Biofilm formation on stainless steel by Streptococcus thermophilus UC8547 in milk environments is mediated by the proteinase PrtS

Applied and Environmental Microbiology

Volumn 83, Issue 8, 2017, Pages

  Bassi, D ^a   Cappa, F ^a   Gazzola, S ^a   Orru L ^b   Cocconcelli, P S ^a  

^a UNIVERSITÀ CATTOLICA DEL SACRO CUORE   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

Author keywords

Biofilm; Genome; Milk; PrtS; Stainless steel; Streptococcus thermophilus

Indexed keywords

BIOFILMS; DAIRIES; GENE TRANSFER; GENES; PROTEINS; STRAIN;

BIOFILM FORMATION; CHEESE MANUFACTURING; ECOLOGICAL BENEFITS; ENVIRONMENTAL CONDITIONS; HIGH FREQUENCY HF; MILK; PRTS; STREPTOCOCCUS THERMOPHILUS;

STAINLESS STEEL;

BACTERIUM; BIOFILM; ENVIRONMENTAL CONDITIONS; ENZYME; ENZYME ACTIVITY; GENE; GENE TRANSFER; GENOME; GENOMICS; MILK; PERSISTENCE; PHENOTYPE; PROTEIN; STEEL; SURVIVAL;

STREPTOCOCCUS THERMOPHILUS;

BACTERIAL PROTEIN; MILK PROTEIN; PRTS PROTEIN, STREPTOCOCCUS THERMOPHILUS; SERINE PROTEINASE; STAINLESS STEEL;

ANIMAL; BACTERIAL GENOME; BIOFILM; CELL WALL; CHEMISTRY; ENZYMOLOGY; GENETICS; GENOMIC ISLAND; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MILK; PHYSIOLOGY; STREPTOCOCCUS THERMOPHILUS;

ANIMALS; BACTERIAL PROTEINS; BIOFILMS; CELL WALL; GENOME, BACTERIAL; GENOMIC ISLANDS; MILK; MILK PROTEINS; SERINE ENDOPEPTIDASES; STAINLESS STEEL; STREPTOCOCCUS THERMOPHILUS;

EID: 85016644428     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02840-16     Document Type: Article

References (37)

1. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, Decaris B, Bolotin A, Delorme C, Ehrlich SD, Guédon E, Monnet V, Renault P, Kleerebezem M. 2005. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev 29:435-463. https://doi.org/10.1016/j.femsre.2005.04.008.
2. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas S, Lapidus A, Goltsman E, Mazur M, Pusch GD, Fonstein M, Overbeek R, Kyprides N, Purnelle B, Prozzi D, Ngui K, Masuy D, Hancy F, Burteau S, Boutry M, Delcour J, Goffeau A, Hols P. 2004. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 22:1554-1558. https://doi.org/10.1038/nbt1034.
3. Makarova KS, Koonin EV. 2007. Evolutionary genomics of lactic acid bacteria. J Bacteriol 189:1199-1208. https://doi.org/10.1128/JB.01351-06.
4. Rasmussen TB, Danielsen M, Valina O, Garrigues C, Johansen E, Pedersen MB. 2008. Streptococcus thermophilus core genome: comparative genome hybridization study of 47 strains. Appl Environ Microbiol 74: 4703-4710. https://doi.org/10.1128/AEM.00132-08.
5. Fernandez-Espla MD, Garault P, Monnet V, Rul F. 2000. Streptococcus thermophilus cell wall-anchored proteinase: release, purification, and biochemical and genetic characterization. Appl Environ Microbiol 66: 4772-4778. https://doi.org/10.1128/AEM.66.11.4772-4778.2000.
6. Dandoy D, Fremaux C, de Frahan MH, Horvath P, Boyaval P, Hols P, Fontaine L. 2011. The fast milk acidifying phenotype of Streptococcus thermophilus can be acquired by natural transformation of the genomic island encoding the cell-envelope proteinase PrtS. Microb Cell Fact 10:S21. https://doi.org/10.1186/1475-2859-10-S1-S21.
7. Selle K, Klaenhammer TR, Barrangou R. 2015. CRISPR-based screening of genomic island excision events in bacteria. Proc Natl Acad Sci U S A 112:8076-8081. https://doi.org/10.1073/pnas.1508525112.
8. Delorme C, Bartholini C, Bolotine A, Dusko Ehrlich S, Renault P. 2010. Emergence of a cell wall protease in the Streptococcus thermophilus population. Appl Environ Microbiol 76:451-460. https://doi.org/10.1128/AEM.01018-09.
9. Couvigny B, Thérial C, Gautier C, Renault P, Briandet R, Guédon E. 2015. Streptococcus thermophilus biofilm formation: a remnant trait of ancestral commensal life? PLoS One 10:e0128099. https://doi.org/10.1371/journal.pone.0128099.
10. de Jong P, te Giffel MC, Kiezebrink EA. 2002. Prediction of the adherence, growth and release of microorganisms in production chains. Int J Food Microbiol 74:13-25. https://doi.org/10.1016/S0168-1605(01)00713-9.
11. Knight GC, Nicol RS, McMeekin TA. 2004. Temperature step changes: a novel approach to control biofilms of Streptococcus thermophilus in a pilot plant-scale cheese-milk pasteurisation plant. Int J Food Microbiol 93:305-318. https://doi.org/10.1016/j.ijfoodmicro.2003.11.013.
12. Hup G, Bangma A, Stadhouders J, Bouman S. 1980. Growth of thermoresistant streptococci in cheese-milk pasteurisers: I. Some observations in cheese factories. North Eur Dairy J 46:245-251.
13. Hood SK, Zottola ZE. 1995. Biofilms in food processing. Food Control 6:9-18. https://doi.org/10.1016/0956-7135(95)91449-U.
14. Palmer J, Flint S, Brooks J. 2007. Bacterial cell attachment, the beginning of a biofilm. J Ind Microbiol Biotechnol 34:577-588. https://doi.org/10.1007/s10295-007-0234-4.
15. Lortal S, Di Blasi A, Madec MN, Pediliggieri C, Tuminello L, Tanguy G, Fauquant J, Lecuona Y, Campo P, Carpino S, Licitra G. 2009. Tina wooden vat biofilm: a safe and highly efficient lactic acid bacteria delivering system in PDO Ragusano cheese making. Int J Food Microbiol 132:1-8. https://doi.org/10.1016/j.ijfoodmicro.2009.02.026.
16. Scatassa ML, Gaglio R, Macaluso G, Francesca N, Randazzo W, Cardamone C, Grigoli Di A, Moschetti G, Settanni L. 2015. Transfer, composition and technological characterization of the lactic acid bacterial populations of the wooden vats used to produce traditional stretched cheeses. Food Microbiol 52:31-41.
17. Vescovo M, Morelli L, Bottazzi V, Gasson MJ. 1983. Conjugal transfer of broad-host-range plasmid pam31 into enteric species of lactic acid bacteria. Appl Environ Microbiol 46:753-755.
18. Clewell DB, Yagi Y, Dunny GM, Schultz SK. 1974. Characterization of three plasmid deoxyribonucleic acid molecules in a strain of Streptococcus faecalis: identification of a plasmid determining erythromycin resistance. J Bacteriol 117:283-289.
19. Rabe M, Verdes D, Seeger S. 2011. Understanding protein adsorption phenomena at solid surfaces. Adv Colloid Interface Sci 162:87-106. https://doi.org/10.1016/j.cis.2010.12.007.
20. Hedberg Y, Karlsson ME, Blomberg E, Odnevall Wallinder I, Hedberg J. 2014 Correlation between surface physicochemical properties and the release of iron from stainless steel AISI 304 in biological media. Colloids Surf B Biointerfaces 122:216-222. https://doi.org/10.1016/j.colsurfb.2014.06.066.
21. Kim JC, Lund DB. 1998. Milk protein/stainless steel interaction relevant to the initial stage of fouling in thermal processing. J Food Process Eng 21:369-386. https://doi.org/10.1111/j.1745-4530.1998.tb00459.x.
22. Barnes L-M, Lo MF, Adams MR, Chamberlain AHL. 1999. Effect of milk proteins on adhesion of bacteria to stainless steel surfaces. Appl Environ Microbiol 65:4543-4548.
23. Al-Makhlafi H, Nasir A, Mcguire J, Daeschel M. 1995. Adhesion of Listeria monocytogenes to silica surfaces after sequential and competitive adsorption of bovine serum albumin and beta-lactoglobulin. Appl Environ Microbiol 61:2013-2015.
24. Stingele F, Neeser JR, Mollet B. 1996. Identification and characterization of the eps (exopolysaccharide) gene cluster from Streptococcus thermo-philus Sfi6. J Bacteriol 178:1680-1690. https://doi.org/10.1128/jb.178.6.1680-1690.1996.
25. Habimana O, Le Goff C, Juillard V, Bellon-Fontaine MN, Buist G, Kulakauskas S, Briandet R. 2007. Positive role of cell wall anchored proteinase PrtP in adhesion of lactococci. BMC Microbiol 7:36. https://doi.org/10.1186/1471-2180-7-36.
26. Reniero R, Cocconcelli P, Bottazzi V, Morelli L. 1992. High frequency of conjugation in Lactobacillus mediated by an aggregation-promoting factor. J Gen Microbiol 138:763-768. https://doi.org/10.1099/00221287-138-4-763.
27. van der Lelie D, Chavarri F, Venema G, Gasson MJ. 1991. Identification of a new genetic determinant for cell aggregation associated with lactose plasmid transfer in Lactococcus lactis. Appl Environ Microbiol 57:201-206.
28. Dunny GM, Leonard BAB, Hedberg PJ. 1995. Pheromone-inducible conjugation in Enterococcus faecalis: interbacterial and host-parasite chemical communication. J Bacteriol 177:871-876.
29. Luo H, Wan K, Wang HH. 2005. High-frequency conjugation system facilitates biofilm formation and pAMbeta1 transmission by Lactococcus lactis. Appl Environ Microbiol 71:2970-2978. https://doi.org/10.1128/AEM.71.6.2970-2978.2005.
30. Huggins AR, Sandine WE. 1984. Differentiation of fast and slow milkcoagulating isolates in strains of lactic streptococci. J Dairy Sci 67: 1674-1679. https://doi.org/10.3168/jds.S0022-0302(84)81491-5.
31. Leloup L, Ehrlich SD, Zagorec M, Morel-Deville F. 1997. Single-crossover integration in the Lactobacillus sakei chromosome and insertional inactivation of the ptsI and lacL genes. Appl Environ Microbiol 63:2117-2123.
32. Marciset O, Mollet B. 1994. Multifactorial experimental design for optimizing transformation: electroporation of Streptococcus thermophilus. Biotechnol Bioeng 43:490-496. https://doi.org/10.1002/bit.260430609.
33. Vandecasteele SJ, Peetermans WE, Merckx R, Van Ranst M, Van Eldere J. 2002 Use of gDNA as internal standard for gene expression in staphylococci in vitro and in vivo. Biochem Biophys Res Commun 291:528-534. https://doi.org/10.1006/bbrc.2002.6465.
34. Rosenberg M, Gutnick D, Rosenberg E. 1980. Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29-33. https://doi.org/10.1111/j.1574-6968.1980.tb05599.x.
35. Palumbo E, Favier CF, Deghorain M, Cocconcelli PS, Grangette C, Mercenier A, Vaughan EE, Hols P. 2004. Knockout of the alanine racemase gene in Lactobacillus plantarum results in septation defects and cell wall perforation. FEMS Microbiol Lett 233:131-138. https://doi.org/10.1016/j.femsle.2004.02.001.
36. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821-829. https://doi.org/10.1101/gr.074492.107.
37. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75.