Bacteriophage-encoded depolymerases: their diversity and biotechnological applications

Applied Microbiology and Biotechnology

Volumn 100, Issue 5, 2016, Pages 2141-2151

  Pires, Diana P ^a   Oliveira, Hugo ^a   Melo, Luís D R ^a   Sillankorva, Sanna ^a   Azeredo, Joana ^a  

^a UNIVERSITY OF MINHO   (Portugal)

Author keywords

Bacteriophages; Biofilms; Capsular polysaccharides; Phage depolymerases

Indexed keywords

BACTERIA; BIOFILMS; CELL MEMBRANES; ENZYMES; FOOD PROCESSING; POLYMERS; POLYSACCHARIDES;

BACTERIAL BIOFILM; BACTERIAL CELL SURFACE; BIOTECHNOLOGICAL APPLICATIONS; CAPSULAR POLYSACCHARIDES; EXTRA-CELLULAR POLYMERIC SUBSTANCES; FOOD PROCESSING INDUSTRY; NATURAL ENEMIES; POLYMERIC SUBSTANCE;

BACTERIOPHAGES;

DEPOLYMERASE; DEXTRANASE; HYALURONIDASE; HYDROLASE; PECTIN LYASE; POLYSACCHARIDE; SIALIDASE; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; VIRUS ENZYME; XYLAN 1,4 BETA XYLOSIDASE; BIOPOLYMER; LYASE;

BACTERIOPHAGE; BIOFILM; BIOTECHNOLOGY; CATALYSIS; ENZYME ACTIVITY; FOOD INDUSTRY; POLYSACCHARIDE;

BACTERIOPHAGE; BIOFILM; MYOVIRIDAE; NONHUMAN; PODOVIRIDAE; POLYMERIZATION; REVIEW; SIPHOVIRIDAE; BIOTRANSFORMATION; ENZYMOLOGY; GENETICS; METABOLISM;

BACTERIA (MICROORGANISMS); MYOVIRIDAE; PODOVIRIDAE; SIPHOVIRIDAE;

BACTERIOPHAGES; BIOPOLYMERS; BIOTRANSFORMATION; HYDROLASES; LYASES;

EID: 84954421775     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-7247-0     Document Type: Review

References (110)

1. Abdi-Ali A, Mohammadi-Mehr M, Agha Alaei Y (2006) Bactericidal activity of various antibiotics against biofilm-producing Pseudomonas aeruginosa. Int J Antimicrob Agents 27:196–200. doi:10.1016/j.ijantimicag.2005.10.007
2. Abedon ST, Kuhl SJ, Blasdel BG, Kutter EM (2011) Phage treatment of human infections. Bacteriophage 1:66–85. doi:10.4161/bact.1.2.15845
3. Albrecht MT, Schiller NL (2005) Alginate lyase (AlgL) activity is required for alginate biosynthesis in Pseudomonas aeruginosa. J Bacteriol 187:3869–3872. doi:10.1128/JB.187.11.3869-3872.2005
4. Alkawash MA, Soothill JS, Schiller NL (2006) Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. APMIS 114:131–138. doi:10.1111/j.1600-0463.2006.apm_356.x
5. Andres D, Hanke C, Baxa U, Seul A, Barbirz S, Seckler R (2010) Tailspike interactions with lipopolysaccharide effect DNA ejection from phage P22 particles in vitro. J Biol Chem 285:36768–36775. doi:10.1074/jbc.M110.169003
6. Baker JR, Dong S, Pritchard DG (2002) The hyaluronan lyase of Streptococcus pyogenes bacteriophage H4489A. Biochem J 365:317. doi:10.1042/BJ20020149
7. Barbirz S, Müller JJ, Uetrecht C, Clark AJ, Heinemann U, Seckler R (2008) Crystal structure of Escherichia coli phage HK620 tailspike: podoviral tailspike endoglycosidase modules are evolutionarily related. Mol Microbiol 69:303–316. doi:10.1111/j.1365-2958.2008.06311.x
8. Bartell PF, Orr TE, Lam GK (1966) Polysaccharide depolymerase associated with bacteriophage infection. J Bacteriol 92:56–62
9. Bayer AS, Speert DP, Park S, Tu J, Witt M, Nast CC, Norman DC (1991) Functional role of mucoid exopolysaccharide (alginate) in antibiotic-induced and polymorphonuclear leukocyte-mediated killing of Pseudomonas aeruginosa. Infect Immun 59:302–308
10. Beg QK, Kapoor M, Mahajan L, Hoondal GS (2001) Microbial xylanases and their industrial applications: a review. Appl Microbiol Biotechnol 56:326–338. doi:10.1007/s002530100704
11. Bertozzi Silva J, Sauvageau D (2014) Bacteriophages as antimicrobial agents against bacterial contaminants in yeast fermentation processes. Biotechnol Biofuels 7:123. doi:10.1186/s13068-014-0123-9
12. Brooks JD, Flint SH (2008) Biofilms in the food industry: problems and potential solutions. Int J Food Sci Technol 43:2163–2176. doi:10.1111/j.1365-2621.2008.01839.x
13. Candela T, Fouet A (2006) Poly-gamma-glutamate in bacteria. Mol Microbiol 60:1091–1098. doi:10.1111/j.1365-2958.2006.05179.x
14. Capparelli R, Parlato M, Borriello G, Salvatore P, Iannelli D (2007) Experimental phage therapy against Staphylococcus aureus in mice. Antimicrob Agents Chemother 51:2765–2773. doi:10.1128/AAC.01513-06
15. Chaffin DO, Mentele LM, Rubens CE (2005) Sialylation of group B streptococcal capsular polysaccharide is mediated by cpsK and is required for optimal capsule polymerization and expression. J Bacteriol 187:4615–4626. doi:10.1128/JB.187.13.4615-4626.2005
16. Chua JE, Manning PA, Morona R (1999) The Shigella flexneri bacteriophage Sf6 tailspike protein (TSP)/endorhamnosidase is related to the bacteriophage P22 TSP and has a motif common to exo- and endoglycanases, and C-5 epimerases. Microbiology 145:1649–1659. doi:10.1099/13500872-145-7-1649
17. Clark LE, Mellette JR (1994) The use of hyaluronidase as an adjunct to surgical procedures. J Dermatol Surg Oncol 20:842–844. doi:10.1111/j.1524-4725.1994.tb03718.x
18. Clementi F (1997) Alginate production by Azotobacter vinelandii. Crit Rev Biotechnol 17:327–361. doi:10.3109/07388559709146618
19. Clokie MR, Millard AD, Letarov AV, Heaphy S (2011) Phages in nature. Bacteriophage 1:31–45. doi:10.4161/bact.1.1.14942
20. Cornelissen A, Ceyssens P-J, T’Syen J, Van Praet H, Noben J-P, Shaburova OV, Krylov VN, Volckaert G, Lavigne R (2011) The T7-related Pseudomonas putida phage φ15 displays virion-associated biofilm degradation properties. PLoS One 6:e18597. doi:10.1371/journal.pone.0018597
21. Cornelissen A, Ceyssens P-J, Krylov VN, Noben J-P, Volckaert G, Lavigne R (2012) Identification of EPS-degrading activity within the tail spikes of the novel Pseudomonas putida phage AF. Virology 434:251–256. doi:10.1016/j.virol.2012.09.030
22. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745. doi:10.1146/annurev.mi.49.100195.003431
23. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science (80-) 284:1318–1322. doi:10.1126/science.284.5418.1318
24. Dahech I, Ben Ayed H, Belghith KS, Belghith H, Mejdoub H (2013) Microbial production of levanase for specific hydrolysis of levan. Int J Biol Macromol 60:128–133. doi:10.1016/j.ijbiomac.2013.05.002
25. Davey ME, O’toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867. doi:10.1128/MMBR.64.4.847-867.2000
26. Davidson IW, Lawson CJ, Sutherland IW (1977) An alginate lysate from Azotobacter vinelandii phage. J Gen Microbiol 98:223–229
27. Davies G, Henrissat B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3:853–859. doi:10.1016/S0969-2126(01)00220-9
28. Donlan RM (2001a) Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis 33:1387–1392. doi:10.1086/322972
29. Donlan RM (2001b) Biofilms and device-associated infections. Emerg Infect Dis 7:277–281. doi:10.3201/eid0702.700277
30. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890. doi:10.3201/eid0809.020063
31. Drulis-Kawa Z, Majkowska-Skrobek G, Maciejewska B (2015) Bacteriophages and phage-derived proteins—application approaches. Curr Med Chem 22:1757–1773. doi:10.2174/0929867322666150209152851
32. Eriksson U, Svenson SB, Lönngren J, Lindberg AA (1979) Salmonella phage glycanases: substrate specificity of the phage P22 endo-rhamnosidase. J Gen Virol 43:503–511. doi:10.1099/0022-1317-43-3-503
33. Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633. doi:10.1038/nrmicro2415
34. Flemming H-C, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J Bacteriol 189:7945–7947. doi:10.1128/JB.00858-07
35. Frirdich E, Whitfield C (2005) Characterization of Gla(KP), a UDP-galacturonic acid C4-epimerase from Klebsiella pneumoniae with extended substrate specificity. J Bacteriol 187:4104–4115. doi:10.1128/JB.187.12.4104-4115.2005
36. Garron M-L, Cygler M (2010) Structural and mechanistic classification of uronic acid-containing polysaccharide lyases. Glycobiology 20:1547–1573. doi:10.1093/glycob/cwq122
37. Gerardy-Schahn R, Bethe A, Brennecke T, Mühlenhoff M, Eckhardt M, Ziesing S, Lottspeich F, Frosch M (1995) Molecular cloning and functional expression of bacteriophage PK1E-encoded endoneuraminidase Endo NE. Mol Microbiol 16:441–450. doi:10.1111/j.1365-2958.1995.tb02409.x
38. Glonti T, Chanishvili N, Taylor PW (2010) Bacteriophage-derived enzyme that depolymerizes the alginic acid capsule associated with cystic fibrosis isolates of Pseudomonas aeruginosa. J Appl Microbiol 108:695–702. doi:10.1111/j.1365-2672.2009.04469.x
39. Gualdi L, Hayre JK, Gerlini A, Bidossi A, Colomba L, Trappetti C, Pozzi G, Docquier J-D, Andrew P, Ricci S, Oggioni MR (2012) Regulation of neuraminidase expression in Streptococcus pneumoniae. BMC Microbiol 12:200. doi:10.1186/1471-2180-12-200
40. Guenther S, Huwyler D, Richard S, Loessner MJ (2009) Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl Environ Microbiol 75:93–100. doi:10.1128/AEM.01711-08
41. Gupta R, Gupta N, Rathi P (2004) Bacterial lipases: an overview of production, purification and biochemical properties. Appl Microbiol Biotechnol 64:763–781. doi:10.1007/s00253-004-1568-8
42. Gutiérrez D, Martínez B, Rodríguez A, García P (2012) Genomic characterization of two Staphylococcus epidermidis bacteriophages with anti-biofilm potential. BMC Genomics 13:228. doi:10.1186/1471-2164-13-228
43. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108. doi:10.1038/nrmicro821
44. Hanlon GW, Denyer SP, Olliff CJ, Ibrahim LJ (2001) Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 67:2746–2753. doi:10.1128/AEM.67.6.2746-2753.2001
45. Harper D, Parracho H, Walker J, Sharp R, Hughes G, Werthén M, Lehman S, Morales S (2014) Bacteriophages and biofilms. Antibiotics 3:270–284. doi:10.3390/antibiotics3030270
46. Hatch RA, Schiller NL (1998) Alginate lyase promotes diffusion of aminoglycosides through the extracellular polysaccharide of mucoid Pseudomonas aeruginosa. Antimicrob Agents Chemother 42:974–977
47. Hsu C-R, Lin T-L, Pan Y-J, Hsieh P-F, Wang J-T (2013) Isolation of a bacteriophage specific for a new capsular type of Klebsiella pneumoniae and characterization of its polysaccharide depolymerase. PLoS One 8:e70092. doi:10.1371/journal.pone.0070092
48. Hughes KA, Sutherland IW, Clark J, Jones MV (1998a) Bacteriophage and associated polysaccharide depolymerases-novel tools for study of bacterial biofilms. J Appl Microbiol 85:583–590. doi:10.1046/j.1365-2672.1998.853541.x
49. Hughes KA, Sutherland IW, Jones MV (1998b) Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase. Microbiology 144:3039–3047. doi:10.1099/00221287-144-11-3039
50. Hugouvieux-Cotte-Pattat N, Condemine G, Shevchik VE (2014) Bacterial pectate lyases, structural and functional diversity. Environ Microbiol Rep 6:427–440. doi:10.1111/1758-2229.12166
51. Hynes WL, Walton SL (2000) Hyaluronidases of gram-positive bacteria. FEMS Microbiol Lett 183:201–207. doi:10.1111/j.1574-6968.2000.tb08958.x
52. Hynes WL, Hancock L, Ferretti JJ (1995) Analysis of a second bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a third hyaluronidase involved in extracellular enzymatic activity. Infect Immun 63:3015–3020
53. Jaeger KE, Ransac S, Dijkstra BW, Colson C, van Heuvel M, Misset O (1994) Bacterial lipases. FEMS Microbiol Rev 15:29–63. doi:10.1111/j.1574-6976.1994.tb00121.x
54. Jiménez ER (2009) Dextranase in sugar industry: a review. Sugar Tech 11:124–134. doi:10.1007/s12355-009-0019-3
55. Juturu V, Wu JC (2012) Microbial xylanases: engineering, production and industrial applications. Biotechnol Adv 30:1219–1227. doi:10.1016/j.biotechadv.2011.11.006
56. Kim WS, Geider K (2000) Characterization of a viral EPS-depolymerase, a potential tool for control of fire blight. Phytopathology 90:1263–1268. doi:10.1094/PHYTO.2000.90.11.1263
57. Kim HS, Lee C-G, Lee EY (2011a) Alginate lyase: structure, property, and application. Biotechnol Bioprocess Eng 16:843–851. doi:10.1007/s12257-011-0352-8
58. Kim S, Oh D-B, Kang HA, Kwon O (2011b) Features and applications of bacterial sialidases. Appl Microbiol Biotechnol 91:1–15. doi:10.1007/s00253-011-3307-2
59. Kimura K, Itoh Y (2003) Characterization of poly-gamma-glutamate hydrolase encoded by a bacteriophage genome: possible role in phage infection of Bacillus subtilis encapsulated with poly-gamma-glutamate. Appl Environ Microbiol 69:2491–2497. doi:10.1128/AEM.69.5.2491-2497.2003
60. Kulkarni N, Shendye A, Rao M (1999) Molecular and biotechnological aspects of xylanases. FEMS Microbiol Rev 23:411–456. doi:10.1111/j.1574-6976.1999.tb00407.x
61. Kutateladze M, Adamia R (2010) Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol 28:591–595. doi:10.1016/j.tibtech.2010.08.001
62. Kutter E, De Vos D, Gvasalia G, Alavidze Z, Gogokhia L, Kuhl S, Abedon ST (2010) Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol 11:69–86. doi:10.2174/138920110790725401
63. Lewis AL, Lewis WG (2012) Host sialoglycans and bacterial sialidases: a mucosal perspective. Cell Microbiol 14:1174–1182. doi:10.1111/j.1462-5822.2012.01807.x
64. Lin T-L, Hsieh P-F, Huang Y-T, Lee W-C, Tsai Y-T, Su P-A, Pan Y-J, Hsu C-R, Wu M-C, Wang J-T (2014) Isolation of a bacteriophage and its depolymerase specific for K1 capsule of Klebsiella pneumoniae: implication in typing and treatment. J Infect Dis 210:1734–1744. doi:10.1093/infdis/jiu332
65. Long GS, Bryant JM, Taylor PW, Luzio JP (1995) Complete nucleotide sequence of the gene encoding bacteriophage E endosialidase: implications for K1E endosialidase structure and function. Biochem J 309(Pt 2):543–550. doi:10.1042/bj3090543
66. Lu TK, Collins JJ (2007) Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci U S A 104:11197–11202. doi:10.1073/pnas.0704624104
67. Luna AJ, Wood TL, Chamakura KR, Kuty Everett GF (2013) Complete genome of Salmonella enterica serovar enteritidis myophage Marshall. Genome Announc. doi:10.1128/genomeA.00867-13
68. Mah TF, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39. doi:10.1016/S0966-842X(00)01913-2
69. Manzanares P, Vallés S, Ramòn D, Orejas M (2007) α-L-rhamnosidases: old and new insights. In: Polaina J, MacCabe AP (eds) Industrial enzymes. Springer Netherlands, Dordrecht, pp 117–140
70. Marvasi M, Visscher PT, Casillas Martinez L (2010) Exopolymeric substances (EPS) from Bacillus subtilis: polymers and genes encoding their synthesis. FEMS Microbiol Lett 313:1–9. doi:10.1111/j.1574-6968.2010.02085.x
71. Matsuzaki S, Rashel M, Uchiyama J, Sakurai S, Ujihara T, Kuroda M, Ikeuchi M, Tani T, Fujieda M, Wakiguchi H, Imai S (2005) Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases. J Infect Chemother 11:211–219. doi:10.1007/s10156-005-0408-9
72. McVay CS, Velásquez M, Fralick JA (2007) Phage therapy of Pseudomonas aeruginosa infection in a mouse burn wound model. Antimicrob Agents Chemother 51:1934–1938. doi:10.1128/AAC.01028-06
73. Melo LDR, Sillankorva S, Ackermann H-W, Kropinski AM, Azeredo J, Cerca N (2014) Characterization of Staphylococcus epidermidis phage vB_SepS_SEP9—a unique member of the Siphoviridae family. Res Microbiol 165:679–685. doi:10.1016/j.resmic.2014.09.012
74. Miasnikov AN (1997) Characterization of a novel endo-levanase and its gene from Bacillus sp. L7. FEMS Microbiol Lett 154:23–28. doi:10.1111/j.1574-6968.1997.tb12619.x
75. Michaud P, Da Costa A, Courtois B, Courtois J (2003) Polysaccharide lyases: recent developments as biotechnological tools. Crit Rev Biotechnol 23:233–266. doi:10.1080/07388550390447043
76. Monday SR, Schiller NL (1996) Alginate synthesis in Pseudomonas aeruginosa: the role of AlgL (alginate lyase) and AlgX. J Bacteriol 178:625–632
77. Morello E, Saussereau E, Maura D, Huerre M, Touqui L, Debarbieux L (2011) Pulmonary bacteriophage therapy on Pseudomonas aeruginosa cystic fibrosis strains: first steps towards treatment and prevention. PLoS One 6:e16963. doi:10.1371/journal.pone.0016963
78. Murakami H, Kuramoto T, Mizutani K, Nakano H, Kitahata S (1992) Purification and some properties of a new levanase from Bacillus sp. No. 71. Biosci Biotechnol Biochem 56:608–613. doi:10.1271/bbb.56.608
79. Mushtaq N, Redpath MB, Luzio JP, Taylor PW (2004) Prevention and cure of systemic Escherichia coli K1 infection by modification of the bacterial phenotype. Antimicrob Agents Chemother 48:1503–1508. doi:10.1128/AAC.48.5.1503-1508.2004
80. Mushtaq N, Redpath MB, Luzio JP, Taylor PW (2005) Treatment of experimental Escherichia coli infection with recombinant bacteriophage-derived capsule depolymerase. J Antimicrob Chemother 56:160–165. doi:10.1093/jac/dki177
81. O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79. doi:10.1146/annurev.micro.54.1.49
82. Oliveira A, Sereno R, Azeredo J (2010) In vivo efficiency evaluation of a phage cocktail in controlling severe colibacillosis in confined conditions and experimental poultry houses. Vet Microbiol 146:303–308. doi:10.1016/j.vetmic.2010.05.015
83. Oliveira H, Melo LDR, Santos SB, Nóbrega FL, Ferreira EC, Cerca N, Azeredo J, Kluskens LD (2013) Molecular aspects and comparative genomics of bacteriophage endolysins. J Virol 87:4558–4570. doi:10.1128/JVI.03277-12
84. Parsek MR, Singh PK (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57:677–701. doi:10.1146/annurev.micro.57.030502.090720
85. Paton AM (1960) The role of Pseudomonas in plant disease. J Appl Bacteriol 23:526–532. doi:10.1111/j.1365-2672.1960.tb00224.x
86. Petter JG, Vimr ER (1993) Complete nucleotide sequence of the bacteriophage K1F tail gene encoding endo-N-acylneuraminidase (endo-N) and comparison to an endo-N homolog in bacteriophage PK1E. J Bacteriol 175:4354–4363
87. Reid G (1999) Biofilms in infectious disease and on medical devices. Int J Antimicrob Agents 11:223–226. doi:10.1016/S0924-8579(99)00020-5
88. Ritz MP, Perl AL, Colquhoun JM, Chamakura KR, Kuty Everett GF (2013) Complete genome of bacillus subtilis myophage CampHawk. Genome Announc. doi:10.1128/genomeA.00984-13
89. Santos SB, Carvalho CM, Sillankorva S, Nicolau A, Ferreira EC, Azeredo J (2009) The use of antibiotics to improve phage detection and enumeration by the double-layer agar technique. BMC Microbiol 9:148. doi:10.1186/1471-2180-9-148
90. Scholl D, Merril C (2005) The genome of bacteriophage K1F, a T7-like phage that has acquired the ability to replicate on K1 strains of Escherichia coli. J Bacteriol 187:8499–8503. doi:10.1128/JB.187.24.8499-8503.2005
91. Scholl D, Rogers S, Adhya S, Merril CR (2001) 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 75:2509–2515. doi:10.1128/JVI.75.6.2509-2515.2001
92. Schwarzer D, Buettner FFR, Browning C, Nazarov S, Rabsch W, Bethe A, Oberbeck A, Bowman VD, Stummeyer K, Muhlenhoff M, Leiman PG, Gerardy-Schahn R (2012) A multivalent adsorption apparatus explains the broad host range of phage phi92: a comprehensive genomic and structural analysis. J Virol 86:10384–10398. doi:10.1128/JVI.00801-12
93. Scorpio A, Chabot DJ, Day WA, O’brien DK, Vietri NJ, Itoh Y, Mohamadzadeh M, Friedlander AM (2007) Poly-gamma-glutamate capsule-degrading enzyme treatment enhances phagocytosis and killing of encapsulated Bacillus anthracis. Antimicrob Agents Chemother 51:215–222. doi:10.1128/AAC.00706-06
94. Scorpio A, Tobery SA, Ribot WJ, Friedlander AM (2008) Treatment of experimental anthrax with recombinant capsule depolymerase. Antimicrob Agents Chemother 52:1014–1020. doi:10.1128/AAC.00741-07
95. Severi E, Hood DW, Thomas GH (2007) Sialic acid utilization by bacterial pathogens. Microbiology 153:2817–2822. doi:10.1099/mic.0.2007/009480-0
96. Shi X, Zhu X (2009) Biofilm formation and food safety in food industries. Trends Food Sci Technol 20:407–413. doi:10.1016/j.tifs.2009.01.054
97. Sieiro C, García-Fraga B, López-Seijas J, da Silva AF, Villa TG (2012) Microbial Pectic Enzymes in the Food and Wine Industry. In: Valdez B (ed) Food Industrial Processes-Methods and Equipment. InTech, pp 201–218
98. Sillankorva S, Neubauer P, Azeredo J (2008) Pseudomonas fluorescens biofilms subjected to phage phiIBB-PF7A. BMC Biotechnol 8:79. doi:10.1186/1472-6750-8-79
99. Singh SK, Bharati AP, Singh N, Pandey P, Joshi P, Singh K, Mitra K, Gayen JR, Sarkar J, Akhtar MS (2014) The prophage-encoded hyaluronate lyase has broad substrate specificity and is regulated by the N-terminal domain. J Biol Chem 289:35225–35236. doi:10.1074/jbc.M113.507673
100. Sulakvelidze A (2005) Phage therapy: an attractive option for dealing with antibiotic-resistant bacterial infections. Drug Discov Today 10:807–809. doi:10.1016/S1359-6446(05)03441-0
101. Sunna A, Antranikian G (1997) Xylanolytic enzymes from fungi and bacteria. Crit Rev Biotechnol 17:39–67. doi:10.3109/07388559709146606
102. Sutherland IW (1995) Polysaccharide lyases. FEMS Microbiol Rev 16:323–347
103. Tait K, Skillman LC, Sutherland IW (2002) The efficacy of bacteriophage as a method of biofilm eradication. Biofouling 18:305–311. doi:10.1080/0892701021000034418
104. Timoney JF, Pesante L, Ernst C (1982) Hyaluronidase associated with a temperate bacteriophage of Streptococcus equi. In: Schlessinger D (ed) Microbiology. American Society for Microbiology, Washington, DC, pp 145–146
105. Traving C, Schauer R (1998) Structure, function and metabolism of sialic acids. Cell Mol Life Sci 54:1330–1349. doi:10.1007/s000180050258
106. Trigo G, Martins TG, Fraga AG, Longatto-Filho A, Castro AG, Azeredo J, Pedrosa J (2013) Phage therapy is effective against infection by Mycobacterium ulcerans in a murine footpad model. PLoS Negl Trop Dis 7:e2183. doi:10.1371/journal.pntd.0002183
107. Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14:2535–2554. doi:10.3390/molecules14072535
108. Wong TY, Preston LA, Schiller NL (2000) Alginate lyase: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu Rev Microbiol 54:289–340. doi:10.1146/annurev.micro.54.1.289
109. Yadav V, Yadav PK, Yadav S, Yadav KDS (2010) α-l-Rhamnosidase: a review. Process Biochem 45:1226–1235. doi:10.1016/j.procbio.2010.05.025
110. Yan J, Mao J, Mao J, Xie J (2014) Bacteriophage polysaccharide depolymerases and biomedical applications. BioDrugs 28:265–274. doi:10.1007/s40259-013-0081-y