life cycle of filamentous phage

Mature Pseudomonas aeruginosa biofilms undergo specific developmental events. [4] (See Russel et al. The Pf4 mutant biofilm is less stable than the WT. In vivo biopanning. This technology is a very promising instrument for several reasons. (2005). In order to collect the cells with the bound phage antibodies, fluorescently labeled antibodies specific to another antigen on the target cell surface are added to the suspension. Google Scholar. A serious advantage of immune libraries is the possibility to select high-affinity antibodies, which appear after viral infections or cancer, and antibodies specific to autoantigens, which are present in patients with autoimmune diseases. Microbiology 151: 15691576. Briefly, bacteria were grown for 17h in MINS medium (Nicas and Iglewski, 1984) at 37C with shaking, diluted 1:100 in MINS medium 3h before infection, concentrated by centrifugation and then re-suspended in phosphate-buffered saline. (1999). Top: Hostmediated (Xer, Zot domains are widely distributed throughout prokaryotic organisms including Gramnegative, Grampositive and Archaeal organisms. Before One mechanism by which phage may contribute to virulence, is through the provision of virulence determinants. In this study, we have generated a defined Pf4 chromosomal deletion mutant of the entire Pf4 prophage genome. Comprehensive research on the phage life cycle and its structure will lead us to the construction of miniature phage and to other methods that will enable an in vivo expanding of the . 2011 Sep 2;411(5):972-85. doi: 10.1016/j.jmb.2011.07.002. ISSN 1751-7362 (print), The persistence and stabilization of auxiliary genes in the human skin virome, Gut commensal Enterocloster species host inoviruses that are secreted in vitro and in vivo, Seasonal dynamics of a complex cheilostome bryozoan symbiosis: vertical transfer challenged, Genomic and Biological Characterization of Ralstonia solanacearum Inovirus Brazil 1, an Inovirus that Alters the Pathogenicity of the Phytopathogen Ralstonia pseudosolanacearum, Environmental pH is a key modulator of Staphylococcus aureus biofilm development under predation by the virulent phage phiIPLA-RODI. An official website of the United States government. The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage Mature Pseudomonas aeruginosa biofilms undergo specific developmental events. Below, we present several biopanning strategies. Here, we show for the first time that biofilms of the Pf4 phage-deficient mutant did not develop hollow centres or undergo cell death, typical of the differentiation process of wild-type (WT) P. aeruginosa PAO1 biofilms. Staffan Kjelleberg. Typhimurium. Acc Chem Res 49(6):11111120, Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D (2007) Colicin biology. Ff phages are chronic phage, releasing their progeny without killing the host cells. Filamentous phages: classification and applications in biotechnology, (A) Bacterial and Archaeal virus subfamilies, Figure 2. Clin Infect Dis 29: 621625. New York: Academic press; 1996. Horton RM, Cai Z, Ho SN, Pease LR . Google Scholar, Chung WJ, Oh JW, Kwak K, Lee BY, Meyer J, Wang E, Hexemer A, Lee SW (2011) Biomimetic self-templating supramolecular structures. PubMed Science 284(5419):15161519, Marks JD, Hoogenboom HR, Bonnert TP, McCafferty J, Griffiths AD, Winter G (1991) By-passing immunization. As a result of these effects on the host genome, bacteriophage can influence bacterial phenotypes. Microbiology 153: 18521859. Bockelmann U, Lunsdorf H, Szewzyk U . Unexpectedly, mice infected with the Pf4 mutant survived significantly longer than those infected with its isogenic WT strain, showing that Pf4 contributes to the virulence of P. aeruginosa. Direct antibody selection against cell surface markers can be performed using either a cell monolayer or a cell suspension. 2020 Jun 22;12(6):670. doi: 10.3390/v12060670. After that a phage usually follows one of two life cycles, lytic (virulent) or lysogenic (temperate). Nature 406: 959964. For example, it has recently been shown that filamentous phage can be isolated from biofilms of P. aeruginosa during the dispersal phase of the biofilm life cycle and that the appearance of the phage correlated with the appearance of small colony variants (SCVs) (Webb et al., 2003, 2004). The basic structure of filamentous phage and its use in the display of Front Microbiol 6:316. https://doi.org/10.3389/fmicb.2015.00316, Sblattero D, Bradbury A (2000) Exploiting recombination in single bacteria to make large phage antibody libraries. (2002). (2007) observed no correlation between the production of the Pf5 filamentous phage and SCV formation in P. aeruginosa PA14 (Mooij et al., 2007). Moreover, the data suggest that microcolony expansion in the WT requires the presence of the phage for the microcolonies to expand beyond 50m in diameter. (1984). Bacteriophages (article) | Viruses | Khan Academy In contrast, no SCVs were detected in the effluent of the Pf4 mutant at the time when the phage converted into the superinfective form. The bacterial strains and plasmids used in this study are listed in Table 1. A broad-host-range flp-frt recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Both clinical and environmental isolates of P. aeruginosa show mutator phenotypes (Kenna et al., 2007). This is one of the main reasons why smaller libraries containing a narrowed repertoire of antibodies are preferable. Front Microbiol 5:734. https://doi.org/10.3389/fmicb.2014.00734, CrossRef Article It has been suggested that Zot has an additional function, where the C-terminal region harbours the toxin activity and the N-terminal domain plays an essential role in phage assembly (Di Pierro et al., 2001). These effects may be mediated by multiple mechanisms, where the prophage encodes potential virulence factors, phage may contribute to microbial evolution through the formation of phenotypic variants, for example SCVs, and phage particles may physically enhance the stability of biofilms. (Moller et al., 1998) with some modifications. Primers Pre-Pfk-F and Pre-Pfk-R bind to positions 784716784735 and 798259798240 (Table 2), which lie outside of the Pf4 genomic region and are not expected to generate a product from either a WT or a single-crossover, but would generate a 2.2kb product in a double-crossover mutant (also see Figure 1). 8600 Rockville Pike The persistence and stabilization of auxiliary genes in the human skin virome. Unauthorized use of these marks is strictly prohibited. Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. This study shows that at the time when cell death occurs in biofilms of the WT, the Pf4 phage converts into a superinfective form, which correlates with the appearance of variants in the dispersal population. DNA sequence of the filamentous bacteriophage Pf1. Chikova AK, Schaaper RM . J Bacteriol 135(3):883887, CAS and transmitted securely. J Bacteriol 107(3):918925, Ou JT (1973) Inhibition of formation of Escherichia coli mating pairs by f1 and MS2 bacteriophages as determined with a coulter counter. Careers. To assess the stability of WT and P. aeruginosa PAO1 and the PAO1Pf4 mutant biofilms to SDS treatment, 4-day-old biofilms were fed with M9 medium containing 0.01% SDS for 2h. Confocal scanning laser microscopy images were acquired before and after the SDS treatment. Mucoid conversion by phages of Pseudomonas aeruginosa strains from patients with cystic fibrosis. Biofilms of P. aeruginosa PAO1 WT, a quorum sensing mutant and the Pf4 mutant were formed in flow cells for 4 days in M9 minimal medium, at which time, they were treated with 0.01% SDS (in M9 medium) under flow conditions for 2h at room temperature. Engineered Phage-Based Cancer Vaccines: Current Advances and Future Directions. biotechniques 8: 528535. Lastly, primers RF-F and RF-R (Table 2) were designed to specifically amplify an 839bp region of the extra chromosomal RF of the Pf4 filamentous phage. Biochemistry (Moscow) V 70: 267274. per ml for each sample were calculated. Bacteriophage | Definition, Life Cycle, & Research | Britannica Self-generated diversity produces Insurance effects in biofilm communities. Similar approaches can be used for identifying tumor-specific antigens and also as a highly productive protocol for selecting antibody fragments specific to conformation-dependent cell surface markers. Appl Environ Microbiol 64: 721732. Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand, Jasna Rakonjac,Sofia Khanum,Sam J. Brooke&Marina Raji, Maurice Wilkins Centre for Molecular Biodiscovery, University of Auckland, Auckland, New Zealand, The Rockefeller University, New York, NY, USA, You can also search for this author in (2006). Life cycle of filamentous phages. CAS Life cycles of bacteriophages During infection a phage attaches to a bacterium and inserts its genetic material into the cell. ml1) for 24h. Viability of the phage treated biofilms along with the negative controls was determined by LIVE/DEAD staining. Nevertheless, despite the existing methodological problems, phage display techniques are showing considerable progress. R. Liss, Inc, New York, pp 413428, Griffiths AD, Malmqvist M, Marks JD, Bye JM, Embleton MJ, McCafferty J, Baier M, Holliger KP, Gorick BD, Hughes-Jones NC et al (1993) Human anti-self antibodies with high specificity from phage display libraries. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Very clearly, biofilms of the Pf4 mutant develop abnormally compared with the WT, where it fails to undergo the process of autolysis and makes smaller microcolonies. A similar approach was used for peptide libraries [88]. Infect Immun 67: 36253630. J Bacteriol 182(6):17391747, Heilpern AJ, Waldor MK (2003) pIIICTX, a predicted CTX minor coat protein, can expand the host range of coliphage fd to include Vibrio cholerae. Cryo-electron microscopy of the f1 filamentous phage reveals insights into viral infection and assembly. Present address: 7Current address: School of Biological Sciences, University of Southampton, Southampton SO16 7PX, UK, The School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, New South Wales, Australia, Scott A Rice,Chuan Hao Tan,Per Jensen Mikkelsen,Jerry Woo,Martin Tay,Diane McDougald,Jeremy S Webb&Staffan Kjelleberg, The Centre for Marine Bio-Innovation, The University of New South Wales, Sydney, New South Wales, Australia, Department of Microbiology/Immunology, Northwestern University, Chicago, IL, USA, Department of Medicine, Northwestern University, Chicago, IL, USA, You can also search for this author in Prog Biophys Mol Biol. (1984). Like the mucoid variants, other variants, such as the SCVs are clinically relevant as they commonly show increased antibiotic resistance and biofilm formation (Haussler, 2004). II. Please enable it to take advantage of the complete set of features! Nature 540:597601, Yan Z, Yin M, Xu D, Zhu Y, Li X (2017) Structural insights into the secretin translocation channel in the type II secretion system. Phage display methodology and its success are defined by the features of filamentous phages. (a) The genomic organization of the Pf4 prophage in P. aeruginosa PAO1 is shown. Nat Rev Drug Discov 2: 114122. The flow cell was sterilized in 10% (v/v) bleach for 4h, thoroughly rinsed in sterile milliQ water and connected to sterile silicon tubing (Silastic laboratory tubings). Nat Struct Mol Biol 24(2):177183, Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. In recent years, more than 14 antibodies on the U.S. pharmaceutical market have been obtained using phage display methods [15]. Epub 2017 Jun 22. Google Scholar, Chamberlain BK, Webster RE (1978) Effect of membrane-associated f1 bacteriophage coat protein upon the activity of Escherichia coli phosphatidylserine synthetase. Molecules 16(4):30893105, Bennett NJ, Gagic D, Sutherland-Smith AJ, Rakonjac J (2011) Characterization of a dual-function domain that mediates membrane insertion and excision of Ff filamentous bacteriophage. Proteins from the UniRef90 database (representing 2,205 UniProt. ISME J 3, 271282 (2009). Both are ~6 nm in diam-eter, with the Ff phage virion approximately 1 lm long and the Pf1 virion approximately 2 lm long. However, zot mutants of V. cholerae were not affected in a pulmonary infection model and Zot was shown to disrupt tight junctions in the small intestine, but not in the colon (Di Pierro et al., 2001; Fullner et al., 2002). Phage particles were concentrated by the addition of an equal volume of phage precipitation buffer (2M NaCl, 4% polyethylene glycerol (m.w. Electroporation was performed using a GenePulserXcell electroporator (Bio-Rad, Hercules, CA, USA) at 25F, 200Ohm and 2.5kV. In terms of mean survival times, mice infected with WT bacteria survived 42.7h (95% confidence interval: 32.9h to 52.4h), whereas mice infected with the Pf4 mutant survived 100.8h (95% confidence interval: 74.0h to 127.6h), indicating that the Pf4 mutant was attenuated in its ability to cause acute pneumonia (P<0.001, log-rank test). Introduction Bacteriophages have been crucial to the development of molecular biology, serving as model systems for elucidating the central molecular mechanisms of living systems: DNA replication, transcription and translation. The next important step after constructing a library or choosing an available one is the enrichment of the original antibody repertoire with the antibodies specific to a target antigen (Fig.5). Gene 185(1):2733, Matochko WL, Derda R (2013) Error analysis of deep sequencing of phage libraries: peptides censored in sequencing. Proc Natl Acad Sci U S A 99(20):1261212616, Gerding MA, Ogata Y, Pecora ND, Niki H, de Boer PA (2007) The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Methods of filamentous phage host chromosome integration and excision, Figure 6. Nat Commun 7:13858, Cao BR, Yang MY, Mao CB (2016) Phage as a genetically modifiable supramacromolecule in chemistry, materials and medicine. Sequence analysis identified the expected flanking sequences disrupted by the gentamicin cassette (data not shown) and no vector sequences were detected, indicating that the clone was a true Pf4 deletion mutant. (1951). This suggests that superinfection may be a key process in the formation of SCVs by phage activity. See this image and copyright information in PMC. The cells are then collected by a FACS-sorter. J Mol Biol 356(2):266273, Bernard JM, Francis MB (2014) Chemical strategies for the covalent modification of filamentous phage. J Bacteriol 114(3):11081115, Pacheco-Gomez R, Kraemer J, Stokoe S, England HJ, Penn CW, Stanley E, Rodger A, Ward J, Hicks MR, Dafforn TR (2012) Detection of pathogenic bacteria using a homogeneous immunoassay based on shear alignment of virus particles and linear dichroism. Some phages can only reproduce via a lytic lifecycle, in which they burst and kill their host cells. Biofilm formation contributes to infection by protecting the bacteria from the host immune defence as well as mediating antibiotic resistance. FEBS Lett 480(23):231234, Fulford W, Model P (1988) Bacteriophage f1 DNA replication genes. New insights into intestinal phages | Mucosal Immunology Nature 472(7344):499503, Feng JN, Russel M, Model P (1997) A permeabilized cell system that assembles filamentous bacteriophage. Nature 413: 860864. Filamentous phage binds to the F pilus of a host E. coli cell through pIII. Ff discovery through gene signatures in prokaryote (host) chromosomes, MeSH The LasR/RhlR strain was included here as a positive control as it was shown earlier that QS-deficient mutants were sensitive to SDS treatment (Allesen-Holm et al., 2006). Six millilitres of an overnight culture grown in LB medium was harvested in four 2ml tubes by centrifugation at 16000g for 2min at room temperature and washed twice with 1ml of 300mM sucrose. Proc Natl Acad Sci U S A 87(3):862866, Brodel AK, Jaramillo A, Isalan M (2016) Engineering orthogonal dual transcription factors for multi-input synthetic promoters. Mutagenic Analysis of a DNA Translocating Tube's Interior Surface. Credit: what-when-how Filamentous phage replication, like that of other bacteriophages, occurs in the cytoplasm of the host bacteria. Note that the latter two primers also incorporate att sites at the ends of the PCR fragment. Biofilm formation by the small colony variant phenotype of Pseudomonas aeruginosa. Bookshelf Virology 122(1):222226, Esvelt KM, Carlson JC, Liu DR (2011) A system for the continuous directed evolution of biomolecules. HHS Vulnerability Disclosure, Help For example, it has been suggested that phage are the major cause of bacterial death in the environment and thus, bacteriophage are thought to have a significant impact on nutrient cycling due to bacterial lysis (Wilhelm and Suttle, 1999). Bioinformatics 22(2):195201, CrossRef It is known that phage can carry foreign genes that may expand the host's phenotypic capacity. Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. Bacterial biofilms: A common cause of persistent infections. Messenger populations in the infected cell. 2023 Apr 29;11(5):919. doi: 10.3390/vaccines11050919. The Pf4 mutant was as sensitive to SDS as a quorum sensing lasR-rhlR mutant. Thus the prophage must either confer a selective advantage on the host or it risks accumulating mutations that render it defective. This suggests that phage generally may play a significant role in biofilm development and the generation of phenotypic variants in clinically relevant strains. Anyone you share the following link with will be able to read this content: Sorry, a shareable link is not currently available for this article. After incubating the antibodies with an antigen conjugated with biotin, phages bound to the tagged antigen are collected with avidin- or streptavidin-covered paramagnetic beads. Due to the excellent understanding of infection and assembly requirements, Ff phage have also been at the core of phage-assisted continual protein evolution strategies (PACE). Re-infection of the Pf4 mutant biofilm with purified, superinfective phage restored biofilm killing (data not shown), showing that the lack of cell death in the Pf4 mutant biofilm is not due to resistance to Pf4 infection but rather can be ascribed to the absence of Pf4 activity in the mutant. Present address: 5Current address: Expression Engineering Group, Bioprocessing Technology Institute, 20 Biopolis Way, No. Such an approach was used for selecting a scFv phage library for antibodies specific to antigens from a yeast library [90]. Bacteriophage ("bacteria eaters") or phage is the collective term for viruses that infect bacteria. J Clin Microbiol 19: 717719. PubMed Central (1998). Selective pressures are also likely to operate on lysogenic phage, which integrate themselves into the host genome. J Mol Biol 231(3):689697, Russel M, Kidd S, Kelley MR (1986) An improved filamentous helper phage for generating single-stranded plasmid DNA. Persister cells and the riddle of biofilm survival. 2015 Jul;39(4):465-87. doi: 10.1093/femsre/fuu007. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Small colony variants (SCVs) were detectable in the dispersal population of the WT biofilm at the time of dispersal and cell death, whereas no SCVs were detected in the effluent of the Pf4 mutant biofilm. Simulation of the M13 life cycle I: Assembly of a genetically Keywords: Science 306(5698):10401042, Marlovits TC, Stebbins CE (2010) Type III secretion systems shape up as they ship out. In situ gene expression in mixed-culture biofilmsevidence of metabolic interactions between community members. J Mol Biol 250(4):496506, Enea V, Horiuchi K, Turgeon BG, Zinder ND (1977) Physical map of defective interfering particles of bacteriophage f1. It has been assumed that the role of the C-terminal domain of pIII in the infection is that of a tether for the receptor-binding domains N1N2 to the main body of the virion. Filamentous bacteriophage - Wikipedia Immune libraries have two main features: they are enriched with antigen-specific antibodies, and the affinity of some of the antibodies has increased during the immune response. Interactions between bacterial and phage communities in natural As a further control, the P. aeruginosa lasR/rhlR quorum sensing deficient double mutant (Beatson et al., 2002), earlier shown to be less stable during SDS treatment than the WT (Davies et al., 1998; Hentzer et al., 2003; Allesen-Holm et al., 2006), was also included. Indeed, we have shown that biofilms of the Pf4 mutant were less stable than the WT when challenged with surfactant stress (Figure 4). Front Microbiol 5:650. https://doi.org/10.3389/fmicb.2014.00650, Davis NG, Boeke JD, Model P (1985) Fine structure of a membrane anchor domain. Google Scholar, Chasteen L, Ayriss J, Pavlik P, Bradbury AR (2006) Eliminating helper phage from phage display. San Diego, Elsevier Academic Press: 375-384, Day LA, Marzec CJ, Reisberg SA, Casadevall A (1988) DNA packing in filamentous bacteriophages. Microbiology 152: 25052514. One key difference between the Pf5 and Pf4 bacteriophage is that the former does not appear to contain a toxinantitoxin gene pair; it has been proposed that such addiction molecules are involved in the formation of persister cells (Lewis, 2005) and we have observed that overexpression of the parE gene (putative toxin) from a plasmid introduced into P. aeruginosa leads to an increased formation of SCVs (Lau and Kjelleberg, unpublished data). Filamentous Phage: Structure and Biology | Request PDF Boles BR, Thoendel M, Singh PK . Antibodies obtained via in vivo biopanning or cell biopanning can be very useful for the functional analysis of newly discovered receptors and in the search for potential targets of novel drugs. J Mol Biol. Identification of the fragment biologically active on tight junctions and of the zonulin receptor binding domain. The medium flow was resumed at a flow rate of 6mlh1. Dominance of Ff over other bacteriophage in display technology stems from the titres that are about 100-fold higher than any other known phage, efficacious transformation ensuring large library size and superior stability of the virion at high temperatures, detergents and pH extremes, allowing broad range of biopanning conditions in screening phage display libraries. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. PubMed Altmetric, Part of the Advances in Experimental Medicine and Biology book series (AEMB,volume 1053). FEMS Microbiol Rev 39(4):465487, Maier B (2005) Using laser tweezers to measure twitching motility in Neisseria.

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