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1. Role of Curing Agents in the Adaptive Response of the Bioprotective Latilactobacillus curvatus CRL 705 from a Physiologic and Proteomic Perspective

Author

Lucrecia C. Terán, Alejandra Orihuel, Emilse Bentencourt, Raúl Raya, and Silvina Fadda

Subjects
lactic acid bacteria, bioprotective cultures, meat products, meat processing conditions, curing agents, adaptive response, Specialties of internal medicine, RC581-951
Abstract

During meat processing, lactic acid bacteria (LAB) have to competitively adapt to the hostile environment produced by curing additives (CA). The objective of this study was to investigate the ability of Latilactobacillus curvatus CRL 705, a bioprotective strain of meat origin, to adapt to CA. A physiological and proteomic approach was performed. CRL 705 was grown in a chemically defined medium (CDM) containing specific concentrations of CA (NaCl, nitrite, sucrose, and ascorbic acid). The results showed minor differences in growth kinetics in the presence of CA. Glucose consumption, present in the CDM, and production of lactic acid and bacteriocins were not significantly affected. Proteomic analyses indicated that most of the identified proteins (36 out of 39) mainly related to carbohydrate metabolism (18%), posttranslational modifications (15.6%), energy production and conversion (11.1%), translation (11.1%), and nucleotide metabolism (8.9%) were underexpressed. In response to the studied CA, CRL 705 slowed down its general metabolism, achieving slight changes in physiological and proteomic parameters. The observed performance is another characteristic that extends the well-known competitive profile of CRL 705 as a meat starter and bioprotective culture. This is the first report dealing with the impact of CA on LAB proteomics.

Published
2023
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2. Genomic and proteomic characterization of two strains of Shigella flexneri 2 isolated from infants’ stool samples in Argentina

Author

Mónica F. Torrez Lamberti, Lucrecia C. Terán, Fabián E. Lopez, María de las Mercedes Pescaretti, and Mónica A. Delgado

Subjects
Shigella, Clinical isolates, Epidemiology, Genomic, Proteomic, Virulence, Biotechnology, TP248.13-248.65, Genetics, QH426-470
Abstract

Abstract Background Shigella specie is a globally important intestinal pathogen disseminated all over the world. In this study we analyzed the genome and the proteomic component of two Shigella flexneri 2a clinical isolates, collected from pediatric patients with gastroenteritis of the Northwest region of Argentina (NWA) in two periods of time, with four years of difference. Our goal was to determine putative changes at molecular levels occurred during these four years, that could explain the presence of this Shigella`s serovar as the prevalent pathogen in the population under study. Results As previously reported, our findings support the idea of Shigella has a conserved “core” genome, since comparative studies of CI133 and CI172 genomes performed against 80 genomes obtained from the NCBI database, showed that there is a large number of genes shared among all of them. However, we observed that CI133 and CI172 harbors a small number of strain-specific genes, several of them present in mobile genetic elements, supporting the hypothesis that these isolates were established in the population by horizontal acquisition of genes. These differences were also observed at proteomic level, where it was possible to detect the presence of certain secreted proteins in a culture medium that simulates the host environment. Conclusion Great similarities were observed between the CI133 and CI172 strains, confirming the high percentage of genes constituting the “core” genome of S. flexneri 2. However, numerous strain specific genes were also determined. The presence of the here identified molecular elements into other strain of our culture collation, is currently used to develop characteristic markers of local pathogens. In addition, the most outstanding result of this study was the first description of a S. flexneri 2 producing Colicin E, as one of the characteristics that allows S. flexneri 2 to persist in the microbial community. These findings could also contribute to clarify the mechanism and the evolution strategy used by this pathogen to specifically colonize, survive, and cause infection within the NWA population.

Published
2022
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3. Lyophilized alginate-based microspheres containing Lactobacillus fermentum D12, an exopolysaccharides producer, contribute to the strain’s functionality in vitro

Author

Katarina Butorac, Jasna Novak, Barbara Bellich, Lucrecia C. Terán, Martina Banić, Andreja Leboš Pavunc, Slaven Zjalić, Paola Cescutti, Jagoda Šušković, and Blaženka Kos

Subjects
Eps cluster, Exopolysaccharides, Limosilactobacillus (Lactobacillus) fermentum, Probiotic, Prebiotic, Microbiology, QR1-502
Abstract

Abstract Lactobacillus (Limosilactobacillus) fermentum D12 is an exopolysaccharide (EPS) producing strain whose genome contains a putative eps operon. Whole-genome analysis of D12 was performed to disclose the essential genes correlated with activation of precursor molecules, elongation and export of the polysaccharide chain, and regulation of EPS synthesis. These included the genes required for EPS biosynthesis such as eps A, B, C, D and E, also gt, wzx, and wzy and those involved in the activation of the precursor molecules gal E, gal T and gal U. Both the biosynthesis and export mechanism of EPS were proposed based on functional annotation. When grown on MRS broth with an additional 2% w/v glucose, L. fermentum D12 secreted up to 200 mg/L of a mixture of EPSs, whose porous structure was visualized by scanning electron microscopy (SEM). Structural information obtained by 1HNMR spectroscopy together with composition and linkage analyses, suggested the presence of at least two different EPSs, a branched heteropolysaccharide containing t-Glcp and 2,6-linked Galf, and glycogen. Since recent reports showed that polysaccharides facilitate the probiotic-host interactions, we at first sought to evaluate the functional potential of L. fermentum D12. Strain D12 survived simulated gastrointestinal tract (GIT) conditions, exhibited antibacterial activity against enteropathogenic bacteria, adhered to Caco-2 cells in vitro, and as such showed potential for in vivo functionality. The EPS crude extract positively influenced D12 strain capacity to survive during freeze-drying and to adhere to extracellular matrix (ECM) proteins but did not interfere Caco-2 and mucin adherence when added at concentrations of 0.2, 0.5, and 1.0 mg/mL. Since the viable bacterial count of free D12 cells was 3 logarithmic units lower after the exposure to simulated GIT conditions than the initial count, the bacterial cells had been loaded into alginate for viability improvement. Microspheres of D12 cells, which were previously analyzed at SEM, significantly influenced their survival during freeze-drying and in simulated GIT conditions. Furthermore, the addition of the prebiotic substrates mannitol and lactulose improved the viability of L. fermentum D12 in freeze-dried alginate microspheres during 1-year storage at 4 °C compared to the control.

Published
2021
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4. Proteomic Studies of the Biofilm Matrix including Outer Membrane Vesicles of Burkholderia multivorans C1576, a Strain of Clinical Importance for Cystic Fibrosis

Author

Lucrecia C. Terán, Marco Distefano, Barbara Bellich, Sara Petrosino, Paolo Bertoncin, Paola Cescutti, and Daniele Sblattero

Subjects
Burkholderia multivorans, proteomic, biofilm, outer membrane vesicles, LC-LC/MS, Biology (General), QH301-705.5
Abstract

Biofilms are aggregates of microbial cells encased in a highly hydrated matrix made up of self-produced extracellular polymeric substances (EPS) which consist of polysaccharides, proteins, nucleic acids, and lipids. While biofilm matrix polysaccharides are unraveled, there is still poor knowledge about the identity and function of matrix-associated proteins. With this work, we performed a comprehensive proteomic approach to disclose the identity of proteins associated with the matrix of biofilm-growing Burkholderia multivorans C1576 reference strain, a cystic fibrosis clinical isolate. Transmission electron microscopy showed that B. multivorans C1576 also releases outer membrane vesicles (OMVs) in the biofilm matrix, as already demonstrated for other Gram-negative species. The proteomic analysis revealed that cytoplasmic and membrane-bound proteins are widely represented in the matrix, while OMVs are highly enriched in outer membrane proteins and siderophores. Our data suggest that cell lysis and OMVs production are the most important sources of proteins for the B. multivorans C1576 biofilm matrix. Of note, some of the identified proteins are lytic enzymes, siderophores, and proteins involved in reactive oxygen species (ROS) scavenging. These proteins might help B. multivorans C1576 in host tissue invasion and defense towards immune system assaults.

Published
2020
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5. Preferencia de hospedero, orientación y rasgos morfológicos-anatómicos de Pleopeltis minima (Polypodiaceae) en un ambiente urbano

Author

Marcela A. Hernández, Rodolfo O. Varela, Lucrecia C. Terán, and Marisol Mata

Subjects
Pleopeltis, epifitismo, anatomía, helechos, Polypodiaceae, Plant culture, SB1-1110, Botany, QK1-989
Abstract

Hernández, M. A.; R. O. Varela; L. C. Terán; M. Mata. 2012. “Preferencia de hospedero, orientación y rasgos morfológicos-anatómicos de Pleopeltis minima (Polypodiaceae) en un ambiente urbano”. Lilloa 49 (2). Pleopeltis minima un helecho epifito de la Familia Polypodiaceae de amplia distribución latitudinal en Sudamérica, con gran tolerancia a la desecación. Este estudio analiza la preferencia de P. minima por la especie de hospedero y orientación y describe las estructuras morfoanatómicas xeromórficas de la fronde y del rizoma, en el arbolado de las ciudades de San Miguel de Tucumán y Yerba Buena (Provincia de Tucumán, Argentina). Se registró la presencia y orientación de P. minima sobre el tronco y ramas laterales (hasta los 4 m de altura), en todos los árboles cultivados de las Avenidas Mate de Luna y Aconquija (9,5 km long. total). Ocho especies de árboles fueron hospederos de P. minima. Handroanthus impetiginosa (“lapacho rosado”) y Jacaranda mimosifolia (“jacarandá”) fueron los principales hospederos y las especies más abundantes de las avenidas. La proporción absoluta de árboles hospederos fue mayor en Enterolobium contortisiliquum (“pacará”), y similar en Ceiba chodatii (“palo borracho”), H. impetiginosa y J. mimosifolia. La frecuencia de P. minima fue significativamente mayor en troncos y ramas con orientación sur. Las escamas del pecíolo en conjunción con el movimiento de apertura y cierre de las alas y el anillo esclerenquimático subepidérmico constituyen mecanismos de control de la pérdida de agua y de hidratación. Estos resultados son los primeros en su tipo para helechos de la Familia Polypodiaceae.

Published
2012

6. The Bep gene cluster in Burkholderia cenocepacia H111 codes for a water-insoluble exopolysaccharide essential for biofilm formation

Author

Barbara Bellich, Lucrecia C. Terán, Magnus M. Fazli, Francesco Berti, Roberto Rizzo, Tim Tolker-Nielsen, and Paola Cescutti

Subjects
Polymers and Plastics, Burkholderia cenocepacia, Polysaccharides, Multigene Family, Biofilms, Organic Chemistry, Materials Chemistry, Humans, Water, Anti-Bacterial Agents
Abstract

Burkholderia cenocepacia is an opportunistic pathogen isolated from cystic fibrosis patients where it causes infections that are extremely difficult to treat with antibiotics, and sometimes have a fatal outcome. Biofilm is a virulence trait of B. cenocepacia, and is associated with infection persistence and increased tolerance to antibiotics. In biofilms exopolysaccharides have an important role, conferring mechanical stability and antibiotic tolerance. Two different exopolysaccharides were isolated from B. cenocepacia H111 biofilms: a water-soluble polysaccharide rich in rhamnose and containing an L-Man residue, and a water-insoluble polymer made of glucose, galactose and mannose. In the present work, the product encoded by B. cenocepacia H111 bepA-L gene cluster was identified as the water-insoluble exopolysaccharide, using mutant strains and NMR spectroscopy of the purified polysaccharides. It was also demonstrated that the B. cenocepacia H111 wild type strain produces the water-insoluble exopolysaccharide in pellicles, thus underlining its potential importance in in vivo infections.

Published
2022

7. Genomic analysis revealed conserved acid tolerance mechanisms from native micro-organisms in fermented feed

Author

Gisela Tubio, Christian Magni, Victor Sebastian Blancato, Sergio H. Alarcón, Luis Esteban, Lucrecia C. Terán, Pablo Mortera, and Martín Espariz

Subjects
Lactobacillus paracasei, biology, Animal feed, food and beverages, Virulence, General Medicine, Genomics, Lacticaseibacillus paracasei, biology.organism_classification, Applied Microbiology and Biotechnology, Saccharomyces, Pathogenicity island, Animal Feed, Yeast, Lactobacillales, Fermentation, Food Microbiology, Animals, Food science, Bacteria, Biotechnology
Abstract

AIMS Fermented feed is an agricultural practice used in many regions of the world to improve the growth performance of farm animals. This study aimed to identify and evaluate the lactic acid bacteria and yeast involved in the production of fermented feed. METHODS AND RESULTS We isolated and described two micro-organisms from autochthonous microbiota origin present in a regional feed product, Lactobacillus paracasei IBR07 (Lacticaseibacillus paracasei) and Kazachstania unispora IBR014 (Saccharomyces unisporum). Genome sequence analyses were performed to characterize both micro-organisms. Potential pathways involved in the acid response, tolerance and persistence were predicted in both genomes. Although L. paracasei and K. unispora are considered safe for animal feed, we analysed the presence of virulence factors, antibiotic resistance and pathogenicity islands. Furthermore, the Galleria mellonella model was used to support the safety of both isolates. CONCLUSIONS We conclude that IBR07 and IBR014 strains are good candidates to be used as starter cultures for feed fermentation. SIGNIFICANCE AND IMPACT OF THE STUDY The data presented here will be helpful to explore other biotechnological aspects and constitute a starting point for further studies to establish the consumption benefit of fermented feed in farm animal production.

Published
2021

8. Additional file 6 of Lyophilized alginate-based microspheres containing Lactobacillus fermentum D12, an exopolysaccharides producer, contribute to the strain’s functionality in vitro

Author

Butorac, Katarina, Novak, Jasna, Bellich, Barbara, Lucrecia C. Terán, Banić, Martina, Pavunc, Andreja Leboš, Zjalić, Slaven, Cescutti, Paola, Šušković, Jagoda, and Blaženka Kos

Abstract

Additional file 6: Table S1. Genes of L. fermentum D12 involved in exopolysaccharides (EPSs) production and in the activation of the precursor molecules.

Published
2021
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9. Exploring the Genome of Fructobacillus tropaeoli CRL 2034, a Fig-Origin Strain that Produces High Levels of Mannitol from Fructose

Author

Raúl R. Raya, Florencia Mohamed, Juliana Bleckwedel, Elvira Maria Hebert, Luciana G. Ruiz Rodríguez, Lucrecia C. Terán, and Fernanda Mozzi

Subjects
Argentina, Fructose, Applied Microbiology and Biotechnology, Microbiology, Genome, 03 medical and health sciences, chemistry.chemical_compound, RNA, Ribosomal, 16S, medicine, Mannitol, Gene, Phylogeny, 030304 developmental biology, Whole genome sequencing, 0303 health sciences, Leuconostocaceae, Strain (chemistry), biology, 030306 microbiology, General Medicine, 16S ribosomal RNA, biology.organism_classification, Ficus, Biochemistry, chemistry, medicine.drug
Abstract

We report the draft genome sequence of Fructobacillus tropaeoli CRL 2034, a strain isolated from ripe fig in Tucuman province, Argentina. The interest in studying the genome of this fructophilic lactic acid bacterium strain was motivated by its ability to produce high levels of mannitol from fructose. This polyol has multiple industrial applications; however, it is mainly used as low calorie sugar in the food industry. The assembled genome of this strain consists of a 1.66-Mbp circular chromosome with 1465 coding sequences and a G+C content of 44.6%. The analysis of this genome supports the one step reaction of fructose reduction to mannitol by the mannitol 2-dehydrogenase enzyme, which together with a fructose permease, were identified as involved in mannitol synthesis. In addition, a phylogenetic analysis was performed including other Leuconostocaceae members to which the Fructobacillus genus belongs to; according to the 16S rRNA gene sequences, the strain CRL 2034 was located in the Fructobacillus clade. The present genome sequence could be useful to further elucidate regulatory processes of mannitol and other bioactive metabolites and to highlight the biotechnological potential of this fruit-origin Fructobacillus strain.

Published
2020

10. Proteomic studies of the biofilm matrix including outer membrane vesicles of burkholderia multivorans c1576, a strain of clinical importance for cystic fibrosis

Author

Paolo Bertoncin, Lucrecia C. Terán, Paola Cescutti, Barbara Bellich, Daniele Sblattero, Marco Distefano, Sara Petrosino, Teran, L. C., Distefano, M., Bellich, B., Petrosino, S., Bertoncin, P., Cescutti, P., and Sblattero, D.

Subjects
Microbiology (medical), Lysis, Outer membrane vesicles, Matrix (biology), Microbiology, 03 medical and health sciences, Extracellular polymeric substance, Virology, LC-LC/MS, Burkholderia multivoran, Biofilm, Burkholderia multivorans, Proteomic, lcsh:QH301-705.5, 030304 developmental biology, 0303 health sciences, biology, 030306 microbiology, Chemistry, Outer membrane vesicle, Biofilm matrix, biology.organism_classification, lcsh:Biology (General), Biochemistry, Cytoplasm, Bacterial outer membrane
Abstract

Biofilms are aggregates of microbial cells encased in a highly hydrated matrix made up of self-produced extracellular polymeric substances (EPS) which consist of polysaccharides, proteins, nucleic acids, and lipids. While biofilm matrix polysaccharides are unraveled, there is still poor knowledge about the identity and function of matrix-associated proteins. With this work, we performed a comprehensive proteomic approach to disclose the identity of proteins associated with the matrix of biofilm-growing Burkholderia multivorans C1576 reference strain, a cystic fibrosis clinical isolate. Transmission electron microscopy showed that B. multivorans C1576 also releases outer membrane vesicles (OMVs) in the biofilm matrix, as already demonstrated for other Gram-negative species. The proteomic analysis revealed that cytoplasmic and membrane-bound proteins are widely represented in the matrix, while OMVs are highly enriched in outer membrane proteins and siderophores. Our data suggest that cell lysis and OMVs production are the most important sources of proteins for the B. multivorans C1576 biofilm matrix. Of note, some of the identified proteins are lytic enzymes, siderophores, and proteins involved in reactive oxygen species (ROS) scavenging. These proteins might help B. multivorans C1576 in host tissue invasion and defense towards immune system assaults.

Published
2020

11. Physiological and proteomic response of Escherichia coli O157:H7 to a bioprotective lactic acid bacterium in a meat environment

Author

Maria Pia Valacco, André M. Almeida, Silvia N.J. Moreno, Emilse Masias, Sébastien Planchon, Lucrecia C. Terán, Jenny Renaut, Alejandra Orihuel, Carlos Minahk, Silvina Fadda, Graciela Vignolo, and Lucila Saavedra

Subjects
Proteomics, Meat, 030309 nutrition & dietetics, Enterococcus mundtii, BIOPROTECTIVE CULTURES, medicine.disease_cause, Escherichia coli O157, Microbiology, Ciencias Biológicas, Bacteriophage, purl.org/becyt/ford/1 [https], 03 medical and health sciences, 0404 agricultural biotechnology, Biología Celular, Microbiología, Bacterial Proteins, Lactobacillales, Escherichia, medicine, Bacteriophages, Amino Acids, purl.org/becyt/ford/1.6 [https], Escherichia coli, Pathogen, chemistry.chemical_classification, 0303 health sciences, Extracellular Matrix Proteins, biology, ENTEROHEMORRHAGIC ESCHERICHIA COLI (EHEC), Shiga toxin, 04 agricultural and veterinary sciences, Gene Expression Regulation, Bacterial, biology.organism_classification, 040401 food science, Coculture Techniques, Amino acid, MEAT SAFETY, Lytic cycle, chemistry, biology.protein, PROTEOMICS, CIENCIAS NATURALES Y EXACTAS, BACTERIAL INTERACTION, Food Science
Abstract

The enterohemorrhagic Escherichia (E.) coli (EHEC) is a pathogen of great concern for public health and the meat industry all over the world. The high economic losses in meat industry and the high costs of the illness highlight the necessity of additional efforts to control this pathogen. Previous studies have demonstrated the inhibitory activity of Enterococcus mundtii CRL35 towards EHEC, showing a specific proteomic response during the co-culture. In the present work, additional studies of the EHEC-Ent. mundtii interaction were carried out: i) differential protein expression of E. coli O157:H7 NCTC12900 growing in co-culture with Ent. mundtii in a meat environment, ii) the reciprocal influence between these two microorganisms in the adhesion to extracellular matrix (ECM) proteins and iii) the possible induction of the phage W933, coding for Shiga toxin (Stx1), by Ent. mundtii CRL35. Proteomic analysis showed a significant repression of a number of E. coli NCTC12900 proteins in co-culture respect to its single culture, these mostly related to the metabolism and transport of amino acids and nucleotides. On the other hand, statistically significant overexpression of EHEC proteins involved in stress, energy production, amino acid metabolism and transcription was observed at 30 h respect to 6 h when EHEC grew in co-culture. Data are available via ProteomeXchange with identifier PXD014588. Besides, EHEC showed a decreased adhesion capacity to ECM proteins in the presence of the bioprotective strain. Finally, Ent. mundtii CRL35 did not induce the lytic cycle of W933 bacteriophage, thus indicating its potential safe use for eliminating this pathogen. Overall, this study expands the knowledge of EHEC- Ent. mundtii CRL35 interaction in a meat environment, which will certainly contribute to find out effective biological strategies to eliminate this pathogen. Fil: Orihuel, Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Teran, Lucrecia Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Renaut, Jenny. Luxembourg Institute of Science and Technology; Luxemburgo Fil: Planchon, Sébastien. Luxembourg Institute of Science and Technology; Luxemburgo Fil: Valacco, Maria Pia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina Fil: Masias, Ruth Emilse. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina Fil: Minahk, Carlos Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto Superior de Investigaciones Biológicas. Universidad Nacional de Tucumán. Instituto Superior de Investigaciones Biológicas; Argentina Fil: Vignolo, Graciela Margarita. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Moreno, Silvia Margarita. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina Fil: Almeida, André Martinho de. Universidade de Lisboa; Portugal Fil: Saavedra, Maria Lucila. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Fadda, Silvina G.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina

Published
2019

12. Genetics and Genomics of Lactobacillus sakei and Lactobacillus curvatus

Author

Monique Zagorec, Lucrecia C. Terán, Raúl R. Raya, Marie-Christine Champomier-Verges, Centro de Referencia para Lactobacilos [Tucumán] (CERELA), Consejo Nacional de Investigaciones Científicas y Técnicas [Buenos Aires] (CONICET), UMR 1014 SECurité des ALIments et Microbiologie, Institut National de la Recherche Agronomique (INRA)-Ecole Nationale Vétérinaire, Agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS), MICrobiologie de l'ALImentation au Service de la Santé (MICALIS), and Institut National de la Recherche Agronomique (INRA)-AgroParisTech

Subjects
Genetics, 03 medical and health sciences, 0302 clinical medicine, 030220 oncology & carcinogenesis, Lactobacillus curvatus, [SDV]Life Sciences [q-bio], food and beverages, Genomics, Biology, biology.organism_classification, 030217 neurology & neurosurgery, Lactobacillus sakei
Abstract

International audience; Lactobacillus sakei and Lactobacillus curvatus are two lactic acid bacteria widely used worldwide as starters for meat fermentation. They are phenotypically closely related species and have often been associated as a 'sakei/curvatus' group in the past. These species have also been more recently described to be phylogenetically closely related to other Lactobacillus species such as L. fuchuensis and L. graminis. Genomic studies have contributed to a better characterization of each species and enlightened their specificities. L. sakei exhibits a high genomic diversity and several genomes are now available. Complete and draft genome sequences are also available from L. curvatus strains originating from various origins. This chapter will provide information on genomic repertoires of each species and illustrate their main common features.

Published
2019

13. Nucleotide sequence and analysis of pRC12 and pRC18, two theta-replicating plasmids harbored by Lactobacillus curvatus CRL 705

Author

Raúl R. Raya, Marie-Christine Champomier-Vergès, Elvira Maria Hebert, Stéphane Chaillou, Lucrecia C. Terán, Sergio Antonio Cuozzo, Silvina Fadda, Maria Cecilia Aristimuño Ficoseco, Monique Zagorec, Centro de Referencia para Lactobacilos [Tucumán] (CERELA), Consejo Nacional de Investigaciones Científicas y Técnicas [Buenos Aires] (CONICET), Planta Piloto de Procesos Industriales Microbiológicos [Tucumán] (PROIMI), MICrobiologie de l'ALImentation au Service de la Santé (MICALIS), AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Sécurité des Aliments (SECALIM), Ecole Nationale Vétérinaire de Nantes-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), ANR-11-INBS-0013,IFB (ex Renabi-IFB),Institut français de bioinformatique(2011), and ANR-10-INBS-0009,France-Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010)

Subjects
Toxin-antitoxin modules, Molecular biology, [SDV]Life Sciences [q-bio], Transposases, Protein domains, Gene prediction, LATIC, Toxicology, Pathology and Laboratory Medicine, Biotecnología Industrial, purl.org/becyt/ford/1 [https], Plasmid, LACTIC ACID BACTERIA, Microbial Physiology, Medicine and Health Sciences, Toxins, Bacterial Physiology, Replicon, Insertion sequence, Genetics, 0303 health sciences, Multidisciplinary, Database and informatics methods, purl.org/becyt/ford/2.9 [https], Sequence analysis, Microbial Genetics, Nucleic acid sequence, food and beverages, Genomics, Bioquímica y Biología Molecular, ACID, BACTERIA, Medicine, Otras Biotecnología Industrial, CIENCIAS NATURALES Y EXACTAS, Research Article, Plasmids, DNA Replication, DNA, Bacterial, Bioinformatics, Science, Toxic Agents, Bacterial Toxins, Genetic Vectors, Replication Origin, INGENIERÍAS Y TECNOLOGÍAS, DNA construction, Plasmid construction, Biology, Microbiology, Ciencias Biológicas, 03 medical and health sciences, Bacterial Proteins, Biología Celular, Microbiología, Shuttle vector, Bacterial Genetics, Amino Acid Sequence, purl.org/becyt/ford/1.6 [https], DNA sequence analysis, 030304 developmental biology, pBluescript, Biology and life sciences, Bacteria, Base Sequence, 030306 microbiology, Gut Bacteria, Organisms, Computational Biology, Bacteriology, Sequence Analysis, DNA, PLASMIDS, Genome Analysis, Research and analysis methods, Lactobacillus, Molecular biology techniques, purl.org/becyt/ford/2 [https], REPLICATION, Antitoxins, PLASMID, Transformation efficiency
Abstract

The nucleotide sequences of plasmids pRC12 (12,342 bp; GC 43.99%) and pRC18 (18,664 bp; GC 34.33%), harbored by the bacteriocin-producer Lactobacillus curvatus CRL 705, were determined and analyzed. Plasmids pRC12 and pRC18 share a region with high DNA identity (> 83% identity between RepA, a Type II toxin-antitoxin system and a tyrosine integrase genes) and are stably maintained in their natural host L. curvatus CRL 705. Both plasmids are low copy number and belong to the theta-type replicating group. While pRC12 is a pUCL287-like plasmid that possesses iterons and the repA and repB genes for replication, pRC18 harbors a 168 amino acid replication protein affiliated to RepB, which was named RepB’. Plasmid pRC18 also possesses a pUCL287-like repA gene but it was disrupted by an 11 kb insertion element that contains RepB’, several transposases/IS elements, and the lactocin Lac705 operon. An Escherichia coli / Lactobacillus shuttle vector, named plasmid p3B1, carrying the pRC18 replicon (i.e. repB’ and replication origin), a chloramphenicol resistance gene and a pBluescript backbone, was constructed and used to define the host range of RepB’. Chloramphenicol-resistant transformants were obtained after electroporation of Lactobacillus plantarum CRL 691, Lactobacillus sakei 23K and a plasmid-cured derivative of L. curvatus CRL 705, but not of L. curvatus DSM 20019 or Lactococcus lactis NZ9000. Depending on the host, transformation efficiency ranged from 102 to 107 per μg of DNA; in the new hosts, the plasmid was relatively stable as 29–53% of recombinants kept it after cell growth for 100 generations in the absence of selective pressure. Plasmid p3B1 could therefore be used for cloning and functional studies in several Lactobacillus species. Fil: Teran, Lucrecia Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Cuozzo, Sergio Antonio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Planta Piloto de Procesos Industriales Microbiológicos; Argentina Fil: Aristimuño Ficoseco, Maria Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Fadda, Silvina G.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Chaillou, Stéphane. Institut National de la Recherche Agronomique; Francia Fil: Champomier Vergès, Marie Christine. Institut National de la Recherche Agronomique; Francia Fil: Zagorec, Monique. Institut National de la Recherche Agronomique; Francia Fil: Hebert, Elvira Maria. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Raya, Raul Ricardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina

Published
2020

14. Differential proteomic analysis of lactic acid bacteria—Escherichia coli O157:H7 Interaction and Its contribution to bioprotection strategies in meat

Author

André M. Almeida, Silvina Fadda, Lucrecia C. Terán, Graciela Vignolo, Alejandra Orihuel, Maria Lucila Saavedra, and Jenny Renaut

Subjects
0301 basic medicine, Microbiology (medical), enterohemorrhagic Escherichia coli (EHEC, BIOPROTECTIVE CULTURES, lcsh:QR1-502, bacterial interaction, medicine.disease_cause, Proteomics, Microbiology, lcsh:Microbiology, meat safety, Ciencias Biológicas, purl.org/becyt/ford/1 [https], 03 medical and health sciences, chemistry.chemical_compound, proteomics, Biología Celular, Microbiología, medicine, purl.org/becyt/ford/1.6 [https], Escherichia coli, enterohemorrhagic Escherichia coli (EHEC), biology, ENTEROHEMORRHAGIC ESCHERICHIA COLI (EHEC), Lactic acid bacteria (LAB), biology.organism_classification, Lactic acid, 030104 developmental biology, MEAT SAFETY, chemistry, Biochemistry, PROTEOMICS, Otros Tópicos Biológicos, LACTIC ACID BACTERIA (LAB), bioprotective cultures, CIENCIAS NATURALES Y EXACTAS, Differential (mathematics), Bacteria, BACTERIAL INTERACTION
Abstract

Human infection by Enterohemorrhagic Escherichia (E.) coli (EHEC) occurs through the ingestion of contaminated foods such as milk, vegetable products, water-based drinks, and particularly minced meats. Indeed EHEC is a pathogen that threatens public health and meat industry. The potential of different Lactic Acid Bacteria (LAB) strains to control EHEC in a meat-based medium was evaluated by using a simple and rapid method and by analyzing the growth kinetics of co-cultures (LAB-EHEC) in a meat-based medium. The activity of LAB toward EHEC in co-cultures showed variable inhibitory effect. Although, LAB were able to control EHEC, neither the produced acid nor bacteriocins were responsible of the inhibition. The bacteriocinogenic Enteroccus (Ent.) mundtii CRL35 presented one of the highest inhibition activities. A proteomic approach was used to evaluate bacterial interaction and antagonistic mechanisms between Ent. mundtii and EHEC. Physiological observations, such as growth kinetics, acidification ability and EHEC inhibitory potential were supported by the proteomic results, demonstrating significant differences in protein expression in LAB: (i) due to the presence of the pathogen and (ii) according to the growth phase analyzed. Most of the identified proteins belonged to carbohydrate/amino acid metabolism, energy production, transcription/translation, and cell division. These results contribute to the knowledge of competition strategies used by Ent. mundtii during its co-culture with EHEC setting new perspectives for the use of LAB to control this pathogen in meat. Fil: Orihuel, Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Teran, Lucrecia Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Renaut, Jenny. Institute of Science and Technology; Luxemburgo Fil: Vignolo, Graciela Margarita. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Almeida, André Martinho de. University of Lisbon. Instituto Superior de Agronomia; Portugal Fil: Saavedra, Maria Lucila. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Fadda, Silvina G.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina

Published
2018

15. Phylogenomic analysis of lactobacillus curvatus reveals two lineages distinguished by genes for fermenting plant-derived carbohydrates

Author

Stéphane Chaillou, Lucrecia C. Terán, Monique Zagorec, Marie-Christine Champomier-Vergès, Gwendoline Coeuret, Raúl R. Raya, Centro de Referencia para Lactobacilos [Tucumán] (CERELA), Consejo Nacional de Investigaciones Científicas y Técnicas [Buenos Aires] (CONICET), MICrobiologie de l'ALImentation au Service de la Santé (MICALIS), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, UMR 1014 SECurité des ALIments et Microbiologie, Institut National de la Recherche Agronomique (INRA)-Ecole Nationale Vétérinaire, Agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS), BecAR Program Argentine, Campus France Argentine, France Genomique National infrastructure [ANR-10-INBS-09], and MicroScope annotation platform

Subjects
0301 basic medicine, pangenome, plant fermentation, Lineage (evolution), [SDV]Life Sciences [q-bio], 030106 microbiology, Carbohydrates, PANGENOME, Biology, PHYLOGENOMICS, Genome, Polymorphism, Single Nucleotide, Coalescent theory, purl.org/becyt/ford/1 [https], Ciencias Biológicas, 03 medical and health sciences, Biología Celular, Microbiología, Phylogenetics, FOOD, LACTIC ACID BACTERIA, Phylogenomics, Lactobacillus curvatus, food, lactic acid bacteria, phylogenomic, Genetics, purl.org/becyt/ford/1.6 [https], Clade, Gene, Ecology, Evolution, Behavior and Systematics, Phylogeny, 2. Zero hunger, PLANT FERMENTATION, Strain (biology), food and beverages, Genomics, Bioquímica y Biología Molecular, Meat Products, Lactobacillus, 030104 developmental biology, Multigene Family, Fermentation, Otros Tópicos Biológicos, LACTOBACILLUS CURVATUS, Genome, Bacterial, CIENCIAS NATURALES Y EXACTAS, Research Article
Abstract

Lactobacillus curvatus is a lactic acid bacterium encountered in many different types of fermented food (meat, seafood, vegetables, and cereals). Although this species plays an important role in the preservation of these foods, few attempts have been made to assess its genomic diversity. This study uses comparative analyses of 13 published genomes (complete or draft) to better understand the evolutionary processes acting on the genome of this species. Phylogenomic analysis, based on a coalescent model of evolution, revealed that the 6,742 sites of single nucleotide polymorphism within the L. curvatus core genome delineate two major groups, with lineage 1 represented by the newly sequenced strain FLEC03, and lineage 2 represented by the type-strain DSM20019. The two lineages could also be distinguished by the content of their accessory genome, which sheds light on a long-term evolutionary process of lineage-dependent genetic acquisition and the possibility of population structure. Interestingly, one clade from lineage 2 shared more accessory genes with strains of lineage 1 than with other strains of lineage 2, indicating recent convergence in carbohydrate catabolism. Both lineages had a wide repertoire of accessory genes involved in the fermentation of plant-derived carbohydrates that are released from polymers of α/β-glucans, α/β-fructans, and N-acetylglucosan. Other gene clusters were distributed among strains according to the type of food from which the strains were isolated. These results give new insight into the ecological niches in which L. curvatus may naturally thrive (such as silage or compost heaps) in addition to fermented food. Fil: Teran, Lucrecia Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Coeuret, Gwendoline. Institut National de la Recherche Agronomique; Francia Fil: Raya, Raul Ricardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Zagorec, Monique. Institut National de la Recherche Agronomique; Francia Fil: Champomier-Vergès, Marie-Christine. Institut National de la Recherche Agronomique; Francia Fil: Chaillou, Stéphane. Institut National de la Recherche Agronomique; Francia

Published
2018

16. Helical Cell Wall Thickenings in Root Cortical Cells of Polypodiaceae Species from Northwestern Argentina

Author

Marisol Mata, Olga Gladys Martínez, Lucrecia C. Terán, Jefferson Prado, and Marcela A. Hernández

Subjects
biology, FERNS, EUPOLYPODS I, Plant Science, Anatomy, biology.organism_classification, ANATOMY, Ciencias Biológicas, Cell wall, Eupolypods I, Polypodiaceae, CELLULOSE, Botany, Microscopy, EPIPHYTES, Melpomene peruviana, Fern, Thickening, Aspleniaceae, Ciencias de las Plantas, Botánica, CIENCIAS NATURALES Y EXACTAS, Ecology, Evolution, Behavior and Systematics
Abstract

The occurrence of helical cell wall thickenings in fern roots is not well investigated and there are few records about it in the literature. To assess the presence of thickenings and their chemical composition, we studied all species of Polypodiaceae, which grow in northwestern Argentina, using light microscopy, scanning electron microscopy, and fluorescence microscopy. Twenty of the twenty-one species studied showed the thickening in the roots. Only in Melpomene peruviana are helical cell wall thickenings absent. All thickenings have cellulose as the main compound. The structure of the thickening may be classified as simple, furcate, or anastomosing. All data presented in this paper corroborate the same structure and chemical composition of thickenings previously reported for Aspleniaceae. Fil: Hernandez, Marcela A.. Fundación Miguel Lillo; Argentina Fil: Teran, Lucrecia Cecilia. Fundación Miguel Lillo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Centro de Referencia para Lactobacilos; Argentina Fil: Mata, Marisol. Fundación Miguel Lillo; Argentina Fil: Martinez, Olga Gladys. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Salta. Instituto de Bio y Geociencias del NOA. Universidad Nacional de Salta. Facultad de Ciencias Naturales. Museo de Ciencias Naturales. Instituto de Bio y Geociencias del NOA; Argentina Fil: Prado, Jefferson. Universidade de Sao Paulo; Brasil

Published
2013

17. Draft Genome Sequence of the Mannitol-Producing Strain Lactobacillus mucosae CRL573

Author

Julieta Bonacina, Fernanda Mozzi, Raúl R. Raya, Lucrecia C. Terán, Lucila Saavedra, and Juliana Bleckwedel

Subjects
Sucrose, Lactobacillus mucosae, MUCOSAE, MANNITOL, Microbiology, purl.org/becyt/ford/1 [https], Ciencias Biológicas, chemistry.chemical_compound, LACTOBACILLUS, Bacteriocin, Lactobacillus, Genetics, medicine, Prokaryotes, purl.org/becyt/ford/1.6 [https], Sugar, Otras Ciencias de la Computación e Información, Molecular Biology, BACTERIOCIN, biology, Strain (chemistry), Fructose, purl.org/becyt/ford/1.2 [https], Bioquímica y Biología Molecular, biology.organism_classification, chemistry, Ciencias de la Computación e Información, Mannitol, CIENCIAS NATURALES Y EXACTAS, medicine.drug
Abstract

Lactobacillus mucosae CRL573, isolated from child fecal samples, efficiently converts fructose and/or sucrose into the lowcalorie sugar mannitol when cultured in modified MRS medium at pH 5.0. Also, the strain is capable of producing bacteriocin. The draft genome sequence of this strain with potential industrial applications is presented here. Fil: Bleckwedel, Juliana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Centro de Referencia Para Lactobacilos; Argentina Fil: Teran, Lucrecia Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Centro de Referencia Para Lactobacilos; Argentina Fil: Bonacina, Julieta. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Centro de Referencia Para Lactobacilos; Argentina Fil: Saavedra, Maria Lucila. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Centro de Referencia Para Lactobacilos; Argentina Fil: Mozzi, Fernanda Beatriz. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Centro de Referencia Para Lactobacilos; Argentina Fil: Raya, Raul Ricardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Centro de Referencia Para Lactobacilos; Argentina

Published
2014

18. Complete genome sequences of nine mycobacteriophages

Author

Jorgelina Judith Franceschelli, Cristian Alejandro Suárez, Raúl R. Raya, Lucrecia C. Terán, and Héctor R. Morbidoni

Subjects
Genetics, MYCOBACTERIOPHAGE, Mycobacteriophages, Mycobacteriophage, Strain (biology), Mycobacterium smegmatis, MYCOBACTERIA, purl.org/becyt/ford/1.2 [https], Biology, biology.organism_classification, Genome, SEQUENCE, purl.org/becyt/ford/1 [https], GENOME, Ciencias Biológicas, Ciencias de la Computación e Información, Viruses, Mycobacterium species, Bacterial virus, purl.org/becyt/ford/1.6 [https], Molecular Biology, Ciencias de la Información y Bioinformática, Virología, CIENCIAS NATURALES Y EXACTAS
Abstract

Genome analyses of a large number of mycobacteriophages, bacterial viruses that infect members of the genus Mycobacterium, yielded novel enzymes and tools for the genetic manipulation of mycobacteria. We report here the complete genome sequences of nine mycobacteriophages, including a new singleton, isolated using Mycobacterium smegmatis mc(2)155 as a host strain. Fil: Franceschelli, Jorgelina Judith. Universidad Nacional de Rosario. Facultad de Cs.médicas. Escuela de Cs.médicas. Cátedra de Microbiología,parasitología y Virologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Suárez, Cristian Alejandro. Universidad Nacional de Rosario. Facultad de Cs.médicas. Escuela de Cs.médicas. Cátedra de Microbiología,parasitología y Virologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Teran, Lucrecia Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Centro de Referencia Para Lactobacilos; Argentina Fil: Raya, Raul Ricardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Centro de Referencia Para Lactobacilos; Argentina Fil: Morbidoni, Héctor Ricardo. Universidad Nacional de Rosario. Facultad de Cs.médicas. Escuela de Cs.médicas. Cátedra de Microbiología,parasitología y Virologia; Argentina

Published
2014

19. Nucleotide sequence and analysis of pRC12 and pRC18, two theta-replicating plasmids harbored by Lactobacillus curvatus CRL 705.

Author

Lucrecia C Terán, Sergio A Cuozzo, María C Aristimuño Ficoseco, Silvina Fadda, Stéphane Chaillou, Marie-Christine Champomier-Vergès, Monique Zagorec, Elvira M Hébert, and Raúl R Raya

Subjects
Medicine, Science
Abstract

The nucleotide sequences of plasmids pRC12 (12,342 bp; GC 43.99%) and pRC18 (18,664 bp; GC 34.33%), harbored by the bacteriocin-producer Lactobacillus curvatus CRL 705, were determined and analyzed. Plasmids pRC12 and pRC18 share a region with high DNA identity (> 83% identity between RepA, a Type II toxin-antitoxin system and a tyrosine integrase genes) and are stably maintained in their natural host L. curvatus CRL 705. Both plasmids are low copy number and belong to the theta-type replicating group. While pRC12 is a pUCL287-like plasmid that possesses iterons and the repA and repB genes for replication, pRC18 harbors a 168 amino acid replication protein affiliated to RepB, which was named RepB'. Plasmid pRC18 also possesses a pUCL287-like repA gene but it was disrupted by an 11 kb insertion element that contains RepB', several transposases/IS elements, and the lactocin Lac705 operon. An Escherichia coli / Lactobacillus shuttle vector, named plasmid p3B1, carrying the pRC18 replicon (i.e. repB' and replication origin), a chloramphenicol resistance gene and a pBluescript backbone, was constructed and used to define the host range of RepB'. Chloramphenicol-resistant transformants were obtained after electroporation of Lactobacillus plantarum CRL 691, Lactobacillus sakei 23K and a plasmid-cured derivative of L. curvatus CRL 705, but not of L. curvatus DSM 20019 or Lactococcus lactis NZ9000. Depending on the host, transformation efficiency ranged from 102 to 107 per μg of DNA; in the new hosts, the plasmid was relatively stable as 29-53% of recombinants kept it after cell growth for 100 generations in the absence of selective pressure. Plasmid p3B1 could therefore be used for cloning and functional studies in several Lactobacillus species.

Published
2020
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