. In [...] Read more.

Bacteriophages have been investigated for clinical utility, both as diagnostic tools and as therapeutic interventions. In order to be applied successfully, a detailed understanding of the influence of the human matrix on the interaction between bacteriophage and the host bacterium is required. In this study, a cocktail of luciferase bacteriophage reporters was assessed for functionality in a matrix containing human serum and spiked with Staphylococcus aureus. The inhibition of signal and loss of sensitivity was evident with minimal amounts of serum. This phenotype was independent of bacterial growth and bacteriophage viability. Serum-mediated loss of signal was common, albeit not universal, among S. aureus strains. Immunoglobulin G was identified as an inhibitory component and partial inhibition was observed with both the f(ab’)₂ and Fc region. A modified bacteriophage cocktail containing recombinant protein A was developed, which substantially improved signal without the need for additional sample purification. This study highlights the importance of assessing bacteriophage activity in relevant host matrices. Furthermore, it identifies an effective solution, recombinant protein A, for promoting bacteriophage-based detection of S. aureus in matrices containing human serum. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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Review

Jump to: Research

25 pages, 1258 KiB

Open AccessReview

Bacteriophages as Biotechnological Tools

by Mariana Alves Elois, Raphael da Silva, Giulia Von Tönnemann Pilati, David Rodríguez-Lázaro and Gislaine Fongaro

Viruses 2023, 15(2), 349; https://doi.org/10.3390/v15020349 - 26 Jan 2023

Cited by 10 | Viewed by 4964

Abstract

Bacteriophages are ubiquitous organisms that can be specific to one or multiple strains of hosts, in addition to being the most abundant entities on the planet. It is estimated that they exceed ten times the total number of bacteria. They are classified as [...] Read more.

Bacteriophages are ubiquitous organisms that can be specific to one or multiple strains of hosts, in addition to being the most abundant entities on the planet. It is estimated that they exceed ten times the total number of bacteria. They are classified as temperate, which means that phages can integrate their genome into the host genome, originating a prophage that replicates with the host cell and may confer immunity against infection by the same type of phage; and lytics, those with greater biotechnological interest and are viruses that lyse the host cell at the end of its reproductive cycle. When lysogenic, they are capable of disseminating bacterial antibiotic resistance genes through horizontal gene transfer. When professionally lytic—that is, obligately lytic and not recently descended from a temperate ancestor—they become allies in bacterial control in ecological imbalance scenarios; these viruses have a biofilm-reducing capacity. Phage therapy has also been advocated by the scientific community, given the uniqueness of issues related to the control of microorganisms and biofilm production when compared to other commonly used techniques. The advantages of using bacteriophages appear as a viable and promising alternative. This review will provide updates on the landscape of phage applications for the biocontrol of pathogens in industrial settings and healthcare. Full article

(This article belongs to the Special Issue Biotechnological Applications of Phage and Phage-Derived Proteins 2022)

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