1,163
Views
6
CrossRef citations to date
0
Altmetric
Review Articles

Potential of bacteriophage proteins as recognition molecules for pathogen detection

, , , &
Pages 787-804 | Received 19 Nov 2021, Accepted 04 Apr 2022, Published online: 18 Jul 2022

References

  • Centers for Disease Control and Prevention. Surveillance for foodborne disease outbreaks, United States, 2017. Annual report. Atlanta (GA): Centers for Disease Control and Prevention; 2019.
  • WHO. Report on the burden of endemic health care-associated infection worldwide. Geneva, Switzerland: World Health Organization; 2011.
  • Mehlhorn H. WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007–2015. Geneva, Switzerland: World Health Organization; 2015.
  • Centers for Disease Control and Prevention. 2018. National and state healthcare-associated infections progress report; 2019. Atlanta, Georgia, USA.
  • Renner LD, Zan J, Hu LI, et al. Detection of ESKAPE bacterial pathogens at the point of care using isothermal DNA-based assays in a portable degas-actuated microfluidic diagnostic assay platform. Appl Environ Microbiol. 2017;83(4):e02449–16.
  • Rees CED, Dodd CER. Phage for rapid detection and control of bacterial pathogens in food. Adv Appl Microbiol. 2006;59:159–186.
  • Opota O, Croxatto A, Prod'hom G, et al. Blood culture-based diagnosis of bacteraemia: state of the art. Clin Microbiol Infect. 2015;21(4):313–322.
  • Feucherolles M, Cauchie HM, Penny C. MALDI-TOF mass spectrometry and specific biomarkers: potential new key for swift identification of antimicrobial resistance in foodborne pathogens. Microorganisms. 2019;7(12):593.
  • Ferreira L, Sánchez-Juanes F, Porras-Guerra I, et al. Microorganisms direct identification from blood culture by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Clin Microbiol Infect. 2011;17(4):546–551.
  • Quainoo S, Coolen JPM, van Hijum SAFT, et al. Whole-genome sequencing of bacterial pathogens: the future of nosocomial outbreak analysis. Clin Microbiol Rev. 2017;30(4):1015–1063.
  • Langley G, Besser J, Iwamoto M, et al. Effect of culture-independent diagnostic tests on future emerging infections program surveillance. Emerg Infect Dis. 2015;21(9):1582–1588.
  • Verma J, Saxena S, Babu SG. ELISA-based identification and detection of microbes. In: Analyzing microbes. Heidelberg, Germany: Springer Protocols; 2013. p. 169–186.
  • Schmelcher M, Loessner MJ. Application of bacteriophages for detection of foodborne pathogens. Bacteriophage. 2014;4(1):e28137.
  • Marder EP, Cieslak PR, Cronquist AB, et al. Incidence and trends of infections with pathogens transmitted commonly through food and the effect of increasing use of culture-Independent diagnostic tests on surveillance – Foodborne Diseases Active Surveillance Network, 10 U.S. sites, 2013–2016. MMWR Morb Mortal Wkly Rep. 2017;66(15):397–403.
  • Stevens KA, Jaykus LA. Bacterial separation and concentration from complex sample matrices: a review. Crit Rev Microbiol. 2004;30(1):7–24.
  • Opota O, Jaton K, Greub G. Microbial diagnosis of bloodstream infection: towards molecular diagnosis directly from blood. Clin Microbiol Infect. 2015;21(4):323–331.
  • Singh A, Poshtiban S, Evoy S. Recent advances in bacteriophage based biosensors for food-borne pathogen detection. Sensors. 2013;13(2):1763–1786.
  • Fratamico PM, Bayles DO. Molecular approaches for detection, identification, and analysis of foodborne pathogens. In: Foodborne pathogens: microbiology and molecular biology. Caister Academic Press; 2005.
  • Hudson JA, Lake RJ, Savill MG, et al. Rapid detection of Listeria monocytogenes in ham samples using immunomagnetic separation followed by polymerase chain reaction. J Appl Microbiol. 2001;90(4):614–621.
  • Fluit AC, Torensma R, Visser MJC, et al. Detection of Listeria monocytogenes in cheese with the magnetic immuno-polymerase chain reaction assay. Appl Environ Microbiol. 1993;59(5):1289–1293.
  • Uyttendaele M, Van Hoorde I, Debevere J. The use of immuno-magnetic separation (IMS) as a tool in a sample preparation method for direct detection of L. monocytogenes in cheese. Int J Food Microbiol. 2000;54(3):205–212.
  • Kaclíková E, Kuchta TV, Kay H, et al. Separation of listeria from cheese and enrichment media using antibody-coated microbeads and centrifugation. J Microbiol Methods. 2001;46(1):63–67.
  • El-Rafie MH, Ahmed HB, Zahran MK. Characterization of nanosilver coated cotton fabrics and evaluation of its antibacterial efficacy. Carbohydr Polym. 2014;107(1):174–181.
  • Singh A, Arutyunov D, Szymanski CM, et al. Bacteriophage based probes for pathogen detection. Analyst. 2012;137(15):3405–3421.
  • Hagens S, Loessner MJ. Application of bacteriophages for detection and control of foodborne pathogens. Appl Microbiol Biotechnol. 2007;76(3):513–519.
  • Garrido-Maestu A, Fuciños P, Azinheiro S, et al. Specific detection of viable Salmonella enteritidis by phage amplification combined with qPCR (PAA-qPCR) in spiked chicken meat samples. Food Control. 2019;99:79–83.
  • Li S, Li Y, Chen H, et al. Direct detection of Salmonella typhimurium on fresh produce using phage-based magnetoelastic biosensors. Biosens Bioelectron. 2010;26(4):1313–1319.
  • Arya SK, Singh A, Naidoo R, et al. Chemically immobilized T4-bacteriophage for specific Escherichia coli detection using surface plasmon resonance. Analyst. 2011;136(3):486–492.
  • Fernandes E, Martins VC, Nóbrega C, et al. A bacteriophage detection tool for viability assessment of Salmonella cells. Biosens Bioelectron. 2014;52:239–246.
  • Lindberg AA, Wollin R, Gemski P, et al. Interaction between bacteriophage Sf6 and shigella flexner. J Virol. 1978;27(1):38–44.
  • Singh A, Arya SK, Glass N, et al. Bacteriophage tailspike proteins as molecular probes for sensitive and selective bacterial detection. Biosens Bioelectron. 2010;26(1):131–138.
  • Bennett AR, Davids FGC, Vlahodimou S, et al. The use of bacteriophage-based systems for the separation and concentration of Salmonella. J Appl Microbiol. 1997;83(2):259–265.
  • Chibli H, Ghali H, Park S, et al. Immobilized phage proteins for specific detection of staphylococci. Analyst. 2014;139(1):179–186.
  • Boratyński J, Syper D, Weber-Da̧browska B, et al. Preparation of endotoxin-free bacteriophages. Cell Mol Biol Lett. 2004;9(2):253–259.
  • Kretzer JW, Lehmann R, Schmelcher M, et al. Use of high-affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Appl Environ Microbiol. 2007;73(6):1992–2000.
  • Walcher G, Stessl B, Wagner M, et al. Evaluation of paramagnetic beads coated with recombinant listeria phage endolysin-derived cell-wall-binding domain proteins for separation of Listeria monocytogenes from raw milk in combination with culture-based and real-time polymerase chain reaction-based quantification. Foodborne Pathog Dis. 2010;7(9):1019–1024.
  • Yu J, Zhang Y, Zhang Y, et al. Sensitive and rapid detection of staphylococcus aureus in milk via cell binding domain of lysin. Biosens Bioelectron. 2016;77:366–371.
  • Singh A, Arutyunov D, McDermott MT, et al. Specific detection of Campylobacter jejuni using the bacteriophage NCTC 12673 receptor binding protein as a probe. Analyst. 2011;136(22):4780–4786.
  • Schmidt A, Rabsch W, Broeker NK, et al. Bacteriophage tailspike protein based assay to monitor phase variable glucosylations in Salmonella O-antigens. BMC Microbiol. 2016;16(1):1–11.
  • Waseh S, Hanifi-Moghaddam P, Coleman R, et al. Orally administered P22 phage tailspike protein reduces salmonella colonization in chickens: prospects of a novel therapy against bacterial infections. PLOS One. 2010;5(11):e13904.
  • Barbirz S, Becker M, Freiberg A, et al. Phage tailspike proteins with beta-solenoid fold as thermostable carbohydrate binding materials. Macromol Biosci. 2009;9(2):169–173.
  • Simpson DJ, Sacher JC, Szymanski CM. Exploring the interactions between bacteriophage-encoded glycan binding proteins and carbohydrates. Curr Opin Struct Biol. 2015;34:69–77.
  • Simpson DJ, Sacher JC, Szymanski CM. Development of an assay for the identification of receptor binding proteins from bacteriophages. Viruses. 2016;8(1):17.
  • Braun P, Wolfschläger I, Reetz L, et al. Rapid microscopic detection of bacillus anthracis by fluorescent receptor binding proteins of bacteriophages. Microorganisms. 2020;8(6):934–921.
  • Fujinami Y, Hirai Y, Sakai I, et al. Sensitive detection of Bacillus anthracis using a binding protein originating from gamma-phage. Microbiol Immunol. 2007;51(2):163–169.
  • Kong M, Na H, Ha N-C, et al. LysPBC2, a novel endolysin harboring a Bacillus cereus spore binding domain. Appl Envir Microbiol. 2019;85(5):e02462-18.
  • Poshtiban S, Javed MA, Arutyunov D, et al. Phage receptor binding protein-based magnetic enrichment method as an aid for real time PCR detection of foodborne bacteria. Analyst. 2013;138(19):5619–5626.
  • Bai YL, Shahed-Al-Mahmud M, Selvaprakash K, et al. Tail fiber protein-immobilized magnetic nanoparticle-based affinity approaches for detection of Acinetobacter baumannii. Anal Chem. 2019;91(15):10335–10342.
  • Brzozowska E, Śmietana M, Koba M, et al. Recognition of bacterial lipopolysaccharide using bacteriophage-adhesin-coated long-period gratings. Biosens Bioelectron. 2015;67:93–99.
  • Rydosz A, Brzozowska E, Górska S, et al. A broadband capacitive sensing method for label-free bacterial LPS detection. Biosens Bioelectron. 2016;75:328–336.
  • Brzozowska E, Koba M, Śmietana M, et al. Label-free gram-negative bacteria detection using bacteriophage-adhesin-coated long-period gratings. Biomed Opt Express. 2016;7(3):829–840.
  • Wang Z, Wang J, Yue T, et al. Immunomagnetic separation combined with polymerase chain reaction for the detection of Alicyclobacillus acidoterrestris in apple juice. PLOS One. 2013;8(12):e82376.
  • Yang H, Qu L, Wimbrow AN, et al. Rapid detection of Listeria monocytogenes by nanoparticle-based immunomagnetic separation and real-time PCR. Int J Food Microbiol. 2007;118(2):132–138.
  • Jung YS, Frank JF, Brackett RE. Evaluation of antibodies for immunomagnetic separation combined with flow cytometry detection of Listeria monocytogenes. J Food Prot. 2003;66(7):1283–1287.
  • Duckworth D. History and basic properties of bacterial viruses. In: Goyal SM, Gerba CP, Bitton G, editors, Phage Ecology. New York: John Wiley & Sons; 1987. p.1–44.
  • Leiman PG, Kanamaru S, Mesyanzhinov VV, et al. Structure and morphogenesis of bacteriophage T4. Cell Mol Life Sci. 2003;60(11):2356–2370.
  • Rakhuba DV, Kolomiets EI, Dey ES, et al. Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol. 2010;59(3):145–155.
  • Dowah ASA, Clokie MRJ. Review of the nature, diversity and structure of bacteriophage receptor binding proteins that target gram-positive bacteria. Biophys Rev. 2018;10(2):535–542.
  • Harada LK, Silva EC, Campos WF, et al. Biotechnological applications of bacteriophages: State of the art. Microbiol Res. 2018;212–213(April):38–58.
  • Vinga I, Baptista C, Auzat I, et al. Role of bacteriophage SPP1 tail spike protein gp21 on host cell receptor binding and trigger of phage DNA ejection. Mol Microbiol. 2012;83(2):289–303.
  • Baptista C, Santos MA, São-José C. Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J Bacteriol. 2008;190(14):4989–4996.
  • Bartual SG, Otero JM, Garcia-doval C, et al. Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc Natl Acad Sci USA. 2010;107(47):20287–20292.
  • Bertozzi Silva J, Storms Z, Sauvageau D. Host receptors for bacteriophage adsorption. FEMS Microbiol Lett. 2016;363(4):1–11.
  • Drulis-Kawa Z, Majkowska-Skrobek G, Maciejewska B. Bacteriophages and phage-derived proteins-application approaches. Curr Med Chem. 2015;22(14):1757–1773.
  • Santos SB, Cunha AP, Macedo M, et al. Bacteriophage-receptor binding proteins for multiplex detection of Staphylococcus and Enterococcus in blood. Biotechnol Bioeng. 2020;117(11):3286–3298.
  • Nogueira CL, Pires DP, Monteiro R, et al. Exploitation of a Klebsiella bacteriophage receptor-binding protein as a superior biorecognition molecule. ACS Infect Dis. 2021;7(11):3077–3087.
  • Li X, Koç C, Kühner P, et al. An essential role for the baseplate protein Gp45 in phage adsorption to Staphylococcus aureus. Sci Rep. 2016;6(May):26455–26411.
  • Dupont K, Vogensen FK, Neve H, et al. Identification of the receptor-binding protein in 936-species lactococcal bacteriophages. Appl Environ Microbiol. 2004;70(10):5818–5824.
  • Uchiyama J, Takemura I, Satoh M, et al. Improved adsorption of an Enterococcus faecalis bacteriophage ΦEF24C with a spontaneous point mutation. PLOS One. 2011;6(10):e26648.
  • Bielmann R, Habann M, Eugster MR, et al. Receptor binding proteins of Listeria monocytogenes bacteriophages A118 and P35 recognize serovar-specific teichoic acids. Virology. 2015;477:110–118.
  • Koç C, Xia G, Kühner P, et al. Structure of the host-recognition device of Staphylococcus aureus phage φ 11. Sci Rep. 2016;6(1):1–11.
  • Scholl D, Rogers S, Adhya S, et al. Bacteriophage K1-5 encodes two different tail fiber proteins, allowing it to infect and replicate on both K1 and K5 strains of Escherichia coli. J Virol. 2001;75(6):2509–2515.
  • Leiman PG, Shneider MM, Mesyanzhinov VV, et al. Evolution of bacteriophage tails: structure of T4 gene product 10. J Mol Biol. 2006;358(3):912–921.
  • Chatterjee S, Rothenberg E. Interaction of bacteriophage with its E. coli receptor, LamB. Viruses. 2012;4(11):3162–3178.
  • Walter M, Fiedler C, Grassl R, et al. Structure of the receptor-binding protein of bacteriophage Det7: a podoviral tail spike in a myovirus. J Virol. 2008;82(5):2265–2273.
  • Taylor NMI, Prokhorov NS, Guerrero-Ferreira RC, et al. Structure of the T4 baseplate and its function in triggering sheath contraction. Nature. 2016;533(7603):346–352.
  • Andres D, Roske Y, Doering C, et al. Tail morphology controls DNA release in two Salmonella phages with one lipopolysaccharide receptor recognition system. Mol Microbiol. 2012;83(6):1244–1253.
  • Marti R, Zurfluh K, Hagens S, et al. Long tail fibres of the novel broad-host-range T-even bacteriophage S16 specifically recognize Salmonella OmpC. Mol Microbiol. 2013;87(4):818–834.
  • Stuer-Lauridsen B, Janzen T, Schnabl J, et al. Identification of the host determinant of two prolate-headed phages infecting Lactococcus lactis. Virology. 2003;309(1):10–17.
  • Duplessis M, Moineau S. Identification of a genetic determinant responsible for host specificity in Streptococcus thermophilus bacteriophages. Mol Microbiol. 2001;41(2):325–336.
  • Veesler D, Cambillau C. A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries. Microbiol Mol Biol Rev. 2011;75(3):423–433.
  • Hendrix RW, Hatfull GF, Ford ME, et al. Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci. 1999;96:2192–2197.
  • Barbirz S, Müller JJ, Uetrecht C, et al. Crystal structure of Escherichia coli phage HK620 tailspike: podoviral tailspike endoglycosidase modules are evolutionarily related. Mol Microbiol. 2008;69(2):303–316.
  • Javed MA, Poshtiban S, Arutyunov D, et al. Bacteriophage receptor binding protein based assays for the simultaneous detection of Campylobacter jejuni and Campylobacter coli. PLOS One. 2013;8(7):e69770.
  • Le S, He X, Tan Y, et al. Mapping the tail fiber as the receptor binding protein responsible for differential host specificity of Pseudomonas aeruginosa bacteriophages PaP1 and JG004. PLOS One. 2013;8(7):e68562.
  • Xiang Y, Leiman PG, Li L, et al. Crystallographic insights into the autocatalytic assembly mechanism of a bacteriophage tail spike. Mol Cell. 2009;34(3):375–386.
  • Baxa U, Steinbacher S, Miller S, et al. Interactions of phage P22 tails with their cellular receptor, Salmonella O-antigen polysaccharide. Biophys J. 1996;71(4):2040–2048.
  • Steinbacher S, Baxa U, Miller S, et al. Crystal structure of phage P22 tailspike protein complexed with Salmonella sp. O-antigen receptors. Proc Natl Acad Sci USA. 1996;93(20):10584–10588.
  • Latka A, Leiman PG, Drulis-Kawa Z, et al. Modeling the architecture of depolymerase-containing receptor binding proteins in Klebsiella phages. Front Microbiol. 2019;10:2649.
  • Knecht LE, Veljkovic M, Fieseler L. Diversity and function of phage encoded depolymerases. Front Microbiol. 2020;10:1–16.
  • Pan Y-J, Lin T-L, Chen C-C, et al. Klebsiella phage ΦK64-1 encodes multiple depolymerases for multiple host capsular types. J Virol. 2017;91(6):e02457–16.
  • Majkowska-Skrobek G, Latka A, Berisio R, et al. Phage-borne depolymerases decrease Klebsiella pneumoniae resistance to innate defense mechanisms. Front Microbiol. 2018;9:2517.
  • Hsieh P-F, Lin H-H, Lin T-L, et al. Two T7-like bacteriophages, K5-2 and K5-4, each encodes two capsule depolymerases: isolation and functional characterization. Sci Rep. 2017;7(1):1–13.
  • Schwarzer D, Stummeyer K, Gerardy-Schahn R, et al. Characterization of a novel intramolecular chaperone domain conserved in endosialidases and other bacteriophage tail spike and fiber proteins. J Biol Chem. 2007;282(5):2821–2831.
  • Ricagno S, Spinelli S, Tremblay D, et al. Crystal structure of the Receptor-Binding protein head domain from Lactococcus lactis phage bIL170. J Virol. 2006;80(18):9331–9335.
  • Spinelli S, Veesler D, Bebeacua C, et al. Structures and host-adhesion mechanisms of lactococcal siphophages. Front Microbiol. 2014;5(January):3–13.
  • Tremblay DM, Tegoni M, Spinelli S, et al. Receptor-binding protein of Lactococcus lactis phages: Identification and characterization of the saccharide receptor-binding site. J Bacteriol. 2006;188(7):2400–2410.
  • Stockdale SR, Mahony J, Courtin P, et al. The lactococcal phages Tuc2009 and TP901-1 incorporate two alternate forms of their tail fiber into their virions for infection specialization. J Biol Chem. 2013;288(8):5581–5590.
  • Sciara G, Siponen M, Grath SM, et al. A topological model of the baseplate of lactococcal phage Tuc2009. J Biol Chem. 2008;283(5):2716–2723.
  • Spinelli S, Campanacci V, Blangy S, et al. Modular structure of the receptor binding proteins of Lactococcus lactis phages. The RBP structure of the temperate phage TP901-1. J Biol Chem. 2006;281(20):14256–14262.
  • Spinelli S, Bebeacua C, Orlov I, et al. Cryo-electron microscopy structure of lactococcal siphophage 1358 virion. J Virol. 2014;88(16):8900–8910.
  • Mahony J, Stockdale SR, Collins B, et al. Lactococcus lactis phage TP901 – 1 as a model for siphoviridae virion assembly. Bacteriophage. 2016;6(1):e1123795–7.
  • Garcia-Doval C, Van Raaij MJ. Structure of the receptor-binding carboxy-terminal domain of bacteriophage T7 tail fibers. Proc Natl Acad Sci USA. 2012;109(24):9390–9395.
  • Steinbacher S, Miller S, Baxa U, et al. Interaction of Salmonella phage P22 with its O-antigen receptor studied by X-ray crystallography. Biol Chem. 1997;378(3–4):337–343.
  • Landström J, Nordmark E-L, Eklund R, et al. Interaction of a Salmonella enteritidis O-antigen octasaccharide with the phage P22 tailspike protein by NMR spectroscopy and docking studies. Glycoconj J. 2008;25(2):137–143.
  • Handa H, Gurczynski S, Jackson MP, et al. Immobilization and molecular interactions between bacteriophage and lipopolysaccharide bilayers. Langmuir. 2010;26(14):12095–12103.
  • Lee I, Tu I, Yang F, et al. Structural basis for fragmenting the exopolysaccharide of Acinetobacter baumannii by bacteriophage Φ AB6 tailspike protein. Sci Rep. 2017;7:42711.
  • Sycheva LV, Shneider MM, Popova AV, et al. Crystal structure of the putative tail fiber protein gp53 from the Acinetobacter baumannii bacteriophage AP22. bioRxiv. 2019.
  • Kropinski AM, Arutyunov D, Foss M, et al. Genome and proteome of Campylobacter jejuni bacteriophage NCTC 12673. Appl Environ Microbiol. 2011;77(23):8265–8271.
  • Mahony J, van Sinderen D. Structural aspects of the interaction of dairy phages with their host bacteria. Viruses. 2012;4(9):1410–1424.
  • Veesler D, Spinelli S, Mahony J, et al. Suggests an alternative host adhesion mechanism; 2012.
  • Dunne M, Rupf B, Tala M, et al. Reprogramming bacteriophage host range through structure-guided design of chimeric receptor binding proteins. Cell Rep. 2019;29(5):1336–1350.
  • Hussain W, Wajid M, Farooq U, et al. Bacteriophage-based advanced bacterial detection: concept, mechanisms, and applications. Biosens Bioelectron. 2021;177:112973.
  • Tay LL, Huang PJ, Tanha J, et al. Silica encapsulated SERS nanoprobe conjugated to the bacteriophage tailspike protein for targeted detection of Salmonella. Chem Commun. 2012;48(7):1024–1026.
  • Poshtiban S, Singh A, Fitzpatrick G, et al. Bacteriophage tail-spike protein derivitized microresonator arrays for specific detection of pathogenic bacteria. Sens Actuators B Chem. 2013;181:410–416.
  • Piestrzyńska M, Dominik M, Kosiel K, et al. Ultrasensitive tantalum oxide nano-coated long-period gratings for detection of various biological targets. Biosens Bioelectron. 2019;133:8–15.
  • Cunha AP, Henriques R, Cardoso S, et al. Rapid and multiplex detection of nosocomial pathogens on a phage-based magnetoresistive lab-on-chip platform. Biotechnol Bioeng. 2021;118(8):3164–3174.
  • Shin HJ, Lim WK. Rapid label-free detection of E. coli using a novel SPR biosensor containing a fragment of tail protein from phage lambda. Prep Biochem Biotechnol. 2018;48(6):498–505.
  • Hyeon SH, Lim WK, Shin HJ. Novel surface plasmon resonance biosensor that uses full‐length Det7 phage tail protein for rapid and selective detection of Salmonella enterica serovar typhimurium. Biotechnol Appl Biochem. 2020;5:bab1883.
  • Denyes JM, Dunne M, Steiner S, et al. Modified bacteriophage S16 long tail fiber proteins for rapid and specific immobilization and detection of Salmonella cells. Appl Environ Microbiol. 2017;83(12):1–15.
  • Górska S, Rydosz A, Brzozowska E, et al. Effectiveness of sensors contact metallization (Ti, Au, and Ru) and biofunctionalization for Escherichia coli detection. Sensors. 2018;18(9):2912.
  • Santos SB, Costa AR, Carvalho C, et al. Exploiting bacteriophage proteomes: the hidden biotechnological potential. Trends Biotechnol. 2018;36(9):966–984.
  • Ahovan ZA, Hashemi A, De Plano LM, et al. Bacteriophage based biosensors: trends, outcomes and challenges. Nanomaterials. 2020;10(3):501.
  • Sharma S, Byrne H, O'Kennedy RJ. Antibodies and antibody-derived analytical biosensors. Essays Biochem. 2016;60(1):9–18.
  • Sande MG, Çaykara T, Silva CJ, et al. New solutions to capture and enrich bacteria from complex samples. Med Microbiol Immunol. 2020;209(3):335–341.
  • He Y, Shi Y, Liu M, et al. Nonlytic recombinant phage tail fiber protein for specific recognition of Pseudomonas aeruginosa. Anal Chem. 2018;90(24):14462–14468.
  • Kunstmann S, Scheidt T, Buchwald S, et al. Bacteriophage Sf6 tailspike protein for detection of Shigella flexneri pathogens. Viruses. 2018;10(8):431.
  • Shi Y, He Y, Zhang L, et al. Dual-site recognition of Pseudomonas aeruginosa using polymyxin B and bacteriophage tail fiber protein. Anal Chim Acta. 2021;1180:338855.
  • Born F, Braun P, Scholz HC, et al. Specific detection of yersinia pestis based on receptor binding proteins of phages. Pathogens. 2020;9(8):611–619.
  • Young R. Phage lysis: three steps, three choices, one outcome. J Microbiol. 2014;52(3):243–258.
  • Loessner MJ. Bacteriophage endolysins-current state of research and applications. Curr Opin Microbiol. 2005;8(4):480–487.
  • Catalão MJ, Gil F, Moniz-Pereira J, et al. Diversity in bacterial lysis systems: bacteriophages show the way. FEMS Microbiol Rev. 2013;37(4):554–571.
  • Fischetti VA. Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol. 2008;11(5):393–400.
  • Hermoso JA, García JL, García P. Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Curr Opin Microbiol. 2007;10(5):461–472.
  • Nelson DC, Schmelcher M, Rodriguez-Rubio L, et al. Endolysins as antimicrobials. Adv Virus Res. 2012;83:299–365.
  • Oliveira H, Azeredo J, Lavigne R, et al. Bacteriophage endolysins as a response to emerging foodborne pathogens. Trends Food Sci Technol. 2012;28(2):103–115.
  • Briers Y, Lavigne R. Breaking barriers: expansion of the use of endolysins as novel antibacterials against gram-negative bacteria. Future Microbiol. 2015;10(3):377–390.
  • Briers Y, Volckaert G, Cornelissen A, et al. Muralytic activity and modular structure of the endolysins of Pseudomonas aeruginosa bacteriophages phiKZ and EL. Mol Microbiol. 2007;65(5):1334–1344.
  • Fischetti VA. Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol. 2005;13(10):491–496.
  • Schmelcher M, Donovan DM, Loessner MJ. Bacteriophage endolysins as novel antimicrobials. Future Microbiol. 2012;7(10):1147–1171.
  • Hermoso JA, Monterroso B, Albert A, et al. Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. Structure. 2003;11(10):1239–1249.
  • Briers Y, Schmelcher M, Loessner MJ, et al. The high-affinity peptidoglycan binding domain of Pseudomonas phage endolysin KZ144. Biochem Biophys Res Commun. 2009;383(2):187–191.
  • Loessner MJ, Kramer K, Ebel F, et al. C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol Microbiol. 2002;44(2):335–349.
  • Sainathrao S, Mohan K, Atreya C. Gamma-phage lysin PlyG sequence-based synthetic peptides coupled with qdot-nanocrystals are useful for developing detection methods for Bacillus anthracis by using its surrogates, B. anthracis-Sterne and B. cereus-4342. BMC Biotechnol. 2009;9:67.
  • Santos SB, Oliveira A, Melo LDR, et al. Identification of the first endolysin cell binding domain (CBD) targeting Paenibacillus larvae. Sci Rep. 2019;9(1):1–9.
  • Son B, Kong M, Ryu S. The auxiliary role of the amidase domain in cell wall binding and exolytic activity of staphylococcal phage endolysins. Viruses. 2018;10(6):284–212.
  • Costa SP, Dias NM, Melo LDR, et al. A novel flow cytometry assay based on bacteriophage-derived proteins for Staphylococcus detection in blood. Sci Rep. 2020;10(1):6260.
  • Broendum SS, Buckle AM, McGowan S. Catalytic diversity and cell wall binding repeats in the phage-encoded endolysins. Mol Microbiol. 2018;110(6):879–896.
  • Pérez-Dorado I, Campillo NE, Monterroso B, et al. Elucidation of the molecular recognition of bacterial cell wall by modular pneumococcal phage endolysin CPL-1. J Biol Chem. 2007;282(34):24990–24999.
  • Grundling A, Schneewind O. Cross-Linked peptidoglycan mediates lysostaphin binding to the cell wall envelope of Staphylococcus aureus. J Bacteriol. 2006;188(7):2463–2472.
  • Korndörfer IP, Danzer J, Schmelcher M, et al. The crystal structure of the bacteriophage PSA endolysin reveals a unique fold responsible for specific recognition of listeria cell walls. J Mol Biol. 2006;364(4):678–689.
  • Bustamante N, Iglesias-Bexiga M, Bernardo-García N, et al. Deciphering how cpl-7 cell wall-binding repeats recognize the bacterial peptidoglycan. Sci Rep. 2017;7(1):16494.
  • Maciejewska B, Źrubek K, Espaillat A, et al. Modular endolysin of burkholderia AP3 phage has the largest lysozyme-like catalytic subunit discovered to date and no catalytic aspartate residue. Sci Rep. 2017;7(1):14501.
  • Fokine A, Miroshnikov KA, Shneider MM, et al. Structure of the bacteriophage phi KZ lytic transglycosylase gp144. J Biol Chem. 2008;283(11):7242–7250.
  • Ohnuma T, Onaga S, Murata K, et al. LysM domains from pteris ryukyuensis chitinase-A: a stability study and characterization of the chitin-binding site. J Biol Chem. 2008;283(8):5178–5187.
  • Oliveira H, Melo LDR, Santos SB, et al. Molecular aspects and comparative genomics of bacteriophage endolysins. J Virol. 2013;87(8):4558–4570.
  • Dunne M, Mertens HDT, Garefalaki V, et al. The CD27L and CTP1L endolysins targeting clostridia contain a built-in trigger and release factor. PLOS Pathog. 2014;10(7):e1004228.
  • Dunne M, Leicht S, Krichel B, et al. Crystal structure of the CTP1L endolysin reveals how its activity is regulated by a secondary translation product. J Biol Chem. 2016;291(10):4882–4893.
  • Gu J, Xu W, Lei L, et al. LysGH15, a novel bacteriophage lysin, protects a murine bacteremia model efficiently against lethal methicillin-resistant Staphylococcus aureus infection. J Clin Microbiol. 2011;49(1):111–117.
  • Linden SB, Zhang H, Heselpoth RD, et al. Biochemical and biophysical characterization of PlyGRCS, a bacteriophage endolysin active against methicillin-resistant Staphylococcus aureus. Appl Microbiol Biotechnol. 2015;99(2):741–752.
  • Chang Y, Kim M, Ryu S. Characterization of a novel endolysin LysSA11 and its utility as a potent biocontrol agent against Staphylococcus aureus on food and utensils. Food Microbiol. 2017;68:112–120.
  • Benešík M, Nováček J, Janda L, et al. Role of SH3b binding domain in a natural deletion mutant of kayvirus endolysin LysF1 with a broad range of lytic activity. Virus Genes. 2018;54(1):130–139.
  • García P, García JL, García E, et al. Modular organization of the lytic enzymes of Streptococcus pneumoniae and its bacteriophages. Gene. 1990;86(1):81–88.
  • Schmelcher M, Shabarova T, Eugster MR, et al. Rapid multiplex detection and differentiation of listeria cells by use of fluorescent phage endolysin cell wall binding domains. Appl Environ Microbiol. 2010;76(17):5745–5756.
  • Kong M, Ryu S. Identification of a bacteria-specific binding protein from the sequenced bacterial genome. J Microbiol Biotechnol. 2016;26(1):38–43.
  • Park C, Kong M, Lee JH, et al. Detection of Bacillus cereus using bioluminescence assay with cell wall-binding domain conjugated magnetic nanoparticles. BioChip J. 2018;12(4):287–293.
  • Singh U, Arutyunov D, Basu U, et al. Mycobacteriophage lysin-mediated capture of cells for the PCR detection of Mycobacterium avium subspecies paratuberculosis. Anal Methods. 2014;6(15):5682–5689.
  • Yang H, Wang DB, Dong Q, et al. Existence of separate domains in lysin PlyG for recognizing Bacillus anthracis spores and vegetative cells. Antimicrob Agents Chemother. 2012;56(10):5031–5039.
  • Schmelcher M, Tchang VS, Loessner MJ. Domain shuffling and module engineering of listeria phage endolysins for enhanced lytic activity and binding affinity. Microb Biotechnol. 2011;4(5):651–662.
  • Rostova E, Ben Adiba C, Dietler G, et al. Kinetics of antibody binding to membranes of living bacteria measured by a photonic crystal-based biosensor. Biosensors. 2016;6(4):52.
  • Medina MB, Van Houten L, Cooke PH, et al. Real-time analysis of antibody binding interactions with immobilized E. coli O157:H7 cells using the BIAcore. Biotechnol Tech. 1997;11(3):173–176.
  • Gómez-Torres N, Dunne M, Garde S, et al. Development of a specific fluorescent phage endolysin for in situ detection of Clostridium species associated with cheese spoilage. Microb Biotechnol. 2018;11(2):332–345.
  • Kong M, Sim J, Kang T, et al. A novel and highly specific phage endolysin cell wall binding domain for detection of Bacillus cereus. Eur Biophys J. 2015;44(6):437–446.
  • Kong M, Shin JH, Heu S, et al. Lateral flow assay-based bacterial detection using engineered cell wall binding domains of a phage endolysin. Biosens Bioelectron. 2017;96:173–177.
  • Wang Y, He Y, Bhattacharyya S, et al. Recombinant bacteriophage cell-binding domain proteins for broad-spectrum recognition of methicillin-resistant Staphylococcus aureus strains. Anal Chem. 2020;92(4):3340–3345.
  • Croux C, Ronda C, López R, et al. Role of the C-terminal domain of the lysozyme of Clostridium acetobutylicum ATCC 824 in a chimeric pneumococcal-clostridial cell wall lytic enzyme. FEBS Lett. 1993;336(1):111–114.
  • Croux C, Ronda C, Lopez R, et al. Interchange of functional domains switches enzyme specificity: construction of a chimeric pneumococcal-clostridial cell wall lytic enzyme. Mol Microbiol. 1993;9(5):1019–1025.
  • Sheehan MM, Garcia JL, López R, et al. Analysis of the catalytic domain of the lysin of the lactococcal bacteriophage Tuc2009 by chimeric gene assembling. FEMS Microbiol Lett. 1996;140(1):23–28.
  • Becker SC, Foster-Frey J, Stodola AJ, et al. Differentially conserved staphylococcal SH3b_5 cell wall binding domains confer increased staphylolytic and streptolytic activity to a streptococcal prophage endolysin domain. Gene. 2009;443(1-2):32–41.
  • Kretzer JW, Schmelcher M, Loessner MJ. Ultrasensitive and fast diagnostics of viable listeria cells by CBD magnetic separation combined with A511::luxAB detection. Viruses. 2018;10(11):626.
  • Kwon SJ, Kim D, Lee I, et al. Sensitive multiplex detection of whole bacteria using self-assembled cell binding domain complexes. Anal Chim Acta. 2018;1030:156–165.
  • Yang H, Wang Y, Liu S, et al. Lateral flow assay of methicillin-resistant Staphylococcus aureus using bacteriophage cellular wall-binding domain as recognition agent. Biosens Bioelectron. 2021;182:113189.
  • Yang Y, Xu F, Xu H, et al. Magnetic nano-beads based separation combined with propidium monoazide treatment and multiplex PCR assay for simultaneous detection of viable Salmonella typhimurium, Escherichia coli O157:H7 and Listeria monocytogenes in food products. Food Microbiol. 2013;34(2):418–424.
  • Skvarc M, Stubljar D, Rogina P, et al. Non-culture-based methods to diagnose bloodstream infection: does it work? Eur J Microbiol Immunol. 2013;3(2):97–104.
  • Yi Z, Wang S, Meng X, et al. Lysin cell-binding domain-functionalized magnetic beads for detection of Staphylococcus aureus via inhibition of fluorescence of amplex red/hydrogen peroxide assay by intracellular catalase. Anal Bioanal Chem. 2019;411(27):7177–7185.
  • Tolba M, Ahmed MU, Tlili C, et al. A bacteriophage endolysin-based electrochemical impedance biosensor for the rapid detection of listeria cells. Analyst. 2012;137(24):5749–5756.
  • Gray A, Bradbury ARM, Knappik A, et al. Animal-free alternatives and the antibody iceberg. Nat Biotechnol. 2020;38(11):1234–1239.
  • Bhowmick T, Mirrett S, Reller LB, et al. Controlled multicenter evaluation of a bacteriophage-based method for rapid detection of Staphylococcus aureus in positive blood cultures. J Clin Microbiol. 2013;51(4):1226–1230.
  • Disruptive phage technology attracts top scientist to PBD Biotech. PBD Biotech [cited 2022 Jan 25]. Available from: https://www.pbdbio.com/news/disruptive-phage-technology-attracts-top-scientist-to-pbd-biotech/
  • VIDAS® – Rapid, automated food pathogen detection | bioMérieux industrial microbiology [cited 2022 Feb 4]. Available from: https://www.biomerieux-industry.com/products/vidas-high-performance-food-pathogen-detection

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.