When bacteria are phage playgrounds: interactions between viruses, cells, and mobile genetic elements

Article Multidisciplinary Sciences

Resolving the structure of phage-bacteria interactions in the context of natural diversity

Kathryn M. Kauffman et al.

Summary: This article investigates the interactions between bacteria and viruses, and reveals strain-specificity and recombination in phages. The study suggests that recombination is an important mode of phage evolution in microbial communities.

NATURE COMMUNICATIONS (2022)

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Article Cell Biology

Metabolic reprogramming of Pseudomonas aeruginosa by phage-based quorum sensing modulation

Hanne Hendrix et al.

Summary: This study reveals the role of the Pseudomonas quinolone signal (PQS) in bacterial virus infection. The virus LUZ19 targets the PQS system by expressing the quorum sensing targeting protein (Qst), which interacts with key enzymes in the PQS biosynthesis pathway. This interaction leads to a decrease in PQS levels and impairs the virus infection, but can be restored by external supplementation of a PQS precursor. Qst represents a potential tool for combating antibiotic resistance in bacterial pathogens.

CELL REPORTS (2022)

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Article Biochemistry & Molecular Biology

Microbial defenses against mobile genetic elements and viruses: Who defends whom from what?

Eduardo P. C. Rocha et al.

Summary: Prokaryotes possess mobile genetic elements that enable horizontal gene transfer between cells. These elements contain defense systems to filter, control, or inactivate other elements. The abundance of defense systems in these mobile genetic elements sheds new light on their role as tools of intragenomic conflict.

PLOS BIOLOGY (2022)

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Article Microbiology

Phages and their satellites encode hotspots of antiviral systems

Francois Rousset et al.

Summary: Bacteria have various genetic systems to defend against viral infection, including those within prophages. Phage satellites pose additional pressures on phages by hijacking viral elements. This study found that E. coli P2-like phages and their P4-like satellites carry genetic hotspots with anti-phage systems. These hotspots participate in inter-viral competition and shape dynamics between the bacterial host, P2-like phages, and P4-like satellites. Importantly, the anti-phage activity of satellites can benefit the helper phage during competition, turning a parasitic relationship into a mutualistic one.

CELL HOST & MICROBE (2022)

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Article Ecology

Genome-driven elucidation of phage-host interplay and impact of phage resistance evolution on bacterial fitness

Pawel Markwitz et al.

Summary: The study found that phage-resistance emergence in bacterial populations had a key ecological impact and could be influenced by self and cross-resistance mechanisms. Using seven phages with distinct receptors to infect five Pseudomonas aeruginosa strains, significant differences were observed in resistance mechanisms between strains, which were correlated with bacterial growth rates.

ISME JOURNAL (2022)

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Article Multidisciplinary Sciences

Two defence systems eliminate plasmids from seventh pandemic Vibrio cholerae

Milena Jaskolska et al.

Summary: Horizontal gene transfer is a key driver of bacterial evolution, facilitated by mobile genetic elements such as plasmids and bacteriophages. This study identifies two conserved plasmid defence systems in Vibrio cholerae, responsible for the ongoing cholera pandemic. These systems rapidly eliminate small plasmids and defend against bacteriophage infection. Additionally, they increase the burden of large conjugative plasmids, leading to a fitness disadvantage for plasmid-carrying cells. These findings explain the rarity of plasmids in pandemic strains and have implications for understanding antibiotic resistance plasmid dissemination and the evolution of pandemic V. cholerae.

NATURE (2022)

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Article Multidisciplinary Sciences

Systematic and quantitative view of the antiviral arsenal of prokaryotes

Florian Tesson et al.

Summary: Bacteria and archaea have developed multiple antiviral mechanisms. Researchers have introduced a tool called DefenseFinder that can automatically detect known antiviral systems in prokaryotic genomes, and have shown that variations in antiviral strategies correlate with genome size, viral threat, and lifestyle traits.

NATURE COMMUNICATIONS (2022)

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Article Cell Biology

A dual-function phage regulator controls the response of cohabiting phage elements via regulation of the bacterial SOS response

Gil Azulay et al.

Summary: A study has identified AriS as a phage regulator in Listeria monocytogenes strain 10403S. AriS controls the induction of two phage elements in the chromosome, inhibiting their lytic induction under SOS conditions. The protein possesses two distinct activities, one regulating phage genes and the other downregulating the bacterial SOS response. The presence of a conserved domain in AriS-like proteins suggests that temperate phages acquired dual-function regulators to align their response with other phage elements.

CELL REPORTS (2022)

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Article Microbiology

Phage-host coevolution in natural populations

Damien Piel et al.

Summary: This study investigates the coevolution between bacteriophages and their bacterial hosts, revealing the changes in resistance and counter-resistance mechanisms. The research finds that the adaptation of phages to local hosts is influenced by their ability to infect closely related bacteria and strain-specific defenses. The study further demonstrates the role of genetic exchanges and mobile genetic elements in the evolution of bacterial defenses and phage counter-defenses.

NATURE MICROBIOLOGY (2022)

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Article Ecology

The coral pathogen Vibrio coralliilyticus kills non-pathogenic holobiont competitors by triggering prophage induction

Weiquan Wang et al.

Summary: Competition in the coral microbiome plays a significant role in coral health, and a study has found that a pathogen called Vibrio coralliilyticus outcompetes commensal bacteria by inducing prophages. This discovery reveals the molecular mechanism underlying colonization competition in corals and highlights the importance of certain genes used by pathogens to gain a competitive advantage.

NATURE ECOLOGY & EVOLUTION (2022)

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Article Biochemistry & Molecular Biology

Bacteriophages benefit from mobilizing pathogenicity islands encoding immune systems against competitors

Alfred Fillol-Salom et al.

Summary: This study discovers a important anti-phage system in bacteria called phage-inducible chromosomal islands (PICIs), which can be disseminated intra-and inter-generically by helper phages and provide broad immunity. Results show that phages can mobilize PICI-encoded immunity systems to use them against other mobile genetic elements, which compete with the phages for the same bacterial hosts. This finding has significant implications for phages, bacteria, and horizontal gene transfer control.

CELL (2022)

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Review Biology

Selfish, promiscuous and sometimes useful: how mobile genetic elements drive horizontal gene transfer in microbial populations

Matthieu Haudiquet et al.

Summary: Horizontal gene transfer (HGT) is a driving force in microbial adaptation, but it is controlled by mobile genetic elements (MGEs) whose interests may not align with those of their hosts. The interactions between cells and MGEs, as well as between MGEs themselves, result in complex evolutionary processes that affect gene flow and microbial adaptation.

PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES (2022)

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Article Microbiology

Phage-Plasmids Spread Antibiotic Resistance Genes through Infection and Lysogenic Conversion

Eugen Pfeifer et al.

Summary: Antibiotic resistance is rapidly spreading through horizontal transfer mediated by phage-plasmids, which carry a diverse range of clinically relevant antibiotic resistance genes and can transfer them across bacteria.

MBIO (2022)

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Article Genetics & Heredity

The Vibrio cholerae Seventh Pandemic Islands act in tandem to defend against a circulating phage

Brendan J. O'Hara et al.

Summary: This study isolated a circulating phage from a cholera patient stool sample and demonstrated that elements in both VSP-I and VSP-II inhibited the propagation of this phage in its native host, providing direct evidence for the role of these genomic islands in phage defense. Furthermore, the research showed that these defense systems are regulated by quorum sensing and are only active at certain cell densities.

PLOS GENETICS (2022)

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Review Microbiology

Mechanisms and clinical importance of bacteriophage resistance

Julia E. Egido et al.

Summary: This article explores the defense mechanisms of bacteriophages and their relevance for the potential clinical use of bacteriophages as therapeutic agents, suggesting new directions for research.

FEMS MICROBIOLOGY REVIEWS (2022)

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Article Biochemistry & Molecular Biology

Coevolving Plasmids Drive Gene Flow and Genome Plasticity in Host-Associated Intracellular Bacteria

Stephan Koestlbacher et al.

Summary: Current chlamydial plasmids are amalgamations of at least one ancestral plasmid and a bacteriophage; the majority of plasmid genes are also found on chromosomes of extant chlamydiae; frequent horizontal gene transfer and chromosomal integration events illustrate the pronounced impact of coevolution with these extrachromosomal elements on bacterial genome dynamics in host-dependent microbes.

CURRENT BIOLOGY (2021)

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Article Microbiology

Prophages encode phage-defense systems with cognate self-immunity

Sian Owen et al.

Summary: The research identified a family of prophage-encoded phage-defense proteins called BstA in diverse Gram-negative bacteria. BstA protein localizes to sites of exogenous phage DNA replication and mediates abortive infection to suppress competing phage epidemic. It allows prophages to defend host cells against exogenous phage attack without affecting lytic replication.

CELL HOST & MICROBE (2021)

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Article Ecology

Pervasive prophage recombination occurs during evolution of spore-forming Bacilli

Anna Dragos et al.

Summary: Under a sporulation selection regime, recombination between SP beta and low copy number phi3Ts phage DNA in Bacillus subtilis leads to the formation of a new prophage and the release of virulent phage hybrids. These phages belong to a unique cluster of large phages inserted into sporulation-related genes, indicating diversification of SP beta-like phages in nature. This study sheds light on the eco-evolutionary relationships between bacteria and their phages by capturing the early stages of phage evolution.

ISME JOURNAL (2021)

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Article Biochemistry & Molecular Biology

Regulation of prophage induction and lysogenization by phage communication systems

John B. Bruce et al.

Summary: Viruses utilize molecular communication to regulate their infection strategies, with some viruses using signaling molecules to enter dormant infections. Understanding these mechanisms can help manipulate host and phage population dynamics in natural environments.

CURRENT BIOLOGY (2021)

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Article Biochemistry & Molecular Biology

The arbitrium system controls Prophage induction

Aisling Brady et al.

Summary: Some Bacillus-infecting bacteriophages utilize a peptide-based communication system, called arbitrium, to coordinate the lysis-lysogeny decision. AimR, a key player in this system, is involved in a complex network of regulation. The SP beta phage, possessing a functional arbitrium system, can optimize production of infective particles while preserving the number of surviving cells, which increases phage persistence in nature.

CURRENT BIOLOGY (2021)

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Article Virology

Jumbo Phages: A Comparative Genomic Overview of Core Functions and Adaptions for Biological Conflicts

Lakshminarayan M. Iyer et al.

Summary: Jumbo phages, with their extraordinary genome size, exhibit diverse adaptations across major biological systems and can be classified into three higher-order groups based on conserved gene patterns. Additionally, sensitive sequence analysis methods have identified novel protein-modifying enzymes that may help exploit host-machinery.

VIRUSES-BASEL (2021)

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Article Biochemistry & Molecular Biology

Causes and Consequences of Bacteriophage Diversification via Genetic Exchanges across Lifestyles and Bacterial Taxa

Jorge A. Moura de Sousa et al.

Summary: Bacteriophages evolve rapidly by acquiring genes from other phages, with genetic transfers happening between phages enriched for specific enzymes. Phage family and host phyla act as strong barriers to gene exchange, while temperate phages have broader host ranges.

MOLECULAR BIOLOGY AND EVOLUTION (2021)

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Article Biochemistry & Molecular Biology

Xenogeneic silencing relies on temperature-dependent phosphorylation of the host H-NS protein in Shewanella

Xiaoxiao Liu et al.

Summary: This study revealed that phosphorylated and nonphosphorylated forms of H-NS can respectively silence or derepress multiple LGT genes in Shewanella oneidensis, thereby controlling gene expression of bacteria at different temperatures. These findings highlight the critical role of posttranslational modification of H-NS in regulating gene expression in bacteria.

NUCLEIC ACIDS RESEARCH (2021)

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Article Biochemistry & Molecular Biology

Bacteria have numerous distinctive groups of phage-plasmids with conserved phage and variable plasmid gene repertoires

Eugen Pfeifer et al.

Summary: Plasmids and temperate phages play crucial roles in bacterial evolution. Some elements, known as phage-plasmids, have been identified as both plasmids and phages. A study identified 780 phage-plasmids among a large number of phages and plasmids, grouped them into different categories, and suggested their ancient origins.

NUCLEIC ACIDS RESEARCH (2021)

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Article Multidisciplinary Sciences

Rapid evolutionary turnover of mobile genetic elements drives bacterial resistance to phages

Fatima Aysha Hussain et al.

Summary: In marine Vibrio, phage resistance evolves rapidly and leads to differential susceptibility among bacterial strains. This resistance is cumulative, with each bacterial genome carrying multiple defense elements. The fast evolution of these elements decouples phage resistance from other genomic features.

SCIENCE (2021)

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Article Biochemistry & Molecular Biology

A phage satellite tunes inducing phage gene expression using a domesticated endonuclease to balance inhibition and virion hijacking

Zoe Netter et al.

Summary: Bacteria face constant threat of predation by bacterial viruses, and one particular bacterial virus satellite, PLE, has developed a specific defense mechanism against lytic phage ICP1. This defense involves molecular parasitism where PLE hijacks ICP1 processes. Through encoding a novel DNA binding protein, CapR, PLE is able to repress ICP1's capsid morphogenesis operon without hindering the overall ICP1 lifecycle. This delicate balance of satellite-mediated inhibition allows PLE to block phage production while successfully mobilizing in a phage-derived particle, showing a unique aspect of bacteriophage interactions.

NUCLEIC ACIDS RESEARCH (2021)

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Article Biochemistry & Molecular Biology

Novel anti-repression mechanism of H-NS proteins by a phage protein

Fredj Ben Bdira et al.

Summary: H-NS family proteins play important roles in genome organization and regulation of foreign genes, with gene repression directly dependent on their DNA binding modes. The protein gp4 encoded by Pseudomonas lytic phage LUZ24 can specifically interfere with the formation and stability of the bridged MvaT-DNA complex, relieving gene silencing and adversely affecting P. aeruginosa growth. Controlling H-NS conformation may provide new ways to combat Pseudomonas multidrug resistance.

NUCLEIC ACIDS RESEARCH (2021)

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Article Multidisciplinary Sciences

Defensive hypervariable regions confer superinfection exclusion in microviruses

Paul C. Kirchberger et al.

Summary: Single-stranded DNA phages of the family Microviridae have independently evolved multiple divergent lineages capable of lysogenizing hosts and developing hypervariable regions in their DNA pilot protein. These hypervariable regions confer the ability of temperate Microviridae to prevent DNA injection and infection by other microviruses, highlighting competition between viruses as a significant selective pressure.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2021)

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Article Multidisciplinary Sciences

Temporal shifts in antibiotic resistance elements govern phage-pathogen conflicts

Kristen N. LeGault et al.

Summary: Through time-shift experiments, fluctuations in Vibrio cholerae's resistance to phages in clinical samples were discovered, with the identification of phage resistance determinants within SXT integrative and conjugative elements (ICEs) that also confer antibiotic resistance. The study revealed that SXT ICEs, widespread in g-proteobacteria, encode phage defense systems linked to a single hotspot of genetic exchange, leading to the selection of a novel phage-encoded defense inhibitor and the concurrent dissemination of phage and antibiotic resistances through high-frequency SXT ICE conjugation stimulated by phage infection.

SCIENCE (2021)

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Article Biochemistry & Molecular Biology

Degradation of host translational machinery drives tRNA acquisition in viruses

Joy Y. Yang et al.

Summary: Viruses under selective pressure to maintain compact genomes depend on host cell translational machinery for reproduction, but some encode abundant tRNA and other translation-related genes to optimize for codon usage differences between virus and host. Research shows that carrying 18 tRNAs may convey selective advantages to a T4-like Vibriophage, suggesting that the main driver behind phage tRNA acquisition is to sustain translation as host machinery degrades, resulting in a dynamically adapted codon usage strategy during infection.

CELL SYSTEMS (2021)

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Review Genetics & Heredity

Evolutionary entanglement of mobile genetic elements and host defence systems: guns for hire

Eugene V. Koonin et al.

NATURE REVIEWS GENETICS (2020)

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Article Microbiology

Exploitation of the Cooperative Behaviors of Anti-CRISPR Phages

Anne Chevallereau et al.

CELL HOST & MICROBE (2020)

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Article Multidisciplinary Sciences

A bacteriophage nucleus-like compartment shields DNA from CRISPR nucleases

Senen D. Mendoza et al.

NATURE (2020)

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Article Multidisciplinary Sciences

Virulent coliphages in 1-year-old children fecal samples are fewer, but more infectious than temperate coliphages

Aurelie Mathieu et al.

NATURE COMMUNICATIONS (2020)

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Article Microbiology

A jumbo phage that forms a nucleus-like structure evades CRISPR-Cas DNA targeting but is vulnerable to type III RNA-based immunity

Lucia M. Malone et al.

NATURE MICROBIOLOGY (2020)

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Article Biology

Dominant Vibrio cholerae phage exhibits lysis inhibition sensitive to disruption by a defensive phage satellite

Stephanie G. Hays et al.

ELIFE (2020)

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Article Biochemistry & Molecular Biology

New candidates for regulated gene integrity revealed through precise mapping of integrative genetic elements

Catherine M. Mageeney et al.

NUCLEIC ACIDS RESEARCH (2020)

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Article Virology

Abortive Infection: Bacterial Suicide as an Antiviral Immune Strategy

Anna Lopatina et al.

ANNUAL REVIEW OF VIROLOGY, VOL 7, 2020 (2020)

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Review Biochemistry & Molecular Biology

Evolutionary Ecology and Interplay of Prokaryotic Innate and Adaptive Immune Systems

Tatiana Dimitriu et al.

CURRENT BIOLOGY (2020)

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Article Cell Biology

Active Lysogeny in Listeria Monocytogenes Is a Bacteria-Phage Adaptive Response in the Mammalian Environment

Anna Pasechnek et al.

CELL REPORTS (2020)

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Article Genetics & Heredity

Phylogenetic background and habitat drive the genetic diversification ofEscherichia coli

Marie Touchon et al.

PLOS GENETICS (2020)

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Article Multidisciplinary Sciences

CRISPR-CasΦ from huge phages is a hypercompact genome editor

Patrick Pausch et al.

SCIENCE (2020)

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Review Biochemistry & Molecular Biology

Impact of Xenogeneic Silencing on Phage-Host Interactions

Eugen Pfeifer et al.

JOURNAL OF MOLECULAR BIOLOGY (2019)

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Article Biochemistry & Molecular Biology

Origin of a Core Bacterial Gene via Co-option and Detoxification of a Phage Lysin

Amelia M. Randich et al.

CURRENT BIOLOGY (2019)

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Review Biochemistry & Molecular Biology

Filamentous phages: masters of a microbial sharing economy

Iain D. Hay et al.

EMBO REPORTS (2019)

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Review Microbiology

CRISPR-Cas in mobile genetic elements: counter-defence and beyond

Guilhem Faure et al.

NATURE REVIEWS MICROBIOLOGY (2019)

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Article Microbiology

Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth's biomes

Simon Roux et al.

NATURE MICROBIOLOGY (2019)

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Article Multidisciplinary Sciences

Virus-borne mini-CRISPR arrays are involved in interviral conflicts

Sofia Medvedeva et al.

NATURE COMMUNICATIONS (2019)

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Article Biology

Phage integration alters the respiratory strategy of its host

Jeffrey N. Carey et al.

ELIFE (2019)

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Article Biochemistry & Molecular Biology

A Host-Produced Quorum-Sensing Autoinducer Controls a Phage Lysis-Lysogeny Decision

Justin E. Silpe et al.

CELL (2019)

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Article Biochemistry & Molecular Biology

Bacteriophage Cooperation Suppresses CRISPR-Cas3 and Cas9 Immunity

Adair L. Borges et al.

CELL (2018)

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Article Biochemistry & Molecular Biology

Anti-CRISPR Phages Cooperate to Overcome CRISPR-Cas Immunity

Mariann Landsberger et al.

CELL (2018)

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Article Microbiology

Bacteriophage Transcription Factor Cro Regulates Virulence Gene Expression in Enterohemorrhagic Escherichia coli

Juan D. Hernandez-Doria et al.

CELL HOST & MICROBE (2018)

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Article Ecology

Phage-inducible chromosomal islands are ubiquitous within the bacterial universe

Alfred Fillol-Salom et al.

ISME JOURNAL (2018)

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Article Biochemistry & Molecular Biology

Rates of Mutation and Recombination in Siphoviridae Phage Genome Evolution over Three Decades

Anne Kupczok et al.

MOLECULAR BIOLOGY AND EVOLUTION (2018)

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Article Multidisciplinary Sciences

Systematic discovery of antiphage defense systems in the microbial pangenome

Shany Doron et al.

SCIENCE (2018)

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Article Multidisciplinary Sciences

Assembly of a nucleus-like structure during viral replication in bacteria

Vorrapon Chaikeeratisak et al.

SCIENCE (2017)

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Article Microbiology

Prophage-mediated defence against viral attack and viral counter-defence

Rebekah M. Dedrick et al.

NATURE MICROBIOLOGY (2017)

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Article Microbiology

Bacteriophage evolution differs by host, lifestyle and genome

Travis N. Mavrich et al.

NATURE MICROBIOLOGY (2017)

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Article Ecology

Genetic and life-history traits associated with the distribution of prophages in bacteria

Marie Touchon et al.

ISME JOURNAL (2016)

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Article Ecology

Prophages mediate defense against phage infection through diverse mechanisms

Joseph Bondy-Denomy et al.

ISME JOURNAL (2016)

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Review Biochemistry & Molecular Biology

The Use and Abuse of LexA by Mobile Genetic Elements

Nadine Fornelos et al.

TRENDS IN MICROBIOLOGY (2016)

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Article Biochemistry & Molecular Biology

Live cell imaging of SOS and prophage dynamics in isogenic bacterial populations

Stefan Helfrich et al.

MOLECULAR MICROBIOLOGY (2015)

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Article Genetics & Heredity

Virus Satellites Drive Viral Evolution and Ecology

Belen Frigols et al.

PLOS GENETICS (2015)

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Article Ecology

Intra- and inter-generic transfer of pathogenicity island-encoded virulence genes by cos phages

John Chen et al.

ISME Journal (2015)

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Article Genetics & Heredity

Temperate Phages Acquire DNA from Defective Prophages by Relaxed Homologous Recombination: The Role of Rad52-Like Recombinases

Marianne De Paepe et al.

PLOS GENETICS (2014)

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Article Multidisciplinary Sciences

Transcription termination controls prophage maintenance in Escherichia coli genomes

Rachid Menouni et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2013)

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Article Ecology

Within-host competition determines reproductive success of temperate bacteriophages

Dominik Refardt

ISME JOURNAL (2011)

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Article Multidisciplinary Sciences

Phage Encoded H-NS: A Potential Achilles Heel in the Bacterial Defence System

Connor T. Skennerton et al.

PLOS ONE (2011)

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Article Genetics & Heredity

Bacteriophage Crosstalk: Coordination of Prophage Induction by Trans-Acting Antirepressors

Sebastien Lemire et al.

PLOS GENETICS (2011)

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Article Multidisciplinary Sciences

Killing niche competitors by remote-control bacteriophage induction

Laura Selva et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2009)

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Article Genetics & Heredity

The λ Red proteins promote efficient recombination between diverged sequences:: Implications for bacteriophage genome mosaicism

Jann T. Martinsohn et al.

PLOS GENETICS (2008)

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Article Biochemistry & Molecular Biology

Causes for the intriguing presence of tRNAs in phages

Marc Bailly-Bechet et al.

GENOME RESEARCH (2007)

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Article Multidisciplinary Sciences

An H-NS-like stealth protein aids horizontal DNA transmission in bacteria

Marie Doyle et al.

SCIENCE (2007)

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Article Biochemistry & Molecular Biology

A truncated H-NS-like protein from enteropathogenic Escherichia coli acts as an H-NS antagonist

HS Williamson et al.

MOLECULAR MICROBIOLOGY (2005)

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When bacteria are phage playgrounds: interactions between viruses, cells, and mobile genetic elements

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