High cell densities favor lysogeny: induction of an H20 prophage is repressed by quorum sensing and enhances biofilm formation in Vibrio anguillarum

ISME Journal - Tập 14 Số 7 - Trang 1731-1742 - 2020
Demeng Tan1,2,3, Mads Frederik Hansen2,4, Luís Nunes de Carvalho2, Henriette Lyng Røder2, Mette Burmølle2, Mathias Middelboe2, Sine Lo Svenningsen2
1Dalian SEM Bio-Engineering Technology Co. Ltd., Dalian, China
2Department of Biology, University of Copenhagen, Copenhagen, Denmark
3Shanghai Public Health Clinical Center, Fudan University, Shanghai, China
4Max Planck Institute for Terrestrial Microbiology, Marburg, Germany

Tóm tắt

Abstract Temperate ϕH20-like phages are repeatedly identified at geographically distinct areas as free phage particles or as prophages of the fish pathogen Vibrio anguillarum. We studied mutants of a lysogenic isolate of V. anguillarum locked in the quorum-sensing regulatory modes of low (ΔvanT) and high (ΔvanO) cell densities by in-frame deletion of key regulators of the quorum-sensing pathway. Remarkably, we find that induction of the H20-like prophage is controlled by the quorum-sensing state of the host, with an eightfold increase in phage particles per cell in high-cell-density cultures of the quorum-sensing-deficient ΔvanT mutant. Comparative studies with prophage-free strains show that biofilm formation is promoted at low cell density and that the H20-like prophage stimulates this behavior. In contrast, the high-cell-density state is associated with reduced prophage induction, increased proteolytic activity, and repression of biofilm. The proteolytic activity may dually function to disperse the biofilm and as a quorum-sensing-mediated antiphage strategy. We demonstrate an intertwined regulation of phage-host interactions and biofilm formation, which is orchestrated by host quorum-sensing signaling, suggesting that increased lysogeny at high cell density is not solely a strategy for phages to piggy-back the successful bacterial hosts but is also a host strategy evolved to take control of the lysis-lysogeny switch to promote host fitness.

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Tài liệu tham khảo

Brussaard, 2008, Global-scale processes with a nanoscale drive: the role of marine viruses, ISME J., 2, 575, 10.1038/ismej.2008.31

Melechen, 1980, Induction of lambdoid prophages by amino acid deprivation: differential inducibility; role of recA, Mol Gen Genet, 180, 147, 10.1007/BF00267364

Little, 1982, The SOS regulatory escherichia coli system of review, Cell., 29, 11, 10.1016/0092-8674(82)90085-X

Nanda, 2015, Impact of spontaneous prophage induction on the fitness of bacterial populations and host-microbe interactions, J Bacteriol., 197, 410, 10.1128/JB.02230-14

Ghosh, 2009, Acyl-homoserine lactones can induce virus production in lysogenic bacteria: an alternative paradigm for prophage induction, Appl Environ Microbiol, 75, 7142, 10.1128/AEM.00950-09

Ng, 2009, Bacterial quorum-sensing network architectures, Annu Rev Genet [Internet], 43, 197, 10.1146/annurev-genet-102108-134304

Papenfort, 2016, Quorum sensing signal–response systems in gram-negative bacteria, Nat Rev Microbiol [Internet], 14, 576, 10.1038/nrmicro.2016.89

Zhu, 1998, Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens, J Bacteriol, 180, 5398, 10.1128/JB.180.20.5398-5405.1998

Rumbaugh, 2012, Kin selection, quorum sensing and virulence in pathogenic bacteria, Proc R Soc B Biol Sci., 279, 3584, 10.1098/rspb.2012.0843

Herzog, 2019, Three autoinducer molecules act in concert to control virulence gene expression in Vibrio cholerae, Nucleic Acids Res, 47, 3171, 10.1093/nar/gky1320

Grundstad, 2019, Quorum sensing, virulence, and antibiotic resistance of USA100 methicillin-resistant staphylococcus aureus isolates, mSphere, 4, 1, 10.1128/mSphere.00553-19

Davies, 1998, The involvement of cell-to-cell signals in the development of a bacterial biofilm, Science, 280, 295, 10.1126/science.280.5361.295

Hammer, 2003, Quor sens controls biofilm formation, Vibrio cholera, 50, 101

Nadell, 2008, The evolution of quorum sensing in bacterial biofilms. Moran NA, editor, PLoS Biol, 6, e14, 10.1371/journal.pbio.0060014

Passos da Silva, 2017, An update on the sociomicrobiology of quorum sensing in gram-negative biofilm development, Pathogens., 6, 51, 10.3390/pathogens6040051

Høyland-Kroghsbo, 2013, A quorum-sensing-induced bacteriophage defense mechanism, MBio [Internet], 4, 1

Tan, 2015, Quorum sensing determines the choice of antiphage defense strategy in Vibrio anguillarum, MBio, 6, e00627, 10.1128/mBio.00627-15

Hoque, 2016, Quorum regulated resistance of vibrio cholerae against environmental bacteriophages, Sci Rep., 6, 37956, 10.1038/srep37956

Patterson, 2016, Quorum sensing controls adaptive immunity through the regulation of multiple CRISPR-Cas systems, Mol Cell, 64, 1102, 10.1016/j.molcel.2016.11.012

Høyland-Kroghsbo, 2017, Quorum sensing controls the Pseudomonas aeruginosa CRISPR-Cas adaptive immune system, Proc Natl Acad Sci, 114, 131, 10.1073/pnas.1617415113

Castillo, 2019, Phage defense mechanisms and their genomic and phenotypic implications in the fish pathogen Vibrio anguillarum, FEMS Microbiol Ecol, 95

Silpe, 2018, A host-produced quorum-sensing autoinducer controls a phage lysis-lysogeny decision, Cell, 1

Laganenka, 2019, Quorum sensing and metabolic state of the host control lysogeny-lysis switch of bacteriophage T1, MBio, 10, 3, 10.1128/mBio.01884-19

Erez, 2017, Communication between viruses guides lysis–lysogeny decisions, Nature, 541, 488, 10.1038/nature21049

Gallego del Sol, 2019, Deciphering the molecular mechanism underpinning phage arbitrium communication systems, Mol Cell., 74, 59, 10.1016/j.molcel.2019.01.025

Stokar-Avihail, 2019, Widespread utilization of peptide communication in phages infecting soil and pathogenic bacteria, Cell Host Microbe, 25, 746, 10.1016/j.chom.2019.03.017

Wigington, 2016, Re-examination of the relationship between marine virus and microbial cell abundances, Nat Microbiol, l

Knowles, 2016, Lytic to temperate switching of viral communities, Nature, 531, 466, 10.1038/nature17193

Weitz, 2017, Lysis, lysogeny and virus–microbe ratios, Nature, 549, E1, 10.1038/nature23295

Knowles, 2017, Knowles & Rohwer reply, Nature., 549, E3, 10.1038/nature23296

Coutinho, 2017, Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans, Nat Commun, 8, 1, 10.1038/ncomms15955

Alrasheed, 2019, Caution in inferring viral strategies from abundance correlations in marine metagenomes, Nat Commun, 10, 501, 10.1038/s41467-018-07950-z.

Coutinho, 2019, Reply to: Caution in inferring viral strategies from abundance correlations in marine metagenomes, Nat Commun, 10, 502, 10.1038/s41467-018-08286-4

Frans, 2011, Vibrio anguillarum as a fish pathogen: virulence factors, diagnosis and prevention, J Fish Dis, 34, 643, 10.1111/j.1365-2761.2011.01279.x

Hickey, 2017, A comprehensive review of Vibrio (Listonella) anguillarum: ecology, pathology and prevention, Rev Aquac, 1893, 1

Rodkhum, 2006, Putative virulence-related genes in Vibrio anguillarum identified by random genome sequencing, J Fish Dis, 29, 157, 10.1111/j.1365-2761.2006.00692.x

Naka, 2011, Genetic determinants of virulence in the marine fish pathogen vibrio anguillarum, Fish Pathol, 46, 1, 10.3147/jsfp.46.1

Castillo, 2017, Comparative genome analyses of Vibrio anguillarum strains reveal a link with pathogenicity traits, mSystems, 2, e00001, 10.1128/mSystems.00001-17

Kalatzis, 2017, Stumbling across the same phage: Comparative genomics of widespread temperate phages infecting the fish pathogen Vibrio anguillarum, Viruses., 9, 1, 10.3390/v9050122

Castillo, 2018, Widespread distribution of prophage-encoded virulence factors in marine Vibrio communities, Sci Rep, 8, 9973, 10.1038/s41598-018-28326-9

Milton, 2006, Quorum sensing in Vibrios: complexity for diversification, Int J Med Microbiol, 296, 61, 10.1016/j.ijmm.2006.01.044

Papenfort, 2015, Differential RNA-seq of Vibrio cholerae identifies the VqmR small RNA as a regulator of biofilm formation, Proc Natl Acad Sci USA, 112, E766, 10.1073/pnas.1500203112

Ng, 2011, Signal production and detection specificity in Vibrio CqsA/CqsS quorum-sensing systems, Mol Microbiol, 79, 1407, 10.1111/j.1365-2958.2011.07548.x

Castillo, 2019, Large phenotypic and genetic diversity of prophages induced from the fish pathogen Vibrio anguillarum, Viruses, 11, 983, 10.3390/v11110983

Croxatto, 2007, Vibrio anguillarum colonization of rainbow trout integument requires a DNA locus involved in exopolysaccharide transport and biosynthesis, Environ Microbiol, 9, 370, 10.1111/j.1462-2920.2006.01147.x

Zhu, 2003, Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae, Dev Cell., 5, 647, 10.1016/S1534-5807(03)00295-8

Milton, 1996, Flagellin A is essential for the virulence of Vibrio anguillarum, J Bacteriol, 178, 1310, 10.1128/jb.178.5.1310-1319.1996

Burmølle, 2003, Presence of N-acyl homoserine lactones in soil detected by a whole-cell biosensor and flow cytometry, Micro Ecol, 45, 226, 10.1007/s00248-002-2028-6

Tan, 2014, Vibriophages and their interactions with the fish pathogen Vibrio anguillarum, Appl Environ Microbiol, 80, 3128, 10.1128/AEM.03544-13

Ceri, 1999, The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms, J Clin Microbiol, 37, 1771, 10.1128/JCM.37.6.1771-1776.1999

Ren, 2014, High-throughput screening of multispecies biofilm formation and quantitative PCR-based assessment of individual species proportions, useful for exploring interspecific bacterial interactions, Micro Ecol, 68, 146, 10.1007/s00248-013-0315-z

Liu, 2017, Low-abundant species facilitates specific spatial organization that promotes multispecies biofilm formation, Environ Microbiol, 19, 2893, 10.1111/1462-2920.13816

RStudio Team., 2016, RStudio: integrated development environment for R

Luo, 2018, A sensitive thresholding method for confocal laser scanning microscope image stacks of microbial biofilms, Sci Rep., 8, 13013, 10.1038/s41598-018-31012-5

Røder, 2018, Enhanced bacterial mutualism through an evolved biofilm phenotype, ISME J, 12, 2608, 10.1038/s41396-018-0165-2

Knowles, 2017, Variability and host density independence in inductions-based estimates of environmental lysogeny, Nat Microbiol, 2, 17064, 10.1038/nmicrobiol.2017.64

Weitz, 2019, Viral invasion fitness across a continuum from lysis to latency†, Virus Evol, 5, 1, 10.1093/ve/vez006/5476198

Ball, 2017, Quorum sensing gene regulation by LuxR/HapR master regulators in Vibrios, J Bacteriol, 199, 1, 10.1128/JB.00105-17

Croxatto, 2004, A distinctive dual-channel quorum-sensing system operates in Vibrio anguillarum, Mol Microbiol, 52, 1677, 10.1111/j.1365-2958.2004.04083.x

Brum, 2016, Seasonal time bombs: dominant temperate viruses affect Southern ocean microbial dynamics, ISME J, 10, 437, 10.1038/ismej.2015.125

Igler, 2019, Commentary: A host-produced quorum-sensing autoinducer controls a phage lysis-lysogeny decision, Front Microbiol, 10, 1171, 10.3389/fmicb.2019.01171

Payet, 2013, To kill or not to kill: the balance between lytic and lysogenic viral infection is driven by trophic status, Limnol Oceanogr, 58, 465, 10.4319/lo.2013.58.2.0465

Thompson, 2004, Biodiveristy of Vibrios, Microbiol Mol Biol Rev, 68, 403, 10.1128/MMBR.68.3.403-431.2004

Kalatzis, 2018, Bacteriophage interactions with marine pathogenic Vibrios: implications for phage therapy, Antibiotics, 7, 15, 10.3390/antibiotics7010015

Obeng, 2016, The significance of mutualistic phages for bacterial ecology and evolution, Trends Microbiol, 24, 440, 10.1016/j.tim.2015.12.009.

Hansen, 2019, Big impact of the tiny: bacteriophage–bacteria interactions in biofilms, Trends Microbiol, 27, 739, 10.1016/j.tim.2019.04.006

Fillol-Salom, 2019, Bacteriophages benefit from generalized transduction, PLoS Pathog, 15, e1007888, 10.1371/journal.ppat.1007888

Argov, 2019, Coordination of cohabiting phage elements supports bacteria–phage cooperation, Nat Commun, 10, 5288, 10.1038/s41467-019-13296-x

Rice, 2009, The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage, ISME J., 3, 271, 10.1038/ismej.2008.109

Carrolo, 2010, Prophage spontaneous activation promotes DNA release enhancing biofilm formation in Streptococcus pneumoniae, PLoS ONE, 5, e15678, 10.1371/journal.pone.0015678

Gödeke, 2011, Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1, ISME J, 5, 613, 10.1038/ismej.2010.153

Croxatto, 2002, VanT, a homologue of Vibrio harveyi LuxR, regulates serine, metalloprotease, pigment, and biofilm production in Vibrio anguillarum, J Bacteriol, 184, 1617, 10.1128/jb.184.6.1617-1629.2002

Hentzer, 2003, Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections, J Clin Invest, 112, 1300, 10.1172/JCI20074

O’Loughlin, 2013, A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation, Proc Natl Acad Sci USA, 110, 17981, 10.1073/pnas.1316981110

Shelford, 2012, Virus-driven nitrogen cycling enhances phytoplankton growth, Aquat Micro Ecol, 66, 41, 10.3354/ame01553

Weitz, 2015, A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes, ISME J., 9, 1352, 10.1038/ismej.2014.220

Zimmerman, 2019, Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems, Nat Rev Microbiol, 18