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ABSTRACT: The use of compounds produced by symbiotic bacteria against pathogens in animals is one of the most exciting discoveries in ecological immunology. The study of those antibiotic metabolites will enable an understanding of the defensive strategies against pathogenic infections. Here, we explore the role of bacteriocins explaining the antimicrobial properties of symbiotic bacteria isolated from the uropygial gland of the hoopoe (Upupa epops). The antagonistic activity of 187 strains was assayed against eight indicator bacteria, and the presence of six bacteriocin genes was detected in the genomic DNA. The presence of bacteriocin genes correlated with the antimicrobial activity of isolates. The most frequently detected bacteriocin genes were those encoding for the MR10 and AS-48 enterocins, which confer the highest inhibition capacity. All the isolates belonged to the genus Enterococcus, with E. faecalis as the most abundant species, with the broadest antimicrobial spectrum and the highest antagonistic activity. The vast majority of E. faecalis strains carried the genes of MR10 and AS-48 in their genome. Therefore, we suggest that fitness-related benefits for hoopoes associated with harbouring the most bactericidal symbionts causes the highest frequency of strains carrying MR10 and AS-48 genes. The study of mechanisms associated with the acquisition and selection of bacterial symbionts by hoopoes is necessary, however, to reach further conclusions. This article is protected by copyright. All rights reserved.
FEMS Microbiology Ecology 04/2013; · 3.41 Impact Factor
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ABSTRACT: A set of 80 Lactobacillus strains (36 Lactobacillus plantarum and 44 Lactobacillus paracasei) isolated from Spanish farmhouse cheeses have been studied as to their functional and safety properties and their survival under gut-related conditions. None of these 80 Lactobacillus strains were able to hydrolyse starch. A high percentage of L. plantarum and L. paracasei strains were, however, capable of hydrolysing casein (86.1% and 68.2% respectively). For the other characteristics investigated, L. plantarum strains generally had more positive responses than L. paracasei. The latter strains tested negative for most of these characteristics, with the exception of stachyose hydrolysis, which was positive in six strains of L. paracasei. A high percentage (91.7%) of L. plantarum produced haemo-dependent catalase. Phytase was present in 10 L. plantarum and in 2 L. paracasei. Most L. plantarum (83.3%) but no L. paracasei hydrolysed bile salts. All strains were completely resistant to a challenge of pH3, but many showed a loss of viability after a subsequent exposure to 0.3% oxgall; in fact, only one L. paracasei strain and 33 L. plantarum strains (91.67%) were tolerant to both stresses. L. plantarum Mb25 and L. plantarum Mb26 were the most adherent to Caco-2 cells (adherence percentages of 36 and 7% respectively). These two strains were also the most adherent to HeLa 229 cells, with 19.3 and 16.0% adhesion respectively. The Mb26 strain inhibited the adhesion of Listeria monocytogenes to Caco-2 cells when added simultaneously to Listeria and also when added 1h before the pathogen (21.0% and 51.6% adhesion inhibition, respectively). Production of H2O2 was detected in 38.9% of L. plantarum strains and in 9.1% of L. paracasei. Twelve L. plantarum and eight L. paracasei strains produced bacteriocin-like inhibitors. PCR amplifications of several plantaricin genes suggest that all the bacteriocinogenic strains may produce plantaricin E/F and some may also manufacture the plantaricin J/K. The nine L. plantarum strains assayed for antibiotic resistance were resistant to ciprofloxacin (MIC>2μg/ml), vancomycin (MIC>16μg/ml), and teicoplanin (MIC>16μg/ml). Moreover, some strains showed intermediate resistance to penicillin, tetracycline, rifampicin, and levofloxacin. We conclude that farmhouse cheeses are good sources of biotechnologically relevant lactobacilli and that the L. plantarum species shows better biotechnological properties than L. paracasei. This can be deduced from the finding of a high percentage of strains of L. plantarum that exhibit remarkable functional and inhibitory properties and high abilities to survive in gut-related conditions, which can be further developed for biotechnological applications.
International journal of food microbiology 03/2013; 163(2-3):136-145. · 3.01 Impact Factor
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ABSTRACT: Potentially, pathogenic bacteria are one of the main infective agents against which a battery of chemical and physical barriers has evolved in animals. Among these are the secretions by the exocrine uropygial gland in birds. The antimicrobial properties of uropygial secretions may prevent colonization and growth of microorganisms on feathers, skin and eggshells. However, uropygial gland secretions also favour the proliferation of feather mites that feed on secretions and microorganisms living on feathers that would otherwise reach eggshells during incubation if not consumed by feather mites. Therefore, at the interspecific level, uropygial gland size (as an index of volume of uropygial secretion) should be positively related to eggshell bacterial load (i.e. the risk of egg infection), whereas eggshell bacterial loads may be negatively related to abundance of feather mites eating bacteria. Here, we explore these previously untested predictions in a comparative framework using information on eggshell bacterial loads, uropygial gland size, diversity and abundance of feather mites and hatching success of 22 species of birds. The size of the uropygial gland was positively related to eggshell bacterial loads (mesophilic bacteria and Enterobacteriaceae), and bird species with higher diversity and abundance of feather mites harboured lower bacterial density on their eggshells (Enterococcus and Staphylococcus), in accordance with the hypothesis. Importantly, eggshell bacterial loads of mesophilic bacteria, Enterococcus and Enterobacteriaceae were negatively associated with hatching success, allowing us to interpret these interspecific relationships in a functional scenario, where both uropygial glands and mutualistic feather mites independently reduce the negative effects of pathogenic bacteria on avian fitness.
Journal of Evolutionary Biology 07/2012; 25(9):1779-91. · 3.28 Impact Factor
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ABSTRACT: Enterococcus faecalis UGRA10, a new AS-48-producer strain, has been isolated from a Spanish sheep's cheese. The inhibitory substance produced by E. faecalis UGRA10 was purified and characterized using matrix-assisted laser desorption ionization-time of flight mass spectrometry, confirming its identity with AS-48 enterocin (7.150 Da). Subsequent genetic analysis showed the existence of the as-48 gene cluster on a plasmid of approximately 70-kb. The UGRA10 strain was examined for safety properties such as enterococci virulence genes, biogenic amine production, and antibiotic resistance. As for most E. faecalis strains, PCR amplification revealed the existence of gene encoding for GelE, Asa1, Esp, EfaA, and Ace antigens and for tyrosine decarboxylase. This strain was sensitive to most of the antibiotics tested, being resistant only to aminoglycosides, lincosamide, and pristinamicins. In addition, UGRA10 developed an ability to form biofilms and to adhere to Caco 2 and HeLa 229 cells. More interestingly, this strain shows a high ability to interfere with the adhesion of Listeria monocytogenes to Caco 2 cells. Altogether, the results suggest that this broad-spectrum bacteriocin-producing strain has biotechnological potential to be developed as a protective agent in food preservation and as a probiotic.
Food Microbiology 05/2012; 30(1):59-67. · 3.28 Impact Factor
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ABSTRACT: The F420 strain, isolated from raw goat milk and identified as Enterococcus hirae, was selected because of its strong activity against gram-positive bacteria, including Listeria monocytogenes. Interestingly, the F420 strain lacks the virulence genes and decarboxylase activity of histidine, lysine, and ornithine, and it is susceptible to 11 of 14 tested antibiotics, including vancomycin. The antimicrobial compounds produced by E. hirae F420 strain showed high resistance to heat treatment and to acidic and basic pHs. The MALDI-TOF mass spectrometry analysis coupled with the sequence of peptide and structural gene analysis of one of the purified enterocins showed 100% identity with enterocin P (EntP), previously described in E. faecium strains. The structural gene for EntP is located on a plasmid of 65 kb. Other enterocins with molecular mass higher than 7 kDa were also detected. This is the first report of the production of EntP by E. hirae species naturally occurring in foods. The biotechnological characteristics of the F420 strain and its enterocins indicate their potential for application in the control of L. monocytogenes and other undesirable bacteria in food systems.
Canadian Journal of Microbiology 04/2012; 58(5):596-604. · 1.36 Impact Factor
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ABSTRACT: Enterocin AS-48 is a cationic cyclic bacteriocin produced by Enterococcus faecalis with broad bactericidal activity. Currently we are assaying the efficacy of AS-48 as biopreservative in foods. In this work we have applied the spray drying process to different AS-48 liquid samples to obtain active dried preparations. We have also assayed different methods, heat, UV irradiation and filtration, to inactivate/remove the AS-48 producer cells from the samples. Best results were obtained for the sample from CM-25 cation exchange, for which it was also possible to completely eliminate/inactivate the producer cells by heat or UV irradiation without loss of activity. When added at 0.016% or 5% to Brain Heart Infusion broth or to skim milk, respectively, the AS-48 powder caused early and complete inactivation of Listeria monocytogenes. A partial inhibition of Staphylococcus aureus was achieved in broth and in skim milk supplemented with 2.5% and 10% AS-48 powder, respectively.
Food Microbiology 02/2010; 27(1):58-63. · 3.28 Impact Factor
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ABSTRACT: Among potential agents that might damage bird feathers are certain microorganisms which secrete enzymes that digest keratin, as is the case of the ubiquitous bacterium Bacillus licheniformis, present in both the feathers and skin of wild birds. It is therefore a good candidate for testing the effects of bird defences against feather-degrading microorganisms. One of these defences is the oil secreted by the uropygial gland, which birds use to protect their feathers against parasites. In previous studies we have shown how Enterococcus faecalis strains isolated from nestling hoopoes exert antagonistic effects against B. licheniformis, mediated by the production of bacteriocins. Consequently we hypothesized that this enterococcus and the bacteriocins it engenders might act as a defence against feather-degrading microorganisms in hoopoes. We investigated this hypothesis in a series of laboratory experiments and evaluated the extent to which the keratinolytic effects caused by B. licheniformis were reduced by the E. faecalis MRR10-3 strain, isolated from hoopoes, and its bacteriocins. In different treatments, feathers or pure keratin was incubated with B. licheniformis, B. licheniformis together with E. faecalis MRR10-3, and B. licheniformis together with the bacteriocins produced by E. faecalis MRR10-3. Our results were in accordance with the predicted effects on hoopoe feathers. There was a significant decrease both in pure keratin loss and in feather degradation in the presence of the symbiotic bacterium or its bacteriocin. These results suggest that by preening their feathers hoopoes benefit from their symbiotic relationship with bacteriocin-producing enterococci, which constitute a chemical defence against feather degradation.
Journal of Experimental Biology 11/2009; 212(Pt 22):3621-6. · 3.00 Impact Factor
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ABSTRACT: 1. It has been recently showed that one bacterial strain isolated from the uropygial gland of a nestling hoopoe Upupa epops produced antimicrobial peptides active against a broad spectrum of pathogenic bacteria. These bacteria might thus mediate antimicrobial properties of the uropygial secretions as a consequence of the symbiotic association with hoopoes.
2. We study antimicrobial properties of white (from males and non-breeding females) and brown (from nestlings and breeding females) uropygial gland secretions of hoopoes Upupa epops, as well as the association with the presence of bacteria living inside their uropygial gland.
3. We found that brown, but not white secretions contained bacteria and showed antimicrobial activity against the feather degrading bacterium Bacillus licheniformis. The antagonistic activity of bacterial colonies was mediated by antimicrobial peptides because protease inhibited antimicrobial properties.
4. All except one identified bacterium in aerobic cultures were of the genus Enterococcus, and the microscopic study of uropygial secretions and glands confirmed a high density of bacteria within the gland.
5. Furthermore, we studied potential benefits of antimicrobial peptides produced by symbiotic bacteria of hoopoes by adding protease to incubating nests.
6. The experiment increased bacterial growth and hatching failures in hoopoes but not in spotless starlings Sturnus unicolor, a species that does not harbour bacteria in its uropygial gland.
7. Thus, microbiological, anatomical and ecological results suggest a tight symbiotic interaction between bacteria that produce antibiotic substances and the hoopoes.
Functional Ecology. 01/2008; 22:864-871.
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Analytical Biochemistry 08/2007; 366(1):102-4. · 3.00 Impact Factor
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ABSTRACT: To determine the effectiveness of enterocin AS-48 on Staphylococcus aureus CECT 976 in combination with chemical preservatives at acidic and neutral pH.
At pH 4.5, the activity of AS-48 increases in the presence of lactic acid (1.0%), acetic acid (0.5% and 1.0%), and citric acid (0.3% and 0.6%). This synergistic effect has also been observed during the first 8 h of incubation with benzoate (0.06% and 0.12%) and sorbate (2% and 3%). Interestingly, at pH 7, lactate (1%) increases the inhibitory effect of AS-48, reducing the S. aureus population by 6 log units compared with the control culture. At neutral pH, combinations of AS-48 and sodium tripolyphosphate, STPP (0.3% and 0.5%) also eliminate this pathogen after 24 h.
These results indicate that enterocin AS-48 could be applied in combination with a range of chemical preservatives in order to increase its efficacy in inhibiting S. aureus.
This study supports the potential use of enterocin AS-48 as a biopreservative to control S. aureus in combination with other food-grade chemical hurdles.
Letters in Applied Microbiology 08/2007; 45(1):19-23. · 1.62 Impact Factor
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ABSTRACT: Enterococcus faecalis produces a cationic and circular enterocin, AS-48, of 7149 Da, the genetic determinants of which are located within the pMB2 plasmid. We have compared enterocin AS-48 production by different enterococci species with that of other 'safe' lactic acid bacteris (LAB) (GRAS status) and looked into the subsequent application of this enterocin in food production.
In an effort to exploit this system for the heterologous expression of enterocin AS-48, a number of vectors containing the as-48 cluster were constructed and used to transform several LAB strains (genera Enterococcus, Lactococcus and Lactobacillus)
Heterologous production of enterocin AS-48 failed when bacteria other than those belonging to the genus Enterococcus were used as hosts, although expression of a partial level of resistance against AS-48 were always detected, ruling out the possibility of a lack of recognition of the enterococcal promoters.
Our results reveal the special capacity of species from the genus Enterococcus to produce AS-48, an enterocin that requires a post-transcriptional modification to generate a circular peptide with a wide range of inhibitory activity against pathogenic and spoilage bacteria. Preliminary experiments in foodstuffs using nonvirulent enterococci with interesting functional properties reveal the possibility of a biotechnological application of these transformants.
Journal of Applied Microbiology 06/2007; 102(5):1350-61. · 2.34 Impact Factor
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ABSTRACT: Alicyclobacillus acidoterrestris is a spoilage-causing bacterium in fruit juices. Control of this bacterium by enterocin AS-48 from Enterococcus faecalis A-48-32 is described. Enterocin AS-48 was active against one A. acidocaldarius and three strains of A. acidoterrestris tested. In natural orange and apple juices incubated at 37 degrees C, vegetative cells of A. acidoterrestris DSMZ 2,498 were inactivated by enterocin AS-48 (2.5 microg/ml) and no growth was observed in 14 days. In commercial fruit juices added of AS-48 (2.5 microg/ml) and inoculated with vegetative cells or with endospores of strain DSMZ 2,498, no viable cells were detected during 90 days of incubation at temperatures of 37 degrees C, 15 degrees C or 4 degrees C, except for apple, peach and grapefruit juices inoculated with vegetative cells and incubated at 37 degrees C which were protected efficiently for up to 60 days. Remarkably, in all commercial fruit juices tested, no viable cells were detected as early as 15 min after incubation with the bacteriocin. Endospores incubated for a very short time (1 min) with increasing bacteriocin concentrations were inactivated by 2.5 microg/ml AS-48. Electron microscopy examination of vegetative cells and endospores treated with enterocin AS-48 revealed substantial cell damage and bacterial lysis as well as disorganization of endospore structure.
International Journal of Food Microbiology 11/2005; 104(3):289-97. · 3.33 Impact Factor
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ABSTRACT: Characterization of Ent F-58 produced by Enterococcus faecium strain F58 isolated from Jben, a soft, farmhouse goat's cheese manufactured without starter cultures.
E. faecium strain F58 was isolated because of its broad inhibitory spectrum, including activity against food-borne pathogenic and spoilage bacteria. The antimicrobial substance was produced during the growth phase, with maximum production after 16-20 h of incubation at 30 degrees C, and was stable over a wide pH range (4-8) and at high temperatures (5 min at 100 degrees C). The enterocin was purified to homogeneity using cation exchange and hydrophobic interaction on C-18 and reverse-phase high-performance liquid chromatography. The activity was eluted as two individual active fractions (F-58A and F-58B) and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry analysis showed masses of 5210.5 and 5234.3 Da respectively. Both peptides were partially sequenced by Edman degradation, and amino-acid sequencing revealed high similarity with enterocin L50 (I). PCR-amplified fragments containing the structural genes for F-58 A and B were located in a 22-kb plasmid harboured by this strain. We verified that it also holds the structural gene for P-like enterocin.
E. faecium strain F58 from Jben cheese, a producer of enterocin L50, exerts an inhibitory effect against strains of genera such as Listeria, Staphylococcus, Clostridium, Brochothrix and Bacillus. Enterocin was characterized according to its functional and biological properties, purification to homogeneity and an analysis of its amino acid and genetic sequences.
E. faecium strain F58 is a newly discovered producer of enterocin L50, the biotechnological characteristics of which indicate its potential for application as a protective agent against pathogens and spoilage bacteria in foods.
Journal of Applied Microbiology 02/2005; 99(1):141-50. · 2.34 Impact Factor
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ABSTRACT: To determine the effects of outer membrane (OM) permeabilizing agents on the antimicrobial activity of enterocin AS-48 against Escherichia coli O157:H7 CECT 4783 strain in buffer and apple juice.
We determined the influence of pH, EDTA, sodium tripolyphosphate (STPP) and heat on E. coli O157:H7 CECT 4783 sensitivity to enterocin AS-48 in buffer and in apple juice. Enterocin AS-48 was not active against intact cells of E. coli O157:H7 CECT 4783 at neutral pH. However, cells sublethally injured by OM permeabilizing agents (EDTA, STPP, pH 5, pH 8.6 and heat) became sensitive to AS-48, decreasing the amount of bacteriocin required for inhibition of E. coli O157:H7 CECT 4783.
The results presented indicate that enterocin AS-48 could potentially be applied with a considerably wider range of protective agents, such as OM permeabilizing agents, with increased efficacy in inhibiting E. coli O157:H7.
Results from this study support the potential use of enterocin AS-48 to control E. coli O157:H7 in combination with other hurdles.
Journal of Applied Microbiology 02/2005; 99(6):1364-72. · 2.34 Impact Factor
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ABSTRACT: Control of the enterotoxigenic Staphylococcus aureus CECT 976 strain by enterocin AS-48 in laboratory cultures, and behaviour of the AS-48 activity in the presence of food preservatives.
Enterocin AS-48 shows inhibitory activity on the majority of the Staphylococcus species tested. This enterocin has a bactericidal and bacteriolytic mode of action on S. aureus CECT 976, a strain selected for this study by its enterotoxigenic character (SEA production). The inhibitory effect of AS-48 was pH and temperature dependent, and enterocin activity was higher at pH 5. The minimum bactericidal concentration (MBC) of AS-48, decreased from 15 microg ml(-1) at 37 degrees C to 10 microg ml(-1) at 15 degrees C. Sublethally injured cells showed an increased sensitivity with a MBC of 5 microg ml(-1). In this way, the highest effectiveness of Ent AS-48 against S. aureus CECT 976 was obtained at 4 degrees C in combination with high concentrations of NaCl (6 and 7%). Interestingly, enterotoxin SEA production by strain CECT 976 was markedly inhibited by subinhibitory concentrations of Ent AS-48. These low concentrations also provoked a delay of bacterial growth.
The results presented indicated that Ent AS-48 has a potential for application as a protective agent against S. aureus in foods.
In this study, we have established the conditions for an efficient inhibition of growth and enterotoxin production by S. aureus CECT 976 in culture media by a combination of environmental factors and Ent AS-48.
Journal of Applied Microbiology 02/2004; 97(1):48-56. · 2.34 Impact Factor
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ABSTRACT: The complete nucleotide sequence of the small (5149 bp) and cryptic plasmid pS86 from Enterococcus faecalis ssp. faecalis S-86 has been determined. Sequence analysis revealed six putative open reading frames (ORFs) encoding polypeptides of 28.3, 11.5, 8.4, 65.1, 7.3, and 11.96 kDa each. Based on sequence similarity, two cassettes have been identified in pS86: ORF1 codes for the replication initiation protein (Rep); ORF4 codes for a putative mobilization protein that shows similarities to Mob/Pre proteins from plasmids of Gram-positive bacteria. No function could be assigned to the other putative ORFs found. According to our results, pS86 plasmid could use a theta-mode of replication, similar to the recently described theta-type replicons from pUCL287 (Tetragenococcus halophila) and pLA1 or pLA105 (Lactobacillus acidophilus) plasmids.
Current Microbiology 11/2000; 41(4):257-61. · 1.82 Impact Factor
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ABSTRACT: The peptide AS-48 is highly active on all Listeria species. It has a bactericidal and bacteriolytic mode of action on Listeria monocytogenes CECT 4032, causing depletion of the membrane electrical potential and pH gradient. The producer strain Enterococcus faecalis A-48-32, releases sufficient amounts of AS-48 into the growth medium to suppress L. monocytogenes in cocultures at enterococcus-to-listeria ratios above 1 at 37 degreesC or above 10 at 15 degreesC. As the temperature decreases, the bactericidal effects of AS-48 are less pronounced, but at 2.5 microgram/ml it still can inhibit the growth of listeria at 6 degreesC. AS-48 is highly active on liquid cultures, although concentrations above 0.2 microgram/ml are required to avoid adaptation of listeria. AS-48-adapted cells can be selected at low (but still inhibitory) concentrations, and they can be inhibited completely by AS-48 at 0.5 microgram/ml. The adaptation is lost gradually upon repeated subcultivation. AS48(ad) cells are cross-resistant to nisin and show an increased resistance to muramidases. Their fatty acid composition is modified: they show a much higher proportion of branched fatty acids as well as a higher C15:0 An-to-C17:0 An ratio. Resistance to AS-48 is also maintained by protoplasts from AS48(ad) cells. Electron microscopy observations show that the cell wall of AS48(ad) cells is thicker and less dense. The structure of wild-type cells is severely modified after AS-48 treatment: the cell wall and the cytoplasmic membrane are disorganized, and the cytoplasmic content is lost. Intracytoplasmic membrane vesicles are also observed when the wild-type strain is treated with high AS-48 concentrations.
Applied and Environmental Microbiology 03/1999; 65(2):618-25. · 3.83 Impact Factor
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ABSTRACT: The sexpheromone system of Enterococcus faecalis is a form of bacterial conjugation that plays an important role in the horizontal dissemination of genes. The ecological significance of 'sexual' plasmids is to permit a rapid mobilization of genes of interest for the species (e.g. those encoding haemolysins, bacteriocins or antibiotic resistance). The physical mapping of pMB1-1, a conjugative plasmid of Ent. faecalis that responds to cCF10 pheromone, has been undertaken. By means of hybridization with conserved sequences of pCF10 plasmid, the regions harbouring the genes responsible for the pheromone inhibitor and the aggregation and exclusion proteins of this plasmid have been identified. The results demonstrated that plasmids pMB1-1 and pCF10 only show homology in the region involved in the conjugative response, suggesting that this region may be transferred in an independent way to that of the rest of the plasmid.
Letters in Applied Microbiology 10/1998; 27(3):125-9. · 1.62 Impact Factor
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Molecular Microbiology 10/1998; 29(5):1318-9. · 5.01 Impact Factor
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ABSTRACT: A region of 7.8 kb of the plasmid pMB2 from Enterococcus faecalis S-48 carrying the information necessary for production and immunity of the peptide antibiotic AS-48 has been cloned and sequenced. It contains the as-48A structural gene plus five open reading frames (as-48B, as-48C, as-48C1, as-48D and as-48D1). Besides As-48D, all the predicted gene products are basic hydrophobic proteins with potential membrane-spanning domains (MSDs). None of them shows any homology with protein sequences stored in databanks, except for As-48D, which shows similarity to the C-terminal domain of ABC transporters and contains a highly conserved ATP-binding site. The gene products of as-48B, as-48C, as-48C1 and as-48D are thought to be involved in AS-48 production and secretion. The only gene able to provide resistance to AS-48 by itself is as-48D1. Immunity also seems to be enhanced at least by the products of as-48B, as-48C1 and as-48D genes. Transcription analysis using probes derived from the different ORFs revealed two large (3.5 and 2.7kb) mRNAs, suggesting that the different genes are organized in two constitutive operons.
Molecular Microbiology 02/1998; 27(2):347-58. · 5.01 Impact Factor
