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(Actinobacillus) Actinomycetemcomitans J Ind Microbiol Biotechnol (2008) 35:103–110 DOI 10.1007/s10295-007-0271-z ORIGINAL PAPER Actinomycetemcomitin: a new bacteriocin produced by Aggregatibacter (Actinobacillus) actinomycetemcomitans Francisca Lúcia Lima · Maria Auxiliadora Roque de Carvalho · Ana Carolina Morais Apolônio · Marcelo Porto Bemquerer · Marcelo Matos Santoro · Jamil Silvano Oliveira · Celuta Sales Alviano · Luiz de Macêdo Farias Received: 9 July 2007 / Accepted: 18 October 2007 / Published online: 8 November 2007 © Society for Industrial Microbiology 2007 Abstract Aggregatibacter (Actinobacillus) actinomyce- has a molecular mass of 20.3 KDa and it represents a new temcomitans P7–20 strain isolated from a periodontally bacteriocin from A. actinomycetemcomitans. diseased patient has produced a bacteriocin (named as actinomycetemcomitin) that is active against Peptostrepto- Keywords Aggregatibacter (Actinobacillus) coccus anaerobius ATCC 27337. Actinomycetemcomitin actinomycetemcomitans · Bacteriocin · was produced during exponential and stationary growth Actinomycetemcomitin phases, and its amount decreased until it disappeared during the decline growth phase. It was puriWed by ammonium sul- phate precipitation (30–60% saturation), and further by Introduction FPLC (mono-Q ionic exchange and Phenyl Superose hydrophobic interaction) and HPLC (C-18 reversed-phase). Aggregatibacter (formerly Actinobacillus) actinomycetem- This bacteriocin loses its activity after incubation at a pH comitans is a microorganism associated with various below 7.0 or above 8.0, following heating for 30 min at diseases, particularly early-onset periodontitis [27, 35, 40, 45°C, and after treatment with proteolytic enzymes such as 33]. This microorganism produces a number of virulence trypsin, -chymotrypsin, and papain. Actinomycetemcomitin factors, including LPS, adhesins, leukotoxin, colagenase and invasins [11, 36]. The relationship between A. actinomycetemcomitans and F. L. Lima · C. S. Alviano Instituto de Microbiologia Prof. Paulo de Góes, other oral microorganisms is complex and currently of Centro de Ciências da Saúde, Universidade Federal much interest [36, 37, 40]. Positive associations between do Rio de Janeiro, Rio de Janeiro, RJ, Brazil A. actinomycetemcomitans and oral microbiota have been reported, including a close relationship with species of F. L. Lima · M. A. R. de Carvalho · A. C. M. Apolônio · L. de Macêdo Farias (&) Capnocytophaga and Eikenella corrodens [2, 31]. Also, a Departamento de Microbiologia, Instituto de Ciências Biológicas, negative association has been reported with A. actinomyce- Universidade Federal de Minas Gerais, temcomitans and Streptococcus sanguinis [19, 20, 25, 37]. Belo Horizonte, MG, Brazil The ability of A. actinomycetemcomitans to produce a e-mail: [email protected] bacteriocin (actinobacillin) was established by Hammond M. P. Bemquerer · M. M. Santoro · J. S. Oliveira et al. [16], and this inhibitory factor was active against S. Departamento de Bioquímica e Imunologia, sanguinis strains, Streptococcus uberis FDC 1 and Actino- Instituto de Ciências Biológicas, Universidade Federal myces viscosus T14, as well as against other A. actinomyce- de Minas Gerais, Belo Horizonte, MG, Brazil temcomitans strains. It is expected that this substance F. L. Lima would be involved in the relationship between A. actinomy- Universidade Estadual do Piauí, Teresina, PI, Brazil cetemcomitans and other oral microorganisms. To study the bactericin action and its characteristics, one M. P. Bemquerer W X Embrapa Recursos Genéticos e Biotecnologia. must rst understand its production, which may be in uenced Parque Estação Biológica-PqEB, Brasília, DF, Brazil by methodological factors such as medium composition, 123 104 J Ind Microbiol Biotechnol (2008) 35:103–110 incubation atmosphere, pH and temperature [4, 23]. The Bacteriocin-like activity assay and protein determinations production is also inXuenced by the growth phase of the microorganism [1, 5, 7, 29]. Although for some bacteria, Bacteriocin activity was assayed by the agar diVusion such as for Enterococcus faecium, the production of bacte- method, and the bacteriocin titer was determined by the riocin has been detected during all growth phases [21, 34], serial dilution method, as previously described [3, 26]. Ali- for other microorganisms, this production has been detected quots of Wltrate extracts were serially twofold diluted with just in a speciWc growth phase, such as for A. actinomyce- sterilized ultra-pure water in microtitration plates (Mic- temcomitans [38], Lactobacillus acidophilus IBB 801 [41] rower Plate 96F). Aliquots of Wltrate extracts (20, 10 or and Bacillus thuringiensis BMG 1.7 [6], in which the pro- 5 l, depending on the puriWcation step) were spotted onto duction occurred at the stationary phase. the surface of the media. After absorption of the extract, the The bacteriocin previously reported by Hammond et al. Petri dishes were overlaid with 4 ml TSB-S soft agar [16] was puriWed and its molecular mass was determined to (0.7%) that had been inoculated with 0.2 ml of a 24-h TSB- be 120 KDa, with two subunits of 50 and 70 KDa [38]. It S culture of P. anaerobius ATCC 27337. The plates were has also been shown that A. Actinomycetemcomitans strains incubated at 37°C for 24–48 h in an anaerobic chamber W recovered from marmosets (Callithrix penicillata) produce (85% N2, 10% H2 and 5% CO2, Forma Scienti c Co., antagonistic substances that have the properties of bacterio- USA), and the titer was deWned as 2n, where n is the recip- cins and haemolysins [28]. rocal of the highest dilution that resulted in inhibition of the Recently, Lima et al. [22] observed in vitro a wide spec- indicator strain. Thus, the arbitrary unit (AU) of antibacte- trum of activity against Gram-positive and Gram-negative rial activity per milliliter (AU ml¡1) was deWned as bacteria and suggested that more than one bacteriocin is 2n £ 1000 l £ l¡1, where is the volume of bacteriocin produced by A. actinomycetemcomitans. To conWrm this used in the test. The protein measurements were determined hypothesis, the aim of the present investigation was to according to Lowry et al. [24]. Bovine serum albumin purify a novel bacteriocin from a strain of A. actinomyce- (BSA) was used as a standard. temcomitans isolated from human periodontal disease. Kinetics of bacteriocin production Materials and methods TSB-S medium (300 ml) was inoculated with a 24 h culture 6 W of A. actinomycetemcomitans P7.20 strain (10 CFU/ml nal Bacterial strains and culture media concentration) and incubated in anaerobic medium up to 96 h at 37°C. During this period, aliquots were taken up to A. actinomycetemcomitans P7.20, isolated from the measure the absorbance at 600 nm. The bacteriocin-like periodontal pocket of a patient with progressive rapid activity was measured at 18, 24, 36, 48, 72 and 96 h of periodontitis, was used to obtain the bacteriocin for this growth. At each time point, the cultures were centrifuged at study. This strain, previously screened for antagonistic 2,500 g for 10 min (Sorvall RC5C Instruments Du Pont), activity, showed a wide spectrum of activity against both and the supernatant was Wltered (0.22 m, Millipore). A. Gram-negative and -positive bacteria, and the antagonis- actinomycetemcomitans cells (sediment) recovered after tic substance presented a proteic nature [22]. Pepto- centrifugation were washed three times in Tris–HCl buVer, streptococcus anaerobius ATCC 27337, Bacteroides pH 8.0 (Sigma), sonicated (Branson SoniWer 450) for merdae ATCC 43184, L. casei ATCC 7469, F. nucleatum 10 min, with 20 cycles of 30 s at 50 W in an ice bath, and P12.2, M5.7, P. gingivalis ATCC 33277, S. sanguinis ultra-centrifuged for 1 h to obtain the intracellular fraction. ATCC 10557, and S. uberis ATCC 9927 were used as The supernatants and intracellular fractions were lyophi- indicator strains. The culture was routinely stored at lized (Freeze Dry System-Labconco), and then diluted in ¡86°C in tryptic-soy broth media (Difco) supplemented 0.01 M Tris–HCl to achieve 1 mg ml¡1. Subsequently, with 0.5% yeast extract and 10% glycerol (TSB-S), pH 50 l were spotted onto TSA-S and assayed as described 7.2. TSB-S supplemented with 0.5% yeast extract, 0.1% above. L-cystine (Difco), and 0.04% sodium bicarbonate (Difco), pH 8.0 was used to produce bacteriocin. The Production of the crude extract assay to evaluate the bacteriocin-like activity was deter- mined via the double-layer method using tryptic-soy A. actinomycetemcomitans P7.20 strain was cultured in agar media (Difco) supplemented as cited above, and 50 ml TSB-S for 24 h at 37°C in an anaerobic chamber. soft TSB agar (0.7%) supplemented with 0.5% yeast Next, the culture was inoculated in 950 ml TSB-S, and extract (Difco), 0.005% hemin (Difco) and 0.001% men- incubated for a further 24 h under the same conditions. The adione (TSA-S; Difco). culture was centrifuged at 2,500 g for 20 min at 4°C (Sorvall 123 J Ind Microbiol Biotechnol (2008) 35:103–110 105 RC5C Instruments Du Pont), and the cells were washed pyroglutamate aminopeptidase in 50 mM Na phosphate thrice with 0.01 M Tris–HCl buVer, pH 8.0. After washing, buVer, pH 7.0, containing 10 mM dithiothreitol and 10 mM the cells were suspended in 20 ml of the same buVer and ethylenediaminetetraacetic acid (EDTA) at 50°C for 6 h. sonicated (Branson SoniWer 450) for 10 min, with 20 cycles The N-terminal amino acid sequences of the S-pyridyl- of 30 s at 50 W in an ice bath. Cellular disruption was veri- ethylated intact proteins (2–10 nmol)
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