Bacteriocins with a broader antimicrobial spectrum prevail in enterococcal symbionts isolated from the hoopoe's uropygial gland

FEMS Microbiology Ecology

Volumn 85, Issue 3, 2013, Pages 495-502

  Ruiz Rodríguez, Magdalena ^a,b   Martínez Bueno, Manuel ^b   Martín Vivaldi, Manuel ^b   Valdivia, Eva ^b   Soler, Juan J ^a,b  

^a DEPARTAMENTO DE ECOLOGÍA FUNCIONAL Y EVOLUTIVA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

Antimicrobial activity; Bacteriocin genes; Ecological immunology; Enterococcus; Symbiosis; Upupa epops

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIOCIN;

ANTAGONISM; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIRD; FITNESS; GENE EXPRESSION; GENOME; IMMUNE SYSTEM; METABOLITE; PATHOGEN; SYMBIONT; SYMBIOSIS; TOXIN;

ANIMAL; ANTIBIOSIS; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIOCIN GENES; BIRD; CLASSIFICATION; ECOLOGICAL IMMUNOLOGY; ENTEROCOCCUS; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; SYMBIOSIS; UPUPA EPOPS;

ANTIMICROBIAL ACTIVITY; BACTERIOCIN GENES; ECOLOGICAL IMMUNOLOGY; ENTEROCOCCUS; SYMBIOSIS; UPUPA EPOPS;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBIOSIS; BACTERIOCINS; BIRDS; ENTEROCOCCUS; SYMBIOSIS;

ANIMALIA; BACTERIA (MICROORGANISMS); ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; UPUPA EPOPS; UPUPIDAE;

EID: 84881550238     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12138     Document Type: Article

References (43)

1. Almeida T, Brandao A, Muñoz-Atienza E, Gonçalves A, Torres C, Igrejas G, Hernández PE, Herranz C, Cintas LM & Poeta P (2011) Identification of bacteriocin genes in enterococci isolated from game animals and saltwater fish. J Food Prot 74: 1252-1260.
2. Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Aymerich T, Holo H, Havarstein LS, Hugas M, Garriga M & Nes IF (1996) Biochemical and genetic characterization of enterocin A from Enterococcus faecium, a new antilisterial bacteriocin in the pediocin family of bacteriocins. Appl Environ Microbiol 62: 1676-1682.
4. Brandão A, Almeida T, Muñoz-Atienza E, Torres C, Igrejas G, Hernandez PE, Cintas LM, Poeta P & Herranz C (2010) Antimicrobial activity and occurrence of bacteriocin structural genes in Enterococcus spp. of human and animal origin isolated in Portugal. Arch Microbiol 192: 927-936.
5. Casaus P, Nilsen T, Cintas LM, Nes IF, Hernandez PE & Holo H (1997) Enterocin B, a new bacteriocin from Enterococcus faecium T136 which can act synergistically with enterocin A. Microbiology 143: 2287-2294.
6. Cintas LM, Casaus P, Holo H, Hernandez PE, Nes IF & Havarstein LS (1998) Enterocins L50A and L50B, two novel bacteriocins from Enterococcus faecium L50, are related to staphylococcal hemolysins. J Bacteriol 180: 1988-1994.
7. Cintas LM, Casaus P, Herranz C, Havarstein LS, Holo H, Hernandez PE & Nes IF (2000) Biochemical and genetic evidence that Enterococcus faecium L50 produces enterocins L50A and L50B, the sec-dependent enterocin P, and a novel bacteriocin secreted without an N-terminal extension termed enterocin Q. J Bacteriol 182: 6806-6814.
8. Clark L & Mason JR (1985) Use of nest material as insecticidal and anti-pathogenic agents by the European starling. Oecologia 67: 169-176.
9. Clark L & Mason JR (1988) Effect of biologically active plants used as nest material and the derived benefit to starling nestlings. Oecologia 77: 174-180.
10. Coelho MLV, Nascimento JD, Fagundes PC, Madureira DJ, de Oliveira SS, Brito MAVP & Bastos MCFB (2007) Activity of staphylococcal bacteriocins against Staphylococcus aureus and Streptococcus agalactiae involved in bovine mastitis. Res Microbiol 158: 625-630.
11. Criado R, Gutierrez J, Martín M, Herranz C, Hernandez PE & Cintas LM (2006) Immunochemical characterization of temperature-regulated production of enterocin L50 (EntL50A and EntL50B), enterocin P, and enterocin Q by Enterococcus faecium L50. Appl Environ Microbiol 72: 7634-7643.
12. Desriac F, Defer D, Bourgougnon N, Brillet B, Le Chevalier P & Fleury Y (2010) Bacteriocin as weapons in the marine animal-associated bacteria warfare: inventory and potential applications as an aquaculture probiotic. Mar Drugs 8: 1153-1177.
13. Devi SM & Halami PM (2011) Detection and characterization of Pediocin PA-1/AcH like bacteriocin producing lactic acid bacteria. Curr Microbiol 63: 181-185.
14. Du Toit M, Franz CMAP, Dicks LMT & Holzapfel WH (2000) Preliminary characterization of bacteriocins produced by Enterococcus faecium and Enterococcus faecalis isolated from pig faeces. J Appl Microbiol 88: 482-494.
15. Franz CMAP, van Belkum MJ, Holzapfel WH, Abriouel H & Galvez A (2007) Diversity of enterococcal bacteriocins and their grouping in a new classification scheme. FEMS Microbiol Rev 31: 293-310.
16. Giraffa G, Carminati D & Neviani E (1997) Enterococci isolated from dairy products: a review of risks and potential technological use. J Food Prot 60: 732-737.
17. Gratia A & Fredericq P (1946) Diversité des souches antibiotiques de E. coli et étendue variable de leur champs d'action. CR Soc Biol 140: 1032-1033.
18. Gutiérrez J, Criado R, Citti R, Martín M, Herranz C, Nes IF, Cintas LM & Hernández PE (2005) Cloning, production and functional expression of enterocin P, a sec-dependent bacteriocin produced by Enterococcus faecium P13, in Escherichia coli. Int J Food Microbiol 103: 239-250.
19. Holtsmark I, Eijsink VGH & Brurberg MB (2008) Bacteriocins from plant pathogenic bacteria. FEMS Microbiol Lett 280: 1-7.
20. Jenssen H, Hamill P & Hancock REW (2006) Peptide antimicrobial agents. Clin Microbiol Rev 19: 491-511.
21. Lozano GA (1998) Parasitic stress and self-medication in wild animals. Adv Study Behav 27: 291-317.
22. Luders T, Birkemo GA, Fimland G, Nissen-Meyer J & Nes IF (2003) Strong synergy between a eukaryotic antimicrobial peptide and bacteriocins from lactic acid bacteria. Appl Environ Microbiol 69: 1797-1799.
23. Martínez-Bueno M, Valdivia E, Gálvez A, Coyette J & Maqueda M (1998) Analysis of the gene cluster involved in production and immunity of the peptide antibiotic AS-48 in Enterococcus faecalis. Mol Microbiol 27: 347-358.
24. Martín-Platero AM, Valdivia E, Ruiz-Rodríguez M, Soler JJ, Martín-Vivaldi M, Maqueda M & Martínez-Bueno M (2006) Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10-3, isolated from the uropygial gland of the hoopoe (Upupa epops). Appl Environ Microbiol 72: 4245-4249.
25. Martín-Platero AM, Valdivia E, Maqueda M & Martínez-Bueno M (2007) Fast, convenient and economical method for isolating genomic DNA from lactic acid bacteria using a modification of the protein "salting-out" procedure. Anal Biochem 366: 102-104.
26. Martín-Platero AM, Valdivia E, Maqueda M & Martínez-Bueno M (2009) Characterization and safety evaluation of enterococci isolated from Spanish goats' milk cheeses. Int J Food Microbiol 132: 24-32.
27. Martín-Vivaldi M, Ruiz-Rodríguez M, Soler JJ, Peralta-Sánchez JM, Méndez M, Valdivia E, Martín-Platero AM & Martínez-Bueno M (2009) Seasonal, sexual and developmental differences in hoopoe Upupa epops preen gland morphology and secretions: evidence for a role of bacteria. J Avian Biol 40: 191-205.
28. Martín-Vivaldi M, Peña A, Peralta-Sánchez JM, Sánchez L, Ananou S, Ruiz-Rodríguez M & Soler JJ (2010) Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc R Soc Lond B 277: 123-130.
29. McEntire JC, Montville TJ & Chikindas ML (2003) Synergy between nisin and select lactates against Listeria monocytogenes is due to the metal cations. J Food Prot 66: 1631-1636.
30. Mennerat A, Mirleau P, Blondel J, Perret P, Lambrechts M & Heeb P (2009) Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria. Oecologia 161: 849-855.
31. Moore J (2002) Parasites and the Behavior of Animals. Oxford University Press, Oxford.
32. Rajchard J (2010) Biologically active substances of bird skin: a review. Vet Med 55: 413-421.
33. Riley MA & Chavan MA (2007) Bacteriocins. Ecology and Evolution. Springer-Verlag, Heidelberg.
34. Riley MA & Wertz JE (2002) Bacteriocins: evolution, ecology and application. Annu Rev Microbiol 56: 117-137.
35. Ruiz-Rodríguez M, Valdivia E, Soler JJ, Martín-Vivaldi M, Martín-Platero AM & Martínez-Bueno M (2009) Symbiotic bacteria living in the hoopoe's uropygial gland prevent feather degradation. J Exp Biol 212: 3621-3626.
36. Ruiz-Rodríguez M, Valdivia E, Martín-Vivaldi M, Martín-Platero AM, Martínez-Bueno M, Méndez M, Peralta-Sánchez JM & Soler JJ (2012) Antimicrobial activity and genetic profile of Enteroccoci isolated from hoopoes uropygial gland. PLoS ONE 7: e41843.
37. Sánchez-Hidalgo M, Maqueda M, Gálvez A, Abriouel H, Valdivia E & Martínez-Bueno M (2003) The genes coding for enterocin EJ97 production by Enterococcus faecalis EJ97 are located on a conjugative plasmid. Appl Environ Microbiol 69: 1633-1641.
38. Sokal RR & Rohlf FJ (1995) Biometry. W. H. Freeman, San Francisco, CA, USA.
39. Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M, Peralta-Sánchez JM & Mendez M (2008) Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22: 864-871.
40. Soler JJ, Martín-Vivaldi M, Peralta-Sánchez JM & Ruiz-Rodríguez M (2010) Antibiotic-producing bacteria as a possible defence of birds against pathogenic microorganisms. Open Ornithol J 3: 93-100.
41. Statsoft I (2006) STATISTICA (data analysis software system), version 7.1. www.statsoft.com
42. Strompfová V, Laukova A, Simonova M & Marcinakova M (2008) Occurrence of the structural enterocin A, P, B, L50B genes in enterococci of different origin. Vet Microbiol 132: 293-301.
43. Williams JGK, Kubelik AR, Livak KJ, Rafalski JA & Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic-markers. Nucleic Acids Res 18: 6531-6535.