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The Diversity of Bacterial Lifestyles Hampers Bacteriophage Tenacity

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The Diversity of Bacterial Lifestyles Hampers Bacteriophage Tenacity viruses Review The Diversity of Bacterial Lifestyles Hampers Bacteriophage Tenacity Marta Lourenço 1,2, Luisa De Sordi 1 and Laurent Debarbieux 1,* ID 1 Department of Microbiology, Institut Pasteur, F-75015 Paris, France; [email protected] (M.L.); [email protected] (L.D.S.) 2 Collège Doctoral, Sorbonne Université, F-75005 Paris, France * Correspondence: [email protected] Received: 18 May 2018; Accepted: 11 June 2018; Published: 15 June 2018 Abstract: Phage therapy is based on a simple concept: the use of a virus (bacteriophage) that is capable of killing specific pathogenic bacteria to treat bacterial infections. Since the pioneering work of Félix d’Herelle, bacteriophages (phages) isolated in vitro have been shown to be of therapeutic value. Over decades of study, a large number of rather complex mechanisms that are used by phages to hijack bacterial resources and to produce their progeny have been deciphered. While these mechanisms have been identified and have been studied under optimal conditions in vitro, much less is known about the requirements for successful viral infections in relevant natural conditions. This is particularly true in the context of phage therapy. Here, we highlight the parameters affecting phage replication in both in vitro and in vivo environments, focusing, in particular, on the mammalian digestive tract. We propose avenues for increasing the knowledge-guided implementation of phages as therapeutic tools. Keywords: virus–host interactions; bacteriophage efficacy; gastrointestinal tract; phage therapy 1. Introduction With the alarming worldwide increase in the prevalence of multidrug-resistant bacteria, phage therapy—the use of phages to target pathogenic bacteria [1]—has recently returned to the spotlight in the USA and Europe, although it had never fallen out of favour in countries such as Georgia [2]. The three main characteristics of phages that make phage therapy an appealing strategy are (i) the self-replication of phages, leading to a local increase in their concentration; (ii) the lack of broad off-target effects due to the narrow host specificity of phages and (iii) genomic flexibility making it possible to rapidly develop optimised variants. The recent publication of a successful compassionate clinical case treatment with phages has highlighted the potential value of phage therapy in the context of human health [3,4]. However, in modern phase II clinical trials, the efficacy of phage therapy was highly variable in a small number of patients with chronic otitis, and phage therapy was ineffective in a larger trial with children with diarrhoea [5,6]. This lack of success may partly reflect the paucity of data relating to the translation from in vitro to clinical settings [7]. We must, therefore, address the challenge of identifying the parameters characterising effective phage treatments. For example, in studies of several experimental models investigating the use of phages to target bacteria residing in the digestive tract of animals, treatment efficacy has been reported to range from complete inefficacy to highly successful [8–12]. These findings contrast strongly with in vitro observations in which most, if not all, phages are highly efficient at infecting their host. These discrepancies may be explained by the influence of the bacterial lifestyle on phage infection, as discussed below. Viruses 2018, 10, 327; doi:10.3390/v10060327 www.mdpi.com/journal/viruses Viruses 20182018,, 1010,, 327x 2 of 1110 2. Bacteria Provide Essential Support for the Parasitic Lifestyle of Phages 2. Bacteria Provide Essential Support for the Parasitic Lifestyle of Phages Bacteria are among the most ubiquitous organisms on the planet and their high levels of diversityBacteria are regularly are among confirmed the most in ubiquitousmetagenomics organisms studies [13–15]. on the planetBacteria and colonise their higha multitude levels of diversityenvironments, are regularly from oceans confirmed to deserts, in metagenomics demonstrati studiesng their [13 great–15]. Bacteriaability to colonise thrive ain multitude different ofenvironments environments, and fromto regulate oceans major to deserts, global processes, demonstrating such theiras the great biogeochemical ability tothrive cycles inof differentessential environmentselements (carbon, and nitrogen, to regulate oxygen) major [16]. global processes, such as the biogeochemical cycles of essential elementsFrom (carbon, an anthropocentric nitrogen, oxygen) point of [16 view,]. most bacteria are harmless while a few are beneficial or pathogenic.From an Bacteria anthropocentric isolated from point many of view, body most sites bacteriahave been are shown harmless to survive while ain few various are beneficial conditions, or pathogenic.such as the acidic Bacteria medium isolated of from the stomach many body or the sites hi haveghly beenoxygenated shown torespiratory survive in tract. various Even conditions, within a suchsingle as species, the acidic bacteria medium may display of the stomach considerable or the phenotypic highly oxygenated flexibility. respiratory This is illustrated tract. Even by the within well- aknown single model species, bacterium bacteria mayEscherichia display coli considerable, a facultative phenotypic anaerobe flexibility. able to survive This is in illustrated environmental by the well-knownconditions that model are bacterium very differentEscherichia from coliits, anatu facultativeral habitat, anaerobe the digestive able to survive tract of in warm-blooded environmental conditionsanimals [17]. that are very different from its natural habitat, the digestive tract of warm-blooded animalsBacterial [17]. physiological responses play a crucial role in shaping the interactions of bacteria with their Bacterialenvironment. physiological The recent responses development play of a seve crucialral techniques role in shaping (membrane, the interactions chip, RNASeq), of bacteria which withfacilitate their the environment. capture of mRNAs, The recent has development made a fundam of severalental contribution techniques (membrane,to the description chip, RNASeq), of global whichphysiological facilitate responses the capture in ofbacteria. mRNAs, These has madetechni aques fundamental have made contribution it possible to for the researchers description ofto globaldescribe physiological the transcriptomic responses profile in bacteria. of bacteria These growing techniques in several have madedifferent it possible types of for conditions researchers [18– to describe23]. For example, the transcriptomic Denou et profileal. compared of bacteria Lactobacillus growing injohnsonii several gene different expression typesof between conditions in vitro [18– 23(in]. Forflasks) example, and in Denou vivo et(mouse al. compared gastrointestinalLactobacillus trac johnsoniit) conditionsgene expression and in betweendifferentin sections vitro (in of flasks) the andgastrointestinalin vivo (mouse tract gastrointestinal (stomach, caecum tract) and conditions colon) [18]. and Their in different observations sections confirmed of the gastrointestinal that the animal tracthost, (stomach,either directly caecum or andindirectly colon) via [18 ].other Their micr observationsobes, influences confirmed gene thatexpression the animal in the host, bacterial either directlypopulations or indirectly colonizing via different other microbes,body sites. influences gene expression in the bacterial populations colonizingPhages different are obligate body parasites sites. and, as such, their distribution matches that of the bacteria they infect.Phages Bacteria are may obligate be susceptible parasites to and, phages as such, or resistant their distribution via many mechanisms matches that developed of the bacteria by bacteria they infect.during Bacteriathe course may of be their susceptible coevolution to phages with or resistantphages. viaBacteria many can mechanisms prevent phage developed adsorption by bacteria by duringdeleting the phage course receptors, of their coevolutionmodifying their with conformation, phages. Bacteria or canreleasing prevent factors phage that adsorption occupy the by deletingbinding phagesite or receptors,even mask modifying it. Other mechanisms their conformation, of protecti or releasingon involve factors the prevention that occupy of the phage binding DNA site injection, or even maskthe digestion it. Other of mechanisms phage DNA of by protection restriction-modific involve theation prevention enzymes of phageor by the DNA CRISPR-Cas injection, the machinery. digestion ofFor phage a more DNA comprehensive by restriction-modification and detailed description enzymes of or these by the phage CRISPR-Cas resistance machinery. mechanisms, For we a morerefer comprehensivethe reader to the and review detailed by Labrie, description S.J., et of al. these [24]. phageIn 2015, resistance a novel system mechanisms, called weBREX refer (bacteriophage the reader to theexclusion) review bywas Labrie, described S.J., etand al. reported [24]. In 2015, to specifical a novel systemly prevent called phage BREX DNA (bacteriophage replication exclusion)[25]. Doron was et describedal. (2018) andrecently reported used to comparative specifically prevent genomics phage to DNApredict replication an impressive [25]. Doron list of et al.26 (2018)new putative recently usedantiphage comparative systems, genomics nine of towhich predict were an impressiveexperiment listally of validated 26 new putative [26]. In antiphage addition, systems,environmental nine of
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