Sociovirology: Conflict, Cooperation, and Communication Among Viruses

Total Page:16

File Type:pdf, Size:1020Kb

Sociovirology: Conflict, Cooperation, and Communication Among Viruses Cell Host & Microbe Commentary Sociovirology: Conflict, Cooperation, and Communication among Viruses Samuel L. Dı´az-Mun˜ oz,1,* Rafael Sanjua´ n,2,3 and Stuart West4 1Department of Microbiology and Molecular Genetics, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA 2Institute for Integrative Systems Biology (I2SysBio), Universitat de Vale` ncia, C/Catedra´ tico Agustı´n Escardino 9, 46980 Paterna Valencia, Spain 3Department of Genetics, Universitat de Vale` ncia, C/Dr. Moliner 50, Burjassot, Vale` ncia 46100, Spain 4Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK *Correspondence: [email protected] https://doi.org/10.1016/j.chom.2017.09.012 Viruses are involved in various interactions both within and between infected cells. Social evolution theory offers a conceptual framework for how virus-virus interactions, ranging from conflict to cooperation, have evolved. A critical examination of these interactions could expand our understanding of viruses and be exploited for epidemiological and medical interventions. Virus-virus interactions are pervasive and Potential misgivings with this social- of another individual. As such, evolu- highly diverse (DaPalma et al., 2010; evolution approach include the idea that tionary analysis of social interactions re- Figure 1). Some viruses need another, viruses are too simple to interact socially, lies fundamentally on natural selection. ‘‘helper’’ virus to complete their infection or that to infer traits like cooperation The only major difference with non-social cycle, and other viruses are commonly would be anthropomorphic. On the flip models is that two or more interacting activated or suppressed by the presence side, social interactions have driven the individuals are involved. For example, of secondary viral infections. Viral pro- evolution of life at all levels of complexity cooperative traits, which benefit others, teins can mix and produce mosaic-like and thus could have a role in viral will only be selected for by natural selec- viral particles (pseudotypes) when a cell evolution as well: genes cooperate to tion if they provide a fitness benefit to the is coinfected with two different viruses. form genomes, cells cooperate to form individual performing them (Figure 2A). Viral coinfection of microbes is wide- multicellular organisms, and multicellular Cooperative traits cannot evolve merely spread (Dı´az-Mun˜ oz, 2017), and viruses organisms form complex cooperative so- because they provide a benefit to a have mechanisms enabling multiple cieties. Conflict is also ubiquitous: ‘‘self- population. Furthermore, the evolution of viral genomes to be cotransmitted in the ish’’ genes drive their transmission at a cooperation does not require the ability same infectious unit (reviewed in Sanjua´ n, cost to the genome, cells exploit collec- of individuals to foresee the conse- 2017). Coinfecting viral genomes can be tively produced goods like nutrient- quences of their actions. In other words, distinct, variants of the same virus, or scavenging molecules, and organisms cooperation and social evolution can be even genetically identical, suggesting compete with each other for resources. explained by, and are not at odds with, different types of functional interplay. Since no complex phenotypes are neces- individual-based natural selection. Furthermore, bacteriophages use a form sary for the evolution of social traits, the One way cooperation can be evolution- of communication to regulate lysis of the appearance of anthropomorphism or the arily favored is when it is directed toward infected cell (Erez et al., 2017). Finally, ‘‘simple’’ organization of viruses may not genetically identical individuals or rela- virus-virus interactions in the absence of pose problems for the application of tives. From an evolutionary perspective, cellular coinfection can also be mediated sociobiology models in virology. helping a genetically identical individual by changes at the host level, such as We argue for a social evolution reproduce is the same as reproducing immune responses. approach to understand and predict yourself. By extension, helping relatives Despite this growing body of empirical virus-virus interactions. This framework reproduce provides a fitness benefit to evidence suggesting virus-virus interac- can clarify unexplained phenomena in the actor, as relatives share a fraction of tions, we lack a well-founded conceptual virus-virus interactions by identifying the actor’s genes. This process by which framework that provides an understand- evolved viral social traits, their genetic individuals increase their fitness by ing of how these interactions have and mechanistic basis, and the selective helping relatives reproduce is termed kin evolved and how they could shape viral pressures underlying these traits. We selection. pathogenesis. Social evolution theory outline how this approach could lead to An important potential difficulty in was originally developed to explain animal new breakthroughs in both fundamental applying social evolution to virology re- behavior, but has since been extended to and applied virology. sides in the definition of an individual. microorganisms, including bacteria and One may consider the virion as an individ- unicellular eukaryotes. Yet this social Cooperation and the Individual ual. Yet in some cases, including para- perspective has not been embraced in Social interactions take place when the myxoviruses, birnaviruses, filoviruses, the study of viruses. traits of one individual influence the fitness retroviruses, and inoviruses, a virion can Cell Host & Microbe 22, October 11, 2017 ª 2017 The Authors. Published by Elsevier Inc. 437 This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Cell Host & Microbe Commentary Figure 1. Virus-Virus Interactions Are Diverse and Provide Multiple Opportunities for Social Evolution (A–F) Indicated by gray shadows and depicting social interactions, where the action of a viral genome changes the fitness of other viral genomes. Cells are ovals with black borders. (A) A viral genome (thick curved segment) enters the cell and performs transcription (mRNAs, thin curved segments +) and translation, leading to generation of shared intracellular viral proteins (open hexagons). Transcription-translation is a social and potentially cooperative trait because it benefits the other viral genomes in the cell. (B–F) Viral genomes can prevent or promote reproduction of other genomes by changing the probability that they can infect a cell or host by: (B) blocking the entry of other viral genomes into the cell; (C) producing host-level immune changes (dark red outline) that favor the transmission of all infecting viral genomes; (D) inducing the cell to produce molecules essential for transmission to neighboring cells, benefiting all viral genomes in the cell; (E) producing viral proteins that communicate cell infection status, signaling to other viral genomes the abundance of cells available for reproduction; and (F) manipulating host immune signals to induce distant cells to differentially expose receptors favoring entry of some viral genomes over others. carry multiple genome copies (n-ploidy). If we think of a genome as an individ- Conflict and Cheating Viruses Functionally, these n-ploid virions should ual, then the natural history of viruses is Evidence in favor of viruses acting as be similar to multiple virions entering the filled with opportunities for social inter- cooperative social agents is, paradoxi- same cell, because they would both lead actions (Figure 1), even though experi- cally, provided by the occasional spread to infections with multiple viral genomes. mental demonstration is still lacking in of uncooperative ‘‘cheats.’’ If individuals As such, we suggest that the definition of many cases. A single viral genome are not genetically identical, they will not an individual should be set at the level of entering a cell needs to accomplish both necessarily have the same evolutionary the single infectious viral genome. replication and gene expression (tran- interests, creating the potential for con- Another potential complication stems scription and translation). The mRNAs flict. Social evolution theory predicts from the fact that some viruses, notably and proteins resulting from viral gene that if multiple genomes infect a cell, one RNA viruses, show extremely high muta- expression can provide a collective that invests less in cooperative traits tion rates, leading to the suggestion that benefit to genomes in the cell, such as such as transcription and invests more in the minimal level at which an individual generating capsids and proteins that its own replication will be favored, RNA virus can be defined is a sequence block host immunity. The fact that these because it will benefit from cooperation cloud, or quasispecies (Andino and Dom- factors act as public goods permits, but without paying as much of the cost ingo, 2015). In this case, the individual does not guarantee, cooperation (Chao (Chao and Elena, 2017). This is analogous could be redefined as the consensus (or and Elena, 2017). Cooperation is more to the tragedy of the commons in humans, predominant) sequence of the quasispe- likely to evolve if most interacting ge- where cooperation breaks down due to cies. If, however, functional social interac- nomes are identical, since such high selfish interests, even though everyone tions are established among genetic relatedness allows kin selection
Recommended publications
  • Rice Scholarship Home
    RICE UNIVERSITY By A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE APPROVED, THESIS COMMITTEE HOUSTON, TEXAS ABSTRACT Data-driven modeling to infer the function of viral replication in a counting-based decision by Seth Coleman Cells use gene regulatory networks, sets of genes connected through a web of bio- chemical interactions, to select a developmental pathway based on signals from their environment. These processes, called cell-fate decisions, are ubiquitous in biology. Yet efforts to study cell-fate decisions are often stymied by the inherent complexity of organisms. Simple model systems provide attractive alternative platforms to study cell-fate decisions and gain insights which may be broadly applicable. Infection of E. coli by the virus lambda is one such model system. The outcome of this viral infection is dependent on the number of initially coinfecting viruses (multiplicity of infection, or MOI), which the viral regulatory network appears to `count'. Yet precisely how the viral regulatory network responds to MOI is still unclear, as is how the system is able to achieve sensitivity to MOI despite viral replication, which quickly obfuscates initial viral copy number. In this thesis, I used mathematical modeling of the network dynamics, calibrated by experimental measurements of viral replication and gene ex- pression during infection, to demonstrate how the network responds to MOI and to show that viral replication actually facilitates, rather than hinders, a counting-based decision. This work provides an example of how complex behaviors can emerge from the interplay between gene/network copy number and gene expression, whose coupling iii cannot be ignored in developing a predictive description of cellular decision-making.
    [Show full text]
  • The Virus Social
    editorial Welcome to the virus social Long-known to happen in other realms of the microscopic and macroscopic worlds, social interactions in viruses are increasingly being appreciated and have the potential to infuence many processes, including viral pathogenesis, resistance to antiviral immunity, establishment of persistence and even life cycle choice. ngoing efforts to characterise show that the ability of a vesicular stomatitis communication system to determine the virosphere have identified virus to suppress interferon (IFN)-mediated the number of recent infections in the Oviruses in every environment innate immunity is a social altruistic trait population by measuring the level of a studied, infecting every life form and even that, though costly for the viruses that phage-encoded peptide, and switch to a parasitizing other viruses. In addition to carry it and produce less progeny in the lysogenic lifestyle to prevent killing off their this vast viral diversity, variants frequently short term, enables the replication of other host when the amount of peptide increases emerge within populations of a given virus members of the viral population that do not over a certain threshold5. Cooperation also through mutation, deletion, recombination repress IFN (ref. 2). The demonstration that allows phage populations to resist bacterial or reassortment. Co-circulation of different social evolution rules govern viral innate CRISPR-mediated immune defence; initial viruses in the same areas of the world, immune evasion and virulence provides phage resistance may not be sufficient to sharing hosts and vectors, increases the a framework for future study of viral overcome the immune response, but creates chances of co-infection and co-transmission social traits.
    [Show full text]
  • Beyond Arbitrium: Identification of a Second Communication System In
    Beyond arbitrium: identification of a second communication system in Bacillus phage phi3T that may regulate host defense mechanisms Charles Bernard, Yanyan Li, Philippe Lopez, Eric Bapteste To cite this version: Charles Bernard, Yanyan Li, Philippe Lopez, Eric Bapteste. Beyond arbitrium: identification of a second communication system in Bacillus phage phi3T that may regulate host defense mechanisms. ISME Journal, Nature Publishing Group, 2020, 10.1038/s41396-020-00795-9. hal-03028148 HAL Id: hal-03028148 https://hal.archives-ouvertes.fr/hal-03028148 Submitted on 27 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. The ISME Journal https://doi.org/10.1038/s41396-020-00795-9 ARTICLE Beyond arbitrium: identification of a second communication system in Bacillus phage phi3T that may regulate host defense mechanisms 1,2 2 1 1 Charles Bernard ● Yanyan Li ● Philippe Lopez ● Eric Bapteste Received: 2 April 2020 / Revised: 17 September 2020 / Accepted: 24 September 2020 © The Author(s) 2020. This article is published with open access Abstract The evolutionary stability of temperate bacteriophages at low abundance of susceptible bacterial hosts lies in the trade-off between the maximization of phage replication, performed by the host-destructive lytic cycle, and the protection of the phage-host collective, enacted by lysogeny.
    [Show full text]
  • Dominant Vibrio Cholerae Phage Exhibits Lysis Inhibition Sensitive to Disruption by a Defensive Phage Satellite Stephanie G Hays1, Kimberley D Seed1,2*
    RESEARCH ARTICLE Dominant Vibrio cholerae phage exhibits lysis inhibition sensitive to disruption by a defensive phage satellite Stephanie G Hays1, Kimberley D Seed1,2* 1Department of Plant and Microbial Biology, University of California, Berkeley, United States; 2Chan Zuckerberg Biohub, San Francisco, United States Abstract Bacteria, bacteriophages that prey upon them, and mobile genetic elements (MGEs) compete in dynamic environments, evolving strategies to sense the milieu. The first discovered environmental sensing by phages, lysis inhibition, has only been characterized and studied in the limited context of T-even coliphages. Here, we discover lysis inhibition in the etiological agent of the diarrheal disease cholera, Vibrio cholerae, infected by ICP1, a phage ubiquitous in clinical samples. This work identifies the ICP1-encoded holin, teaA, and antiholin, arrA, that mediate lysis inhibition. Further, we show that an MGE, the defensive phage satellite PLE, collapses lysis inhibition. Through lysis inhibition disruption a conserved PLE protein, LidI, is sufficient to limit the phage produced from infection, bottlenecking ICP1. These studies link a novel incarnation of the classic lysis inhibition phenomenon with conserved defensive function of a phage satellite in a disease context, highlighting the importance of lysis timing during infection and parasitization. Introduction Following the discovery of bacteriophages (D’Herelle, 1917; Twort, 1915), Escherichia coli’s T1 through T7 phages were widely accepted as model systems (Keen,
    [Show full text]
  • Expert Opinion on Three Phage Therapy Related
    Expert Opinion on Three Phage Therapy Related Topics: Bacterial Phage Resistance, Phage Training and Prophages in Bacterial Production Strains Christine Rohde, Gregory Resch, Jean-Paul Pirnay, Bob Blasdel, Laurent Debarbieux, Daniel Gelman, Andrzej Górski, Ronen Hazan, Isabelle Huys, Elene Kakabadze, et al. To cite this version: Christine Rohde, Gregory Resch, Jean-Paul Pirnay, Bob Blasdel, Laurent Debarbieux, et al.. Ex- pert Opinion on Three Phage Therapy Related Topics: Bacterial Phage Resistance, Phage Training and Prophages in Bacterial Production Strains. Viruses, MDPI, 2018, 10 (4), 10.3390/v10040178. pasteur-01827308 HAL Id: pasteur-01827308 https://hal-pasteur.archives-ouvertes.fr/pasteur-01827308 Submitted on 2 Jul 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License viruses Conference Report Expert Opinion on Three Phage Therapy Related Topics: Bacterial Phage Resistance, Phage Training and Prophages in Bacterial Production Strains Christine Rohde 1,†,‡, Grégory Resch 2,†,‡, Jean-Paul Pirnay 3,†,‡ ID , Bob G. Blasdel 4,†, Laurent Debarbieux 5 ID , Daniel Gelman 6, Andrzej Górski 7,8, Ronen Hazan 6, Isabelle Huys 9, Elene Kakabadze 10, Małgorzata Łobocka 11,12, Alice Maestri 13, Gabriel Magno de Freitas Almeida 14 ID , Khatuna Makalatia 10, Danish J.
    [Show full text]
  • Structural Basis of the Arbitrium Peptide–Aimr Communication System in the Phage Lysis–Lysogeny Decision
    ARTICLES https://doi.org/10.1038/s41564-018-0239-y Structural basis of the arbitrium peptide–AimR communication system in the phage lysis–lysogeny decision Qiang Wang1,4, Zeyuan Guan1,4, Kai Pei1, Jing Wang1, Zhu Liu1, Ping Yin1, Donghai Peng2 and Tingting Zou 3* A bacteriophage can replicate and release virions from a host cell in the lytic cycle or switch to a lysogenic process in which the phage integrates itself into the host genome as a prophage. In Bacillus cells, some types of phages employ the arbitrium com- munication system, which contains an arbitrium hexapeptide, the cellular receptor AimR and the lysogenic negative regulator AimX. This system controls the decision between the lytic and lysogenic cycles. However, both the mechanism of molecular recognition between the arbitrium peptide and AimR and how downstream gene expression is regulated remain unknown. Here, we report crystal structures for AimR from the SPbeta phage in the apo form and the arbitrium peptide-bound form at 2.20 Å and 1.92 Å, respectively. With or without the peptide, AimR dimerizes through the C-terminal capping helix. AimR assembles a superhelical fold and accommodates the peptide encircled by its tetratricopeptide repeats, which is reminiscent of RRNPP fam- ily members from the quorum-sensing system. In the absence of the arbitrium peptide, AimR targets the upstream sequence of the aimX gene; its DNA binding activity is prevented following peptide binding. In summary, our findings provide a structural basis for peptide recognition in the phage lysis–lysogeny decision communication system. uring the infection of a bacterial host, a temperate phage can The AimP protein consists of 43 amino acids that encode an either enter the lytic cycle or the lysogenic cycle.
    [Show full text]
  • Ab Komplet 6.07.2018
    CONTENTS 1. Welcome addresses 2 2. Introduction 3 3. Acknowledgements 10 4. General information 11 5. Scientific program 16 6. Abstracts – oral presentations 27 7. Abstracts – poster sessions 99 8. Participants 419 1 EMBO Workshop Viruses of Microbes 2018 09 – 13 July 2018 | Wrocław, Poland 1. WELCOME ADDRESSES Welcome to the Viruses of Microbes 2018 EMBO Workshop! We are happy to welcome you to Wrocław for the 5th meeting of the Viruses of Microbes series. This series was launched in the year 2010 in Paris, and was continued in Brussels (2012), Zurich (2014), and Liverpool (2016). This year our meeting is co-organized by two partner institutions: the University of Wrocław and the Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of Sciences. The conference venue (University of Wrocław, Uniwersytecka 7-10, Building D) is located in the heart of Wrocław, within the old, historic part of the city. This creates an opportunity to experience the over 1000-year history of the city, combined with its current positive energy. The Viruses of Microbes community is constantly growing. More and more researchers are joining it, and they represent more and more countries worldwide. Our goal for this meeting was to create a true global platform for networking and exchanging ideas. We are most happy to welcome representatives of so many countries and continents. To accommodate the diversity and expertise of the scientists and practitioners gathered by VoM2018, the leading theme of this conference is “Biodiversity and Future Application”. With the help of your contribution, this theme was developed into a program covering a wide range of topics with the strongest practical aspect.
    [Show full text]
  • A Review of Phage Therapy Against Bacterial Pathogens of Aquatic and Terrestrial Organisms
    viruses Review A Review of Phage Therapy against Bacterial Pathogens of Aquatic and Terrestrial Organisms Janis Doss, Kayla Culbertson, Delilah Hahn, Joanna Camacho and Nazir Barekzi * Old Dominion University, Department of Biological Sciences, 5115 Hampton Blvd, Norfolk, VA 23529, USA; [email protected] (J.D.); [email protected] (K.C.); [email protected] (D.H.); [email protected] (J.C.) * Correspondence: [email protected] Academic Editor: Jens H. Kuhn Received: 27 January 2017; Accepted: 13 March 2017; Published: 18 March 2017 Abstract: Since the discovery of bacteriophage in the early 1900s, there have been numerous attempts to exploit their innate ability to kill bacteria. The purpose of this report is to review current findings and new developments in phage therapy with an emphasis on bacterial diseases of marine organisms, humans, and plants. The body of evidence includes data from studies investigating bacteriophage in marine and land environments as modern antimicrobial agents against harmful bacteria. The goal of this paper is to present an overview of the topic of phage therapy, the use of phage-derived protein therapy, and the hosts that bacteriophage are currently being used against, with an emphasis on the uses of bacteriophage against marine, human, animal and plant pathogens. Keywords: bacteriophage; Vibrio phage; phage therapy; aquaculture 1. Introduction Bacteriophage are commonly referred to as phage and are defined as viruses that infect bacteria. Phage are ubiquitous and require a bacterial host. They are also the most abundant organisms found in the biosphere. Bacteriophage-bacterial host interactions have been exploited by scientists as tools to understand basic molecular biology, genetic recombination events, horizontal gene transfer, and how bacterial evolution has been driven by phage [1].
    [Show full text]
  • Cap 1 I VIRUS
    Cap 1 I VIRUS BIOLOGIA Un virus (voce dotta dal latino virus, -i, 'veleno') è un microrganismo a-cellulare con caratteristiche di parassita obbligato, in quanto si replica esclusivamente all'interno delle cellule di altri organismi. I virus possono infettare tutti i tipi di forme di vita, dagli animali, alle piante, ai microrganismi (compresi batteri e archeobatteri) e anche altri virus. Nel 1892 Dmitri Ivanovsky descrisse in un articolo un agente patogeno non batterico in grado di infettare le piante di tabacco, da cui in seguito, sei anni più tardi, Martinus BeiJerinck scoprì il virus del mosaico del tabacco nel 1898. Da allora, circa 5.000 specie di virus sono state descritte in dettaglio, anche se si ritiene che ve ne siano milioni di diversi tipi. I virus si trovano in quasi tutti gli ecosistemi della Terra e rappresentano l'entità biologica più abbondante in assoluto. La disciplina che si occupa dello studio dei virus è nota come virologia, una sub-specialità della microbiologia. Quando non si trovano all'interno di una cellula infetta o nella fase di infettarne una, i virus esistono in forma di particelle indipendenti e inattive. Queste particelle virali, note anche come virioni, sono costituite da due o tre parti: 1. il materiale genetico costituito da DNA o RNA, lunghe molecole che trasportano le informazioni genetiche; 2. un rivestimento proteico, chiamato capside, che circonda e protegge il materiale genetico; e in alcuni casi 3. una sacca di lipidi che circonda il rivestimento proteico quando sono fuori dalla cellula. Le forme di queste particelle di virus vanno da semplici forme elicoidali e icosaedriche per alcune specie di virus, fino a strutture più complesse per altre.
    [Show full text]
  • University of Groningen the Ecology and Evolution of Bacteriophages Of
    University of Groningen The ecology and evolution of bacteriophages of mycosphere-inhabiting Paraburkholderia spp. Pratama, Akbar Adjie IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2018 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Pratama, A. A. (2018). The ecology and evolution of bacteriophages of mycosphere-inhabiting Paraburkholderia spp. Rijksuniversiteit Groningen. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 29-09-2021 Chapter 1 General Introduction Akbar Adjie Pratama and Jan Dirk van Elsas Partly published in Book chapter: The viruses in soil – potential roles, activities and impacts.
    [Show full text]
  • The Secret Social Lives of Viruses Long Thought the Lone Wolves of the Microbial World, Viruses Are Turning out to Be Surprisingly Sociable
    The secret social lives of viruses Long thought the lone wolves of the microbial world, viruses are turning out to be surprisingly sociable. Listening in could be the key to fighting infection. BY ELIE DOLGIN eneticist Rotem Sorek could see that his bacteria replicate and burst out, in search of new victims. were sick — so far, so good. He had deliberately It was an accidental discovery that would fundamentally infected them with a virus to test whether each ail- change scientists’ understanding of how viruses behave. Ging microbe soldiered on alone or communicated Viruses that infect bacteria — spiky lollipop-like crea- with its allies to fight the attack. tures known as bacteriophages (or phages) — have surveil- But when he and his team at the Weizmann Institute lance mechanisms that bring them intel on whether to stay of Science in Rehovot, Israel, looked into the contents of dormant or attack, depending on the availability of fresh their flasks, they saw something completely unexpected: victims. But researchers long thought these processes were KAROL BANACH BY ILLUSTRATION the bacteria were silent, and it was the viruses that were passive; the phages seemed to just sit back and listen in, chattering away, passing notes to each other in a molecular waiting for bacterial distress signals to reach fever pitch language only they could understand. They were decid- before taking action. ing together when to lie low in the host cell and when to Sorek and his colleagues had found phages actively 290 | NATURE | VOL 570 | 20 JUNE 2019 ©2019 Spri nger Nature Li mited.
    [Show full text]
  • Repeated Outbreaks Drive the Evolution of Bacteriophage Communication Hilje M Doekes1,2*, Glenn a Mulder1, Rutger Hermsen1
    RESEARCH ARTICLE Repeated outbreaks drive the evolution of bacteriophage communication Hilje M Doekes1,2*, Glenn A Mulder1, Rutger Hermsen1 1Theoretical Biology, Department of Biology, Utrecht University, Utrecht, Netherlands; 2Laboratory of Genetics, Department of Plant Sciences, Wageningen University, Wageningen, Netherlands Abstract Recently, a small-molecule communication mechanism was discovered in a range of Bacillus-infecting bacteriophages, which these temperate phages use to inform their lysis-lysogeny decision. We present a mathematical model of the ecological and evolutionary dynamics of such viral communication and show that a communication strategy in which phages use the lytic cycle early in an outbreak (when susceptible host cells are abundant) but switch to the lysogenic cycle later (when susceptible cells become scarce) is favoured over a bet-hedging strategy in which cells are lysogenised with constant probability. However, such phage communication can evolve only if phage-bacteria populations are regularly perturbed away from their equilibrium state, so that acute outbreaks of phage infections in pools of susceptible cells continue to occur. Our model then predicts the selection of phages that switch infection strategy when half of the available susceptible cells have been infected. Introduction For several decades now, it has been recognised that communication between individuals is not lim- ited to multicellular organisms, but is also common among microbes. The best-known example of microbial communication is bacterial
    [Show full text]