Publications by authors named "Marianne De Paepe"

16 Publications

  • Page 1 of 1

Viruses of Microbes 2020: The Latest Conquest on Viruses of Microbes.

Viruses 2021 04 30;13(5). Epub 2021 Apr 30.

Centre for Ecology and Evolution in Microbial Model Systems (EEMiS), Department of Biology and Environmental Science, Faculty of Health and Life Sciences, Linnaeus University, SE-39231 Kalmar, Sweden.

This Special Issue celebrates viruses of microbes: those viruses that infect archaea, bacteria and microbial eukaryotes [...].
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http://dx.doi.org/10.3390/v13050802DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8147119PMC
April 2021

The enemy from within: a prophage of Roseburia intestinalis systematically turns lytic in the mouse gut, driving bacterial adaptation by CRISPR spacer acquisition.

ISME J 2020 03 11;14(3):771-787. Epub 2019 Dec 11.

Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, 78350, Jouy-en-Josas, France.

Despite an overall temporal stability in time of the human gut microbiota at the phylum level, strong variations in species abundance have been observed. We are far from a clear understanding of what promotes or disrupts the stability of microbiome communities. Environmental factors, like food or antibiotic use, modify the gut microbiota composition, but their overall impacts remain relatively low. Phages, the viruses that infect bacteria, might constitute important factors explaining temporal variations in species abundance. Gut bacteria harbour numerous prophages, or dormant viruses, which can evolve to become ultravirulent phage mutants, potentially leading to important bacterial death. Whether such phenomenon occurs in the mammal's microbiota has been largely unexplored. Here we studied temperate phage-bacteria coevolution in gnotoxenic mice colonised with Roseburia intestinalis, a dominant symbiont of the human gut microbiota, and Escherichia coli, a sub-dominant member of the same microbiota. We show that R. intestinalis L1-82 harbours two active prophages, Jekyll and Shimadzu. We observed the systematic evolution in mice of ultravirulent Shimadzu phage mutants, which led to a collapse of R. intestinalis population. In a second step, phage infection drove the fast counter-evolution of host phage resistance mainly through phage-derived spacer acquisition in a clustered regularly interspaced short palindromic repeats array. Alternatively, phage resistance was conferred by a prophage originating from an ultravirulent phage with a restored ability to lysogenize. Our results demonstrate that prophages are a potential source of ultravirulent phages that can successfully infect most of the susceptible bacteria. This suggests that prophages can play important roles in the short-term temporal variations observed in the composition of the gut microbiota.
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http://dx.doi.org/10.1038/s41396-019-0566-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7031369PMC
March 2020

Viral metagenomic analysis of the cheese surface: A comparative study of rapid procedures for extracting viral particles.

Food Microbiol 2020 Feb 24;85:103278. Epub 2019 Jul 24.

UMR1319 MICALIS, INRA, AgroParisTech, Université Paris-Saclay, Domaine de Vilvert, 78350, Jouy-en-Josas, France.

The structure and functioning of microbial communities from fermented foods, including cheese, have been extensively studied during the past decade. However, there is still a lack of information about both the occurrence and the role of viruses in modulating the function of this type of spatially structured and solid ecosystems. Viral metagenomics was recently applied to a wide variety of environmental samples and standardized procedures for recovering viral particles from different type of materials has emerged. In this study, we adapted a procedure originally developed to extract viruses from fecal samples, in order to enable efficient virome analysis of cheese surface. We tested and validated the positive impact of both addition of a filtration step prior to virus concentration and substitution of purification by density gradient ultracentrifugation by a simple chloroform treatment to eliminate membrane vesicles. Viral DNA extracted from the several procedures, as well as a vesicle sample, were sequenced using Illumina paired-end MiSeq technology and the subsequent clusters assembled from the virome were analyzed to assess those belonging to putative phages, plasmid-derived DNA, or even from bacterial chromosomal DNA. The best procedure was then chosen, and used to describe the first cheese surface virome, using Epoisses cheese as example. This study provides the basis of future investigations regarding the ecological importance of viruses in cheese microbial ecosystems.
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http://dx.doi.org/10.1016/j.fm.2019.103278DOI Listing
February 2020

Phages infecting Faecalibacterium prausnitzii belong to novel viral genera that help to decipher intestinal viromes.

Microbiome 2018 04 3;6(1):65. Epub 2018 Apr 3.

Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, 78350, Jouy-en-Josas, France.

Background: Viral metagenomic studies have suggested a role for bacteriophages in intestinal dysbiosis associated with several human diseases. However, interpretation of viral metagenomic studies is limited by the lack of knowledge of phages infecting major human gut commensal bacteria, such as Faecalibacterium prausnitzii, a bacterial symbiont repeatedly found depleted in inflammatory bowel disease (IBD) patients. In particular, no complete genomes of phages infecting F. prausnitzii are present in viral databases.

Methods: We identified 18 prophages in 15 genomes of F. prausnitzii, used comparative genomics to define eight phage clades, and annotated the genome of the type phage of each clade. For two of the phages, we studied prophage induction in vitro and in vivo in mice. Finally, we aligned reads from already published viral metagenomic data onto the newly identified phages.

Results: We show that each phage clade represents a novel viral genus and that a surprisingly large fraction of them (10 of the 18 phages) codes for a diversity-generating retroelement, which could contribute to their adaptation to the digestive tract environment. We obtained either experimental or in silico evidence of activity for at least one member of each genus. In addition, four of these phages are either significantly more prevalent or more abundant in stools of IBD patients than in those of healthy controls.

Conclusion: Since IBD patients generally have less F. prausnitzii in their microbiota than healthy controls, the higher prevalence or abundance of some of its phages may indicate that they are activated during disease. This in turn suggests that phages could trigger or aggravate F. prausnitzii depletion in patients. Our results show that prophage detection in sequenced strains of the microbiota can usefully complement viral metagenomic studies.
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http://dx.doi.org/10.1186/s40168-018-0452-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5883640PMC
April 2018

Inflammation boosts bacteriophage transfer between spp.

Science 2017 03 16;355(6330):1211-1215. Epub 2017 Mar 16.

Institute of Microbiology, ETH Zurich, Switzerland.

Bacteriophage transfer (lysogenic conversion) promotes bacterial virulence evolution. There is limited understanding of the factors that determine lysogenic conversion dynamics within infected hosts. A murine Typhimurium (Tm) diarrhea model was used to study the transfer of SopEΦ, a prophage from Tm SL1344, to Tm ATCC14028S. Gut inflammation and enteric disease triggered >55% lysogenic conversion of ATCC14028S within 3 days. Without inflammation, SopEΦ transfer was reduced by up to 10-fold. This was because inflammation (e.g., reactive oxygen species, reactive nitrogen species, hypochlorite) triggers the bacterial SOS response, boosts expression of the phage antirepressor Tum, and thereby promotes free phage production and subsequent transfer. Mucosal vaccination prevented a dense intestinal Tm population from inducing inflammation and consequently abolished SopEΦ transfer. Vaccination may be a general strategy for blocking pathogen evolution that requires disease-driven transfer of temperate bacteriophages.
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http://dx.doi.org/10.1126/science.aaf8451DOI Listing
March 2017

Carriage of λ Latent Virus Is Costly for Its Bacterial Host due to Frequent Reactivation in Monoxenic Mouse Intestine.

PLoS Genet 2016 Feb 12;12(2):e1005861. Epub 2016 Feb 12.

Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France.

Temperate phages, the bacterial viruses able to enter in a dormant prophage state in bacterial genomes, are present in the majority of bacterial strains for which the genome sequence is available. Although these prophages are generally considered to increase their hosts' fitness by bringing beneficial genes, studies demonstrating such effects in ecologically relevant environments are relatively limited to few bacterial species. Here, we investigated the impact of prophage carriage in the gastrointestinal tract of monoxenic mice. Combined with mathematical modelling, these experimental results provided a quantitative estimation of key parameters governing phage-bacteria interactions within this model ecosystem. We used wild-type and mutant strains of the best known host/phage pair, Escherichia coli and phage λ. Unexpectedly, λ prophage caused a significant fitness cost for its carrier, due to an induction rate 50-fold higher than in vitro, with 1 to 2% of the prophage being induced. However, when prophage carriers were in competition with isogenic phage susceptible bacteria, the prophage indirectly benefited its carrier by killing competitors: infection of susceptible bacteria led to phage lytic development in about 80% of cases. The remaining infected bacteria were lysogenized, resulting overall in the rapid lysogenization of the susceptible lineage. Moreover, our setup enabled to demonstrate that rare events of phage gene capture by homologous recombination occurred in the intestine of monoxenic mice. To our knowledge, this study constitutes the first quantitative characterization of temperate phage-bacteria interactions in a simplified gut environment. The high prophage induction rate detected reveals DNA damage-mediated SOS response in monoxenic mouse intestine. We propose that the mammalian gut, the most densely populated bacterial ecosystem on earth, might foster bacterial evolution through high temperate phage activity.
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http://dx.doi.org/10.1371/journal.pgen.1005861DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4752277PMC
February 2016

Killing the killers.

Elife 2014 Sep 2;3:e04168. Epub 2014 Sep 2.

Marie-Agnès Petit is in the French National Institute for Agricultural Research and AgroParisTech, Micalis Institute, Jouy-en-Josas, France

The bacteria that infect humans and cause cholera are themselves infected by viruses, which have the potential to influence the course of a cholera infection.
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http://dx.doi.org/10.7554/eLife.04168DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4151084PMC
September 2014

Bacteriophages: an underestimated role in human and animal health?

Front Cell Infect Microbiol 2014 28;4:39. Epub 2014 Mar 28.

Institut National de la Recherche Agronomique, Micalis, UMR 1319 Jouy en Josas, France ; Agroparistech, Micalis, UMR 1319 Jouy en Josas, France.

Metagenomic approaches applied to viruses have highlighted their prevalence in almost all microbial ecosystems investigated. In all ecosystems, notably those associated with humans or animals, the viral fraction is dominated by bacteriophages. Whether they contribute to dysbiosis, i.e., the departure from microbiota composition in symbiosis at equilibrium and entry into a state favoring human or animal disease is unknown at present. This review summarizes what has been learnt on phages associated with human and animal microbiota, and focuses on examples illustrating the several ways by which phages may contribute to a shift to pathogenesis, either by modifying population equilibrium, by horizontal transfer, or by modulating immunity.
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http://dx.doi.org/10.3389/fcimb.2014.00039DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3975094PMC
September 2014

Temperate phages acquire DNA from defective prophages by relaxed homologous recombination: the role of Rad52-like recombinases.

PLoS Genet 2014 Mar 6;10(3):e1004181. Epub 2014 Mar 6.

INRA, UMR1319, Micalis, domaine de Vilvert, Jouy en Josas, France; AgroParisTech, UMR1319, Micalis, domaine de Vilvert, Jouy en Josas, France.

Bacteriophages (or phages) dominate the biosphere both numerically and in terms of genetic diversity. In particular, genomic comparisons suggest a remarkable level of horizontal gene transfer among temperate phages, favoring a high evolution rate. Molecular mechanisms of this pervasive mosaicism are mostly unknown. One hypothesis is that phage encoded recombinases are key players in these horizontal transfers, thanks to their high efficiency and low fidelity. Here, we associate two complementary in vivo assays and a bioinformatics analysis to address the role of phage encoded recombinases in genomic mosaicism. The first assay allowed determining the genetic determinants of mosaic formation between lambdoid phages and Escherichia coli prophage remnants. In the second assay, recombination was monitored between sequences on phage λ, and allowed to compare the performance of three different Rad52-like recombinases on the same substrate. We also addressed the importance of homologous recombination in phage evolution by a genomic comparison of 84 E. coli virulent and temperate phages or prophages. We demonstrate that mosaics are mainly generated by homology-driven mechanisms that tolerate high substrate divergence. We show that phage encoded Rad52-like recombinases act independently of RecA, and that they are relatively more efficient when the exchanged fragments are divergent. We also show that accessory phage genes orf and rap contribute to mosaicism. A bioinformatics analysis strengthens our experimental results by showing that homologous recombination left traces in temperate phage genomes at the borders of recently exchanged fragments. We found no evidence of exchanges between virulent and temperate phages of E. coli. Altogether, our results demonstrate that Rad52-like recombinases promote gene shuffling among temperate phages, accelerating their evolution. This mechanism may prove to be more general, as other mobile genetic elements such as ICE encode Rad52-like functions, and play an important role in bacterial evolution itself.
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http://dx.doi.org/10.1371/journal.pgen.1004181DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3945230PMC
March 2014

Respiratory complex I deficiency induces drought tolerance by impacting leaf stomatal and hydraulic conductances.

Planta 2012 Mar 15;235(3):603-14. Epub 2011 Oct 15.

Laboratoire de Physiologie et Biologie des Organismes, Université des Sciences et de la Technologie Houari Boumediene, BP 39, El Alia, Bab Ezzouar, Algiers, Algeria.

To investigate the role of plant mitochondria in drought tolerance, the response to water deprivation was compared between Nicotiana sylvestris wild type (WT) plants and the CMSII respiratory complex I mutant, which has low-efficient respiration and photosynthesis, high levels of amino acids and pyridine nucleotides, and increased antioxidant capacity. We show that the delayed decrease in relative water content after water withholding in CMSII, as compared to WT leaves, is due to a lower stomatal conductance. The stomatal index and the abscisic acid (ABA) content were unaffected in well-watered mutant leaves, but the ABA/stomatal conductance relation was altered during drought, indicating that specific factors interact with ABA signalling. Leaf hydraulic conductance was lower in mutant leaves when compared to WT leaves and the role of oxidative aquaporin gating in attaining a maximum stomatal conductance is discussed. In addition, differences in leaf metabolic status between the mutant and the WT might contribute to the low stomatal conductance, as reported for TCA cycle-deficient plants. After withholding watering, TCA cycle derived organic acids declined more in CMSII leaves than in the WT, and ATP content decreased only in the CMSII. Moreover, in contrast to the WT, total free amino acid levels declined whilst soluble protein content increased in CMSII leaves, suggesting an accelerated amino acid remobilisation. We propose that oxidative and metabolic disturbances resulting from remodelled respiration in the absence of Complex I activity could be involved in bringing about the lower stomatal and hydraulic conductances.
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http://dx.doi.org/10.1007/s00425-011-1524-7DOI Listing
March 2012

Trade-off between bile resistance and nutritional competence drives Escherichia coli diversification in the mouse gut.

PLoS Genet 2011 Jun 16;7(6):e1002107. Epub 2011 Jun 16.

INSERM, U989, Université Paris Descartes, Paris, France.

Bacterial diversification is often observed, but underlying mechanisms are difficult to disentangle and remain generally unknown. Moreover, controlled diversification experiments in ecologically relevant environments are lacking. We studied bacterial diversification in the mammalian gut, one of the most complex bacterial environments, where usually hundreds of species and thousands of bacterial strains stably coexist. Herein we show rapid genetic diversification of an Escherichia coli strain upon colonisation of previously germ-free mice. In addition to the previously described mutations in the EnvZ/OmpR operon, we describe the rapid and systematic selection of mutations in the flagellar flhDC operon and in malT, the transcriptional activator of the maltose regulon. Moreover, within each mouse, the three mutant types coexisted at different levels after one month of colonisation. By combining in vivo studies and determination of the fitness advantages of the selected mutations in controlled in vitro experiments, we provide evidence that the selective forces that drive E. coli diversification in the mouse gut are the presence of bile salts and competition for nutrients. Altogether our results indicate that a trade-off between stress resistance and nutritional competence generates sympatric diversification of the gut microbiota. These results illustrate how experimental evolution in natural environments enables identification of both the selective pressures that organisms face in their natural environment and the diversification mechanisms.
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http://dx.doi.org/10.1371/journal.pgen.1002107DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3116916PMC
June 2011

Emergence of variability in isogenic Escherichia coli populations infected by a filamentous virus.

PLoS One 2010 Jul 27;5(7):e11823. Epub 2010 Jul 27.

INSERM, Unité 1001, Génétique Moléculaire Evolutive et Médicale, Paris, France; Université Paris-Descartes, Paris, France.

The spread of epidemics not only depends on the average number of parasites produced per host, but also on the existence of highly infectious individuals. It is widely accepted that infectiousness depends on genetic and environmental determinants. However, even in clonal populations of host and viruses growing in homogeneous conditions, high variability can exist. Here we show that Escherichia coli cells commonly display high differentials in viral burst size, and address the kinetics of emergence of such variability with the non-lytic filamentous virus M13. By single-cell imaging of a virally-encoded fluorescent reporter, we monitor the viral charge distribution in infected bacterial populations at different time following infection. A mathematical model assuming autocatalytic virus replication and inheritance of bacterial growth rates quantitatively reproduces the experimental distributions, demonstrating that deterministic amplification of small host inhomogeneities is a mechanism sufficient to explain large and highly skewed distributions. This mechanism of amplification is general and may occur whenever a parasite has an initial phase of exponential growth within its host. Moreover, it naturally reproduces the shift towards higher virulence when the host is experimenting poor conditions, as observed commonly in host-parasite systems.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0011823PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2910729PMC
July 2010

The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses.

Immunity 2009 Oct;31(4):677-89

INRA, U910, Unité Ecologie et Physiologie du Système Digestif, Domaine de Vilvert, 78350 Jouy-en-Josas, France.

Microbiota-induced cytokine responses participate in gut homeostasis, but the cytokine balance at steady-state and the role of individual bacterial species in setting the balance remain elusive. Herein, systematic analysis of gnotobiotic mice indicated that colonization by a whole mouse microbiota orchestrated a broad spectrum of proinflammatory T helper 1 (Th1), Th17, and regulatory T cell responses whereas most tested complex microbiota and individual bacteria failed to efficiently stimulate intestinal T cell responses. This function appeared the prerogative of a restricted number of bacteria, the prototype of which is the segmented filamentous bacterium, a nonculturable Clostridia-related species, which could largely recapitulate the coordinated maturation of T cell responses induced by the whole mouse microbiota. This bacterium, already known as a potent inducer of mucosal IgA, likely plays a unique role in the postnatal maturation of gut immune functions. Changes in the infant flora may thus influence the development of host immune responses.
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http://dx.doi.org/10.1016/j.immuni.2009.08.020DOI Listing
October 2009

Dissecting the genetic components of adaptation of Escherichia coli to the mouse gut.

PLoS Genet 2008 Jan 27;4(1):e2. Epub 2007 Nov 27.

INSERM, U571, Paris, France.

While pleiotropic adaptive mutations are thought to be central for evolution, little is known on the downstream molecular effects allowing adaptation to complex ecologically relevant environments. Here we show that Escherichia coli MG1655 adapts rapidly to the intestine of germ-free mice by single point mutations in EnvZ/OmpR two-component signal transduction system, which controls more than 100 genes. The selective advantage conferred by the mutations that modulate EnvZ/OmpR activities was the result of their independent and additive effects on flagellin expression and permeability. These results obtained in vivo thus suggest that global regulators may have evolved to coordinate activities that need to be fine-tuned simultaneously during adaptation to complex environments and that mutations in such regulators permit adjustment of the boundaries of physiological adaptation when switching between two very distinct environments.
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http://dx.doi.org/10.1371/journal.pgen.0040002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2174974PMC
January 2008

Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare.

Curr Biol 2006 Oct;16(20):2048-52

Section of Integrative Biology, University of Texas at Austin, Austin, Texas 78712, USA.

Locally adapted residents present a formidable barrier to invasion . One solution for invaders is to kill residents . Here, we explore the comparative ecological dynamics of two distinct microbial mechanisms of killing competitors, via the release of chemicals (e.g., bacteriocins ) and via the release of parasites (e.g., temperate phage ). We compared the short-term population dynamics of susceptible E. coli K12 and isogenic carriers of phage varphi80 in experimental cultures to that anticipated by mathematical models using independently derived experimental parameters. Whereas phages are a direct burden to their carriers because of probabilistic host lysis, by killing competitor bacteria they can indirectly benefit bacterial kin made immune by carrying isogenic phage. This is similar to previously described bacteriocin-mediated effects. However, unlike chemical killing, viable phage trigger an epidemic among susceptible competitors, which become factories producing more phage. Amplification makes phage carriers able to invade well-mixed susceptibles even faster when rare, whereas chemical killers can only win in a well-mixed environment when sufficiently abundant. We demonstrate that for plausible parameters, the release of chemical toxins is superior as a resident strategy to repel invasions, whereas the release of temperate phage is superior as a strategy of invasion.
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http://dx.doi.org/10.1016/j.cub.2006.08.089DOI Listing
October 2006

Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages.

PLoS Biol 2006 Jul;4(7):e193

Laboratoire de Genetique Moleculaire, Evolutive et Medicale, University of Paris 5, INSERM, Paris, France.

Life history theory accounts for variations in many traits involved in the reproduction and survival of living organisms, by determining the constraints leading to trade-offs among these different traits. The main life history traits of phages-viruses that infect bacteria-are the multiplication rate in the host, the survivorship of virions in the external environment, and their mode of transmission. By comparing life history traits of 16 phages infecting the bacteria Escherichia coli, we show that their mortality rate is constant with time and positively [corrected] correlated to their multiplication rate in the bacterial host. Even though these viruses do not age, this result is in line with the trade-off between survival and reproduction previously observed in numerous aging organisms. Furthermore, a multiple regression shows that the combined effects of two physical parameters, namely, the capsid thickness and the density of the packaged genome, account for 82% of the variation in the mortality rate. The correlations between life history traits and physical characteristics of virions may provide a mechanistic explanation of this trade-off. The fact that this trade-off is present in this very simple biological situation suggests that it might be a fundamental property of evolving entities produced under constraints. Moreover, such a positive correlation between mortality and multiplication reveals an underexplored trade-off in host-parasite interactions.
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http://dx.doi.org/10.1371/journal.pbio.0040193DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1475768PMC
July 2006
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