Distribution and genetic diversity of bacteriocin gene clusters in rumen microbial genomes

Applied and Environmental Microbiology

Volumn 81, Issue 20, 2015, Pages 7290-7304

  Azevedo, Analice C ^a   Bento, Cláudia B P ^a   Ruiz, Jeronimo C ^b   Queiroz, Marisa V ^a   Mantovani, Hilário C ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BACTERIOLOGY; BIOCHEMISTRY; BIOSYNTHESIS; ENCODING (SYMBOLS); GENE ENCODING; GENETIC ENGINEERING; MICROORGANISMS; PEPTIDES; POLYPEPTIDES; PROTEINS;

ANTIMICROBIAL PEPTIDE; BACTERIAL SPECIES; BACTERIOCIN PRODUCTION; BIOSYNTHETIC GENE CLUSTER; OPEN READING FRAME; RUMINAL MICROORGANISMS; SCREENING PROCEDURES; STANDARDIZED METHODS;

GENES;

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOASSAY; GENE EXPRESSION; GENETIC DIFFERENTIATION; GENOME; PEPTIDE; POPULATION DISTRIBUTION; PROTEIN; RUMINANT; SPECIES DIVERSITY; STANDARDIZATION;

BACTERIA (MICROORGANISMS); RUMINOCOCCUS ALBUS; STREPTOCOCCUS;

BACTERIOCIN;

GENETICS; MICROBIAL GENOME; MULTIGENE FAMILY; STREPTOCOCCUS;

BACTERIOCINS; GENOME, MICROBIAL; MULTIGENE FAMILY; STREPTOCOCCUS;

EID: 84943279381     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01223-15     Document Type: Article

References (57)

1. Flaherty RA, Freed SD, Lee SW. 2014. The wide world of ribosomally encoded bacterial peptides. PLoS Pathog 10:e1004221. http://dx.doi.org/10.1371/journal.ppat.1004221.
2. Yang SC, Lin CH, Sung CT, Fang JY. 2014. Antibacterial activities of bacteriocins: application in foods and pharmaceuticals. Front Microbiol 5:241. http://dx.doi.org/10.3389/fmicb.2014.00241.
3. Cotter PD, Ross RP, Hill C. 2013. Bacteriocins-a viable alternative to antibiotics? Nat Rev Microbiol 11:95-105. http://dx.doi.org/10.1038/nrmicro2937.
4. Russell JB, Mantovani HC. 2002. The bacteriocins of ruminal bacteria and their potential as an alternative to antibiotics. J Mol Microbiol Biotechnol 4:347-355.
5. Blair JMA, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJV. 2015. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol 13:42-51. http://dx.doi.org/10.1038/nrmicro3380.
6. Cotter PD, Hill C, Ross RP. 2005. Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777-788. http://dx.doi.org/10.1038/nrmicro1273.
7. Heng NCK, Tagg JR. 2006. What's in a name? Class distinctions for bacteriocins. Nat Rev Microbiol, vol 4. http://dx.doi.org/10.1038/nrmicro1273-c1.
8. Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS, Bulaj G, Camarero JA, Campopiano DJ, Challis GL, Clardy J, Cotter PD, Craik DJ, Dawson M, Dittmann E, Donadio S, Dorrestein PC, Entian KD, Fischbach MA, Garavelli JS, Göransson U, Gruber CW, Haft DH, Hemscheidt TK, Hertweck C, Hill C, Horswill AR, Jaspars M, Kelly WL, Klinman JP, Kuipers OP, Link AJ, Liu W, Marahiel MA, Mitchell DA, Moll GN, Moore BS, Müller R, Nair SK, Nes IF, Norris GE, Olivera BM, Onaka H, Patchett ML, Piel J, Reaney MJT, Rebuffat S, Ross RP, Sahl H-G, Schmidt EW, Selsted ME, et al. 2013. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 30:108-160. http://dx.doi.org/10.1039/C2NP20085F.
9. Kjos M, Borrero J, Opsata M, Birri DJ, Holo H, Cintas LM, Snipen L, Hernández PE, Nes IF, Diep DB. 2011. Target recognition, resistance, immunity and genome mining of class II bacteriocins from Gram-positive bacteria. Microbiology 157:3256-3267. http://dx.doi.org/10.1099/mic.0.052571-0.
10. Nilsen T, Nes IF, Holo H. 2003. Enterolysin A, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. Appl Environ Microbiol 69:2975-2984. http://dx.doi.org/10.1128/AEM.69.5.2975-2984.2003.
11. Soomro AH, Masud T, Sammi S, Rathore HA. 2007. Comparison of different methods for detection of antimicrobial activity of Lactobacillus spp. Pakistan J Zool 39:265-268.
12. Wang H, Fewer DP, Sivonen K. 2011. Genome mining demonstrates the widespread occurrence of gene clusters encoding bacteriocins in cyanobacteria. PLoS One 6:e22384. http://dx.doi.org/10.1371/journal.pone.0022384.
13. Begley M, Cotter PD, Hill C, Ross RP. 2009. Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins. Appl Environ Microbiol 75:5451-5460. http://dx.doi.org/10.1128/AEM.00730-09.
14. Singh M, Sareen D. 2014. Novel LanT associated lantibiotic clusters identified by genome database mining. PLoS One 9:e91352. http://dx.doi.org/10.1371/journal.pone.0091352.
15. Rychlik JL, Russell JB. 2002. Bacteriocin-like activity of Butyrivibrio fibrisolvens JL5 and its effect on other ruminal bacteria and ammonia production. Appl Environ Microbiol 68:1040-1046. http://dx.doi.org/10.1128/AEM.68.3.1040-1046.2002.
16. Chen J, Weimer PJ. 2001. Competition among three predominant ruminal cellulolytic bacteria in the absence or presence of non-cellulolytic bacteria. Microbiology 147:21-30.
17. Joachimsthal EL, Reeves RKH, Hung J, Nielsen LK, Ouwerkerk D, Klieve AV, Vickers CE. 2010. Production of bacteriocins by Streptococcus bovis strains from Australian ruminants. J Appl Microbiol 108:428-436. http://dx.doi.org/10.1111/j.1365-2672.2009.04432.x.
18. Mantovani HC, Kam DK, Ha JK, Russell JB. 2001. The antibacterial activity and sensitivity of Streptococcus bovis strains isolated from the rumen of cattle. FEMS Microbiol Ecol 37:223-229. http://dx.doi.org/10.1111/j.1574-6941.2001.tb00869.x.
19. Pattnaik P, Grover S, Batish VK. 2005. Effect of environmental factors on production of lichenin, a chromosomally encoded bacteriocin-like compound produced by Bacillus licheniformis 26L-10/3RA. Microbiol Res 160: 213-218. http://dx.doi.org/10.1016/j.micres.2005.01.006.
20. Mantovani HC, Hu H, Warobo RW, Russell JB. 2002. Bovicin HC5, a bacteriocin from Streptococcus bovis HC5. Microbiology 148:3347-3352.
21. Whitford MF, McPherson MA, Forster RJ, Teather RM. 2001. Identification of bacteriocin-like inhibitors from rumen Streptococcus spp. and isolation and characterization of bovicin 255. Appl Environ Microbiol 67:569-574. http://dx.doi.org/10.1128/AEM.67.2.569-574.2001.
22. Kalmokoff ML, Lu D, Whitford MF, Teather RM. 1999. Evidence for production of a new lantibiotic (butyrivibriocin OR79A) by the ruminal anaerobe Butyrivibrio fibrisolvens OR79: characterization of the structural gene encoding butyrivibriocin OR79A. Appl Environ Microbiol 65:2128-2135.
23. Paiva AD, Fernandes KM, Dias RS, Rocha ADS, de Oliveira LL, Neves CA, de Paula SO, Mantovani HC. 2013. Safety evaluation of the antimicrobial peptide bovicin HC5 orally administered to a murine model. BMC Microbiol 13:69. http://dx.doi.org/10.1186/1471-2180-13-69.
24. Van Heel AJ, de Jong A, Montalbán-López M, Kok J, Kuipers OP. 2013. BAGEL3: automated identification of genes encoding bacteriocins and (non-)bactericidal posttranslationally modified peptides. Nucleic Acids Res 41:448-453. http://dx.doi.org/10.1093/nar/gkt391.
25. Medema MH, Blin K, Cimermancic P, De Jager V, Zakrzewski P, Fischbach MA, Weber T, Takano E, Breitling R. 2011. AntiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 39:W339-W346. http://dx.doi.org/10.1093/nar/gkr466.
26. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 2725-2729. http://dx.doi.org/10.1093/molbev/mst197.
27. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680. http://dx.doi.org/10.1093/nar/22.22.4673.
28. Heidrich C, Pag U, Josten M, Jack RW, Bierbaum G, Jung G, Metzger RG. 1998. Isolation, characterization, and heterologous expression of the novel lantibiotic epicidin 280 and analysis of its biosynthetic gene cluster. Appl Environ Microbiol 64:3140-3146.
29. Chen J, Stevenson DM, Weimer PJ. 2004. Albusin B, a bacteriocin from the ruminal bacterium Ruminococcus albus 7 that inhibits growth of Ruminococcus flavefaciens. Appl Environ Microbiol 70:3167-3170. http://dx.doi.org/10.1128/AEM.70.5.3167-3170.2004.
30. Baar C, Eppinger M, Raddatz G, Simon J, Lanz C, Klimmek O, Nandakumar R, Gross R, Rosinus A, Keller H, Jagtap P, Linke B, Meyer F, Lederer H, Schuster SC. 2003. Complete genome sequence and analysis of Wolinella succinogenes. Proc Natl Acad Sci U S A 100:11690-11695. http://dx.doi.org/10.1073/pnas.1932838100.
31. Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Conlon BP, Mueller A, Schaberle TF, Hughes DE, Epstein S, Jones M, Lazarides L, Steadman VA, Cohen DR, Felix CR, Fetterman KA, Millett WP, Nitti AG, Zullo AM, Chen C, Lewis K. 2015. A new antibiotic kills pathogens without detectable resistance. Nature 517:455-459. http://dx.doi.org/10.1038/nature14098.
32. Settanni L, Valmorri S, Suzzi G, Corsetti A. 2008. The role of environmental factors and medium composition on bacteriocin-like inhibitory substances (BLIS) production by Enterococcus mundtii strains. Food Microbiol 25:722-728. http://dx.doi.org/10.1016/j.fm.2008.01.011.
33. Delgado A, Arroyo López FN, Brito D, Peres C, Fevereiro P, GarridoFernández A. 2007. Optimum bacteriocin production by Lactobacillus plantarum 17.2b requires absence of NaCl and apparently follows a mixed metabolite kinetics. J Biotechnol 130:193-201. http://dx.doi.org/10.1016/j.jbiotec.2007.01.041.
34. Eijsink VH, Axelsson L, Diep D, Håvarstein L, Holo H, Nes I. 2002. Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie Van Leeuwenhoek 81: 639-654. http://dx.doi.org/10.1023/A:1020582211262.
35. Kalmokoff ML, Teather RM. 1997. Isolation and characterization of a bacteriocin (butyrivibriocin AR10) from the ruminal anaerobe Butyrivibrio fibrisolvens AR10: evidence in support of the widespread occurrence of bacteriocin-like activity among ruminal isolates of B. fibrisolvens. Appl Environ Microbiol 63:394-402.
36. Morovskỳ M, Pristas P, Javorskỳ P, Nes IF, Holo H. 2001. Isolation and characterization of enterocin BC25 and occurrence of the entA gene among ruminal gram-positive cocci. Microbiol Res 156:133-138. http://dx.doi.org/10.1078/0944-5013-00090.
37. Lauková A, Czikková S. 1998. Inhibition effect of enterocin CCM 4231 in the rumen fluid environment. Lett Appl Microbiol 26:215-218. http://dx.doi.org/10.1046/j.1472-765X.1998.00326.x.
38. Velásquez JE, Van der Donk WA. 2011. Genome mining for ribosomally synthesized natural products. Curr Opin Chem Biol 15:11-21. http://dx.doi.org/10.1016/j.cbpa.2010.10.027.
39. Claesen J, Bibb M. 2010. Genome mining and genetic analysis of cypemycin biosynthesis reveal an unusual class of posttranslationally modified peptides. Proc Natl Acad Sci U S A 107:16297-16302. http://dx.doi.org/10.1073/pnas.1008608107.
40. Flühe L, Marahiel MA. 2013. Radical S-adenosylmethionine enzyme catalyzed thioether bond formation in sactipeptide biosynthesis. Curr Opin Chem Biol 17:605-612. http://dx.doi.org/10.1016/j.cbpa.2013.06.031.
41. Rea MC, Sit CS, Clayton E, O'Connor PM, Whittal RM, Zheng J, Vederas JC, Ross RP, Hill C. 2010. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc Natl Acad Sci U S A 107:9352-9357. http://dx.doi.org/10.1073/pnas.0913554107.
42. Haft DH, Basu MK. 2011. Biological systems discovery in silico: radical S-adenosylmethionine protein families and their target peptides for posttranslational modification. J Bacteriol 193:2745-2755. http://dx.doi.org/10.1128/JB.00040-11.
43. Murphy K, O'Sullivan O, Rea MC, Cotter PD, Ross RP, Hill C. 2011. Genome mining for radical SAM protein determinants reveals multiple sactibiotic-like gene clusters. PLoS One 6:e20852. http://dx.doi.org/10.1371/journal.pone.0020852.
44. Lima JR, Ribon AOB, Russell JB, Mantovani HC. 2009. Bovicin HC5 inhibits wasteful amino acid degradation by mixed ruminal bacteria in vitro. FEMS Microbiol Lett 292:78-84. http://dx.doi.org/10.1111/j.1574-6968.2008.01474.x.
45. Zhang Q, Yu Y, Velasquez JE, van der Donk WA. 2012. Evolution of lanthipeptide synthetases. Proc Natl Acad Sci U S A 109:18361-18366. http://dx.doi.org/10.1073/pnas.1210393109.
46. Marsh AJ, O'Sullivan O, Ross RP, Cotter PD, Hill C. 2010. In silico analysis highlights the frequency and diversity of type 1 lantibiotic gene clusters in genome sequenced bacteria. BMC Genomics 11:679. http://dx.doi.org/10.1186/1471-2164-11-679.
47. Dirix G, Monsieurs P, Dombrecht B, Daniels R, Marchal K, Vanderleyden J, Michiels J. 2004. Peptide signal molecules and bacteriocins in Gram-negative bacteria: a genome-wide in silico screening for peptides containing a double-glycine leader sequence and their cognate transporters. Peptides 25:1425-1440. http://dx.doi.org/10.1016/j.peptides.2003.10.028.
48. Blin K, Kazempour D, Wohlleben W, Weber T. 2014. Improved lanthipeptide detection and prediction for antiSMASH. PLoS One 9:e89420. http://dx.doi.org/10.1371/journal.pone.0089420.
49. Lubelski J, Rink R, Khusainov R, Moll GN, Kuipers OP. 2008. Biosynthesis, immunity, regulation, mode of action and engineering of the model lantibiotic nisin. Cell Mol Life Sci 65:455-476. http://dx.doi.org/10.1007/s00018-007-7171-2.
50. Dischinger J, Josten M, Szekat C, Sahl HG, Bierbaum G. 2009. Production of the novel two-peptide lantibiotic lichenicidin by Bacillus licheniformis DSM 13. PLoS One 4:e6788. http://dx.doi.org/10.1371/journal.pone.0006788.
51. McClerren AL, Cooper LE, Quan C, Thomas PM, Kelleher NL, van der Donk WA. 2006. Discovery and in vitro biosynthesis of haloduracin, a two-component lantibiotic. Proc Natl Acad Sci U S A 103:17243-17248. http://dx.doi.org/10.1073/pnas.0606088103.
52. Klaenhammer T. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12:39-85. http://dx.doi.org/10.1016/0168-6445(93)90057-G.
53. Miron J, Morag E, Bayer EA, Lamed R, Ben-Ghedalia D. 1998. An adhesion-defective mutant of Ruminococcus albus SY3 is impaired in its capability to degrade cellulose. J Appl Microbiol 84:249-254. http://dx.doi.org/10.1046/j.1365-2672.1998.00336.x.
54. Kenters N, Henderson G, Jeyanathan J, Kittelmann S, Janssen PH. 2011. Isolation of previously uncultured rumen bacteria by dilution to extinction using a new liquid culture medium. J Microbiol Methods 84: 52-60. http://dx.doi.org/10.1016/j.mimet.2010.10.011.
55. Wang HT, Yu C, Hsieh YH, Chen SW, Chen BJ, Chen CY. 2011. Effects of albusin B (a bacteriocin) of Ruminococcus albus 7 expressed by yeast on growth performance and intestinal absorption of broiler chickens-its potential role as an alternative to feed antibiotics. J Sci Food Agric 91: 2338-2343. http://dx.doi.org/10.1002/jsfa.4463.
56. Nigutova K, Morovsky M, Pristas P, Teather RM, Holo H, Javorsky P. 2007. Production of enterolysin A by rumen Enterococcus faecalis strain and occurrence of enlA homologues among ruminal Gram-positive cocci. J Appl Microbiol 102:563-569.
57. Lee SS, Hsu JT, Mantovani HC, Russell JB. 2002. The effect of bovicin HC5, a bacteriocin from Streptococcus bovis HC5, on ruminal methane production in vitro. FEMS Microbiol Lett 217:51-55. http://dx.doi.org/10.1111/j.1574-6968.2002.tb11455.x.