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<I>Bacillus Cereus</I> 2346 Journal of Food Protection, Vol. 70, No. 10, 2007, Pages 2346–2353 Copyright ᮊ, International Association for Food Protection Occurrence of Bacillus cereus Spores with a Damaged Exosporium: Consequences on the Spore Adhesion on Surfaces of Food Processing Lines C. FAILLE,1* G. TAUVERON,1 C. LE GENTIL-LELIE` VRE,1 AND C. SLOMIANNY2,3 1INRA-UR638, 369 rue Jules Guesde, BP 20039, F-59651 Villeneuve d’Ascq Cedex, France; 2INSERM-LPC, U-800, F-59655 Villeneuve d’Ascq Cedex, France; and 3Laboratoire de Physiologie Cellulaire, Universite´ des Sciences et Technologies de Lille 1, F-59655 Villeneuve d’Ascq Cedex, France Downloaded from http://meridian.allenpress.com/jfp/article-pdf/70/10/2346/1677253/0362-028x-70_10_2346.pdf by guest on 24 September 2021 MS 07-195: Received 10 April 2004/Accepted 14 May 2007 ABSTRACT This study was designed to evaluate the occurrence of Bacillus cereus spores with a damaged exosporium and the consequences of such damages on spore adhesion. The analysis of nine strains sporulated under optimal conditions (Spo8- agar, 30ЊC) revealed that damaged exosporia were systematically found in one strain (B. cereus D17) and occasionally in two others (B. cereus ATCC 14579T and B. cereus D6). The prevalence of spores with damaged exosporia increased when spor- ulation occurred under less favorable conditions (Spo8-broth or high temperature); for example, more than 50% of the B. cereus ATCC 14579T spores were damaged when sporulation occurred at 40ЊC on Spo8-agar or at 30ЊC in Spo8-broth. Furthermore, when subjected to shear stresses by circulation of spore suspensions through a peristaltic pump, the exosporium of a significant amount of spores became partially or totally shorn off (for example, 40% of the B. cereus ATCC 14579T spores). The ability of damaged spores to adhere to inert surfaces and to resist cleaning under shear stress was significantly affected when compared with intact spores, resulting in a decreased number of adhering spores (P Յ 0.004) and enhanced resistance to cleaning (P Յ 0.008). This study provides evidence that, under various conditions, the exosporium of B. cereus spores can be partly or wholly damaged, thereby affecting the ability of spores to contaminate the surfaces of food processing lines. The presence of spores devoid of exosporium will be of importance in determining the risk associated with B. cereus spores adherent to food processing line surfaces. Bacillus cereus spores are widespread in environments ed results remain controversial, and for the time being, it such as soil, air, and work surfaces or in food and are would seem difficult to conclude that appendages would known to be responsible for foodborne illness. These spores either inhibit or promote adhesion (16, 26). Conversely, the are highly resistant to most of the treatments devised by exosporium’s length has recently been shown to affect both food producers to limit bacterial survival and growth during the resistance of adherent spores to a cleaning procedure food processing and storage: spores can survive pasteuri- and, to a lesser extent, the number of adherent spores (29). zation or disinfection procedures (6, 14, 21) and adhere Most of these previous studies have been carried out firmly to inert surfaces (12), and some psychrotrophic on spores produced under favorable conditions, far from strains can even germinate and grow under refrigerated con- the conditions probably encountered by bacteria in the real ditions. environment, such as high or low temperatures and desic- Spores from B. cereus strains are enclosed in a loose- cation. However, many studies have dealt with the influence fitting outermost integument, called the exosporium, and of growth conditions on their surface properties and adhe- surrounded by appendages. The remarkable ability of B. sion of various microorganisms (4, 10, 22) or have reported cereus spores to adhere to inert surfaces and to resist clean- on the influence of sporulation conditions on other spore ing in place (CIP) procedures may arise from the specific properties, such as thermal resistance (18, 20), density (17), surface properties of exosporia and the presence of ap- or coat and cortex composition (19). Conversely, no find- pendages. Many studies have reported that some spore sur- ings have as yet been reported on the effect of sporulation face properties have an influence on the adhesion ability of conditions on spore surface and adhesion. Moreover, it has spores. The hydrophobic character of spores from strains belonging to the B. cereus species has often been reported not been demonstrated that the exosporium is strong to play an important part in their ability to firmly adhere to enough to resist those shear or friction stresses encountered stainless steel and other inert surfaces (8, 12). The presence by some mature spores in food processing lines. Indeed, of appendages has also been suggested to have an important few studies have been carried out on the influence of shear role in spore adhesion (1, 29). However, previously report- on cells; these studies have mainly dealt with biotechnology or medicine, and no data have been reported on bacterial * Author for correspondence. Tel: ϩ33 (0)3-20-43-54-04; Fax: ϩ33 (0)3- cells. For example, the damage to microalgal cells (13) or 20-43-54-26; E-mail: [email protected]. to plant cells (15) due to shear inside a pump was found J. Food Prot., Vol. 70, No. 10 DAMAGE TO B. CEREUS EXOSPORIUM 2347 to be dependent on the pump technology and on the time ultramicrotome (Applied Biosystems, Foster City, Calif.) and col- of exposure. lected on 100- or 150-mesh grids. After double-staining with 2% The aim of the present study was to demonstrate the uranyl acetate in 50% ethanol and lead citrate (23), the sections occurrence of B. cereus spores with a damaged exosporium were observed under a Hitachi H600 electron microscope at 75 when spores were produced under various sporulation con- kV. ditions (e.g., temperature sporulation, liquid-agar medium) Mechanical damage to spore exosporia through a test rig. or subjected to shear stresses such as those encountered by To evaluate the consequence of shear stress on the integrity of the mature spores during food processing. We then inves- exosporia, aqueous suspensions of 106 spores per ml (B. cereus tigated the incidence of the lack of exosporium on the abil- CUETM 98/4, 5832, and ATCC 14579T) were circulated through ity of spores to adhere to stainless steel surfaces and to a peristaltic pump (704S, Watson-Marlowe Limited, Falmouth, Њ Ϫ1 resist a cleaning procedure. Cornwall, UK) at 20 C for 4 h at a flow rate of 300 liters h . The test rig consisted of a vessel containing the spore suspension, the pump, a surge tank to limit pulse flow rate variations, and MATERIALS AND METHODS Downloaded from http://meridian.allenpress.com/jfp/article-pdf/70/10/2346/1677253/0362-028x-70_10_2346.pdf by guest on 24 September 2021 pipes made of Marpren (Watson-Marlowe) and silicon. For trans- Bacillus strains and spore production. Nine strains be- mission electron microscopy observations and determination of longing to the B. cereus species were analyzed in this study: the the percentage of spores with lost or injured exosporium, samples type strain (ATCC 14579T), three strains isolated from the envi- were taken after 4 h of circulation, and spores were pelleted by ronment (748, 5832, and LM9), one strain isolated from a dairy centrifugation at 3,500 ϫ g for 30 min at 4ЊC. processing line (CUETM 98/4), and four strains from patients with diarrheic symptoms (D1, D6, D17, and D23). Spores from Production of batches of spores devoid of exosporium. the nine strains were produced at 30ЊC on Spo8-agar consisting Spores from B. cereus CUETM 98/4 and 5832 (15 ml of an aque- 9 of 8 g literϪ1 nutrient broth (Biokar Diagnostics, Beauvais, ous spore suspension of 10 spores per ml) were subjected to three Ϫ1 Ϫ1 successive passages through a French press at 20,000 psi (SLM France), 0.51 g liter MgSO4·7H2O, 0.97 g liter KCl, 0.2 g literϪ1 CaCl ·2H O, 3 ϫ 10Ϫ3 g literϪ1 MnCl ·4H O, 0.55 ϫ 10Ϫ3 Instruments, Urbana, Ill.). The detached exosporia and appendages 2 2 2 2 ϫ g literϪ1 FeSO ·7H O, and 1.5% agar. When over 95% of spores were separated from spores by two centrifugations (3,000 g, 4 2 Њ were obtained, they were harvested by scraping the surface, 30 min, 4 C). The pellet, containing 100% spores devoid of intact Њ washed five times in chilled water (by centrifugation at 1,200 ϫ exosporium, was resuspended in chilled water and stored at 4 C g for 15 min), and stored at 4ЊC until use. until use. Within spore batches passed through the French press, Spores from B. cereus CUETM 98/4, 5832, and ATCC many spores were still surrounded with fragments of exosporium, 14579T were also produced under other conditions. Sporulation suggesting that the underlying coat remained intact. was performed on the Spo8-agar at the following temperatures: Microbial affinity to hexadecane. A partitioning method 15, 20, 40, and 45ЊC, in the way described above. Spores from was used, based on the affinity of spores to an apolar solvent, the three strains were also produced in Spo8-broth (same com- hexadecane (Sigma, St. Louis, Mo.) (3), and slightly modified in position as Spo8-agar, except that no agar was added) at 30ЊC. our laboratory. Briefly, a saline spore suspension was adjusted to When sporulation occurred in liquid medium, cells were activated an absorbance of 0.5 to 0.6 at 600 nm (A0) in glass tubes (10 mm by two successive transfers to nutrient agar slants and incubated in diameter by 75 mm).
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