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Y. Navarro
Department of Biochemistry and Biotechnology, Faculty of Oenology, University Rovira i Virgili (URV), Marcel·lí Domingo 1, 43007 Tarragona, Catalonia, Spain

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Journal article
Published: 15 March 2021 in Foods
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Microbiological strategies are currently being considered as methods for reducing the ethanol content of wine. Fermentations started with a multistarter of three non-Saccharomyces yeasts (Metschnikowia pulcherrima (Mp), Torulaspora delbrueckii (Td) and Zygosaccharomyces bailii (Zb)) at different inoculum concentrations. S. cerevisiae (Sc) was inoculated into fermentations at 0 h (coinoculation), 48 h or 72 h (sequential fermentations). The microbial populations were analyzed by a culture-dependent approach (Wallerstein Laboratory Nutrient (WLN) culture medium) and a culture-independent method (PMA-qPCR). The results showed that among these three non-Saccharomyces yeasts, Td became the dominant non-Saccharomyces yeast in all fermentations, and Mp was the minority yeast. Sc was able to grow in all fermentations where it was involved, being the dominant yeast at the end of fermentation. We obtained a significant ethanol reduction of 0.48 to 0.77% (v/v) in sequential fermentations, with increased concentrations of lactic and acetic acids. The highest reduction was achieved when the inoculum concentration of non-Saccharomyces yeast was 10 times higher (107 cells/mL) than that of S. cerevisiae. However, this reduction was lower than that obtained when these strains were used as single non-Saccharomyces species in the starter, indicating that interactions between them affected their performance. Therefore, more combinations of yeast species should be tested to achieve greater ethanol reductions.

ACS Style

Xiaolin Zhu; María-Jesús Torija; Albert Mas; Gemma Beltran; Yurena Navarro. Effect of a Multistarter Yeast Inoculum on Ethanol Reduction and Population Dynamics in Wine Fermentation. Foods 2021, 10, 623 .

AMA Style

Xiaolin Zhu, María-Jesús Torija, Albert Mas, Gemma Beltran, Yurena Navarro. Effect of a Multistarter Yeast Inoculum on Ethanol Reduction and Population Dynamics in Wine Fermentation. Foods. 2021; 10 (3):623.

Chicago/Turabian Style

Xiaolin Zhu; María-Jesús Torija; Albert Mas; Gemma Beltran; Yurena Navarro. 2021. "Effect of a Multistarter Yeast Inoculum on Ethanol Reduction and Population Dynamics in Wine Fermentation." Foods 10, no. 3: 623.

Journal article
Published: 27 September 2020 in Foods
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The use of controlled mixed inocula of Saccharomyces cerevisiae and non-Saccharomyces yeasts is a common practice in winemaking, with Torulaspora delbrueckii, Lachancea thermotolerans and Metschnikowia pulcherrima being the most commonly used non-Saccharomyces species. Although S. cerevisiae is usually the dominant yeast at the end of mixed fermentations, some non-Saccharomyces species are also able to reach the late stages; such species may not grow in culture media, which is a status known as viable but non-culturable (VBNC). Thus, an accurate methodology to properly monitor viable yeast population dynamics during alcoholic fermentation is required to understand microbial interactions and the contribution of each species to the final product. Quantitative PCR (qPCR) has been found to be a good and sensitive method for determining the identity of the cell population, but it cannot distinguish the DNA from living and dead cells, which can overestimate the final population results. To address this shortcoming, viability dyes can be used to avoid the amplification and, therefore, the quantification of DNA from non-viable cells. In this study, we validated the use of PMAxx dye (an optimized version of propidium monoazide (PMA) dye) coupled with qPCR (PMAxx-qPCR), as a tool to monitor the viable population dynamics of the most common yeast species used in wine mixed fermentations (S. cerevisiae, T. delbrueckii, L. thermotolerans and M. pulcherrima), comparing the results with non-dyed qPCR and colony counting on differential medium. Our results showed that the PMAxx-qPCR assay used in this study is a reliable, specific and fast method for quantifying these four yeast species during the alcoholic fermentation process, being able to distinguish between living and dead yeast populations. Moreover, the entry into VBNC status was observed for the first time in L. thermotolerans and S. cerevisiae during alcoholic fermentation. Further studies are needed to unravel which compounds trigger this VBNC state during alcoholic fermentation in these species, which would help to better understand yeast interactions.

ACS Style

Yurena Navarro; María-Jesús Torija; Albert Mas; Gemma Beltran. Viability-PCR Allows Monitoring Yeast Population Dynamics in Mixed Fermentations Including Viable but Non-Culturable Yeasts. Foods 2020, 9, 1373 .

AMA Style

Yurena Navarro, María-Jesús Torija, Albert Mas, Gemma Beltran. Viability-PCR Allows Monitoring Yeast Population Dynamics in Mixed Fermentations Including Viable but Non-Culturable Yeasts. Foods. 2020; 9 (10):1373.

Chicago/Turabian Style

Yurena Navarro; María-Jesús Torija; Albert Mas; Gemma Beltran. 2020. "Viability-PCR Allows Monitoring Yeast Population Dynamics in Mixed Fermentations Including Viable but Non-Culturable Yeasts." Foods 9, no. 10: 1373.

Journal article
Published: 01 May 2020 in Microorganisms
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The alcohol content in wine has increased due to external factors in recent decades. In recent reports, some non-Saccharomyces yeast species have been confirmed to reduce ethanol during the alcoholic fermentation process. Thus, an efficient screening of non-Saccharomyces yeasts with low ethanol yield is required due to the broad diversity of these yeasts. In this study, we proposed a rapid method for selecting strains with a low ethanol yield from forty-five non-Saccharomyces yeasts belonging to eighteen species. Single fermentations were carried out for this rapid selection. Then, sequential fermentations in synthetic and natural must were conducted with the selected strains to confirm their capacity to reduce ethanol compared with that of Saccharomyces cerevisiae. The results showed that ten non-Saccharomyces strains were able to reduce the ethanol content, namely, Hanseniaspora uvarum (2), Issatchenkia terricola (1), Metschnikowia pulcherrima (2), Lachancea thermotolerans (1), Saccharomycodes ludwigii (1), Torulaspora delbrueckii (2), and Zygosaccharomyces bailii (1). Compared with S. cerevisiae, the ethanol reduction of the selected strains ranged from 0.29 to 1.39% (v/v). Sequential inoculations of M. pulcherrima (Mp51 and Mp FA) and S. cerevisiae reduced the highest concentration of ethanol by 1.17 to 1.39% (v/v) in synthetic or natural must. Second, sequential fermentations with Z. bailii (Zb43) and T. delbrueckii (Td Pt) performed in natural must yielded ethanol reductions of 1.02 and 0.84% (v/v), respectively.

ACS Style

Xiaolin Zhu; Yurena Navarro; Albert Mas; María-Jesús Torija; Gemma Beltran. A Rapid Method for Selecting Non-Saccharomyces Strains with a Low Ethanol Yield. Microorganisms 2020, 8, 658 .

AMA Style

Xiaolin Zhu, Yurena Navarro, Albert Mas, María-Jesús Torija, Gemma Beltran. A Rapid Method for Selecting Non-Saccharomyces Strains with a Low Ethanol Yield. Microorganisms. 2020; 8 (5):658.

Chicago/Turabian Style

Xiaolin Zhu; Yurena Navarro; Albert Mas; María-Jesús Torija; Gemma Beltran. 2020. "A Rapid Method for Selecting Non-Saccharomyces Strains with a Low Ethanol Yield." Microorganisms 8, no. 5: 658.

Article
Published: 23 April 2019 in Nature Communications
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Bacteria of the genera Pseudomonas and Bacillus can promote plant growth and protect plants from pathogens. However, the interactions between these plant-beneficial bacteria are understudied. Here, we explore the interaction between Bacillus subtilis 3610 and Pseudomonas chlororaphis PCL1606. We show that the extracellular matrix protects B. subtilis colonies from infiltration by P. chlororaphis. The absence of extracellular matrix results in increased fluidity and loss of structure of the B. subtilis colony. The P. chlororaphis type VI secretion system (T6SS) is activated upon contact with B. subtilis cells, and stimulates B. subtilis sporulation. Furthermore, we find that B. subtilis sporulation observed prior to direct contact with P. chlororaphis is mediated by histidine kinases KinA and KinB. Finally, we demonstrate the importance of the extracellular matrix and the T6SS in modulating the coexistence of the two species on melon plant leaves and seeds. Pseudomonas and Bacillus can promote plant growth but their mutual interactions are unclear. Here, the authors show that the extracellular matrix protects Bacillus colonies from infiltration by Pseudomonas cells, while the Pseudomonas type VI secretion system stimulates Bacillus sporulation.

ACS Style

Carlos Molina-Santiago; John R. Pearson; Yurena Navarro; María Victoria Berlanga-Clavero; Andrés Mauricio Caraballo-Rodriguez; Daniel Petras; María Luisa García-Martín; Gaelle Lamon; Birgit Haberstein; Francisco M. Cazorla; Antonio de Vicente; Antoine Loquet; Pieter C. Dorrestein; Diego Romero. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nature Communications 2019, 10, 1 -15.

AMA Style

Carlos Molina-Santiago, John R. Pearson, Yurena Navarro, María Victoria Berlanga-Clavero, Andrés Mauricio Caraballo-Rodriguez, Daniel Petras, María Luisa García-Martín, Gaelle Lamon, Birgit Haberstein, Francisco M. Cazorla, Antonio de Vicente, Antoine Loquet, Pieter C. Dorrestein, Diego Romero. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nature Communications. 2019; 10 (1):1-15.

Chicago/Turabian Style

Carlos Molina-Santiago; John R. Pearson; Yurena Navarro; María Victoria Berlanga-Clavero; Andrés Mauricio Caraballo-Rodriguez; Daniel Petras; María Luisa García-Martín; Gaelle Lamon; Birgit Haberstein; Francisco M. Cazorla; Antonio de Vicente; Antoine Loquet; Pieter C. Dorrestein; Diego Romero. 2019. "The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization." Nature Communications 10, no. 1: 1-15.

Journal article
Published: 01 May 2017 in Journal of Clinical Microbiology
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Clonal complexity is increasingly accepted in Mycobacterium tuberculosis infection, including mixed infections by ≥2 strains, which usually occur in settings with a high burden of tuberculosis and/or a high risk of overexposure to infected patients. Mixed infections can hamper diagnostic procedures; obtaining an accurate antibiogram is difficult when the susceptibility patterns of the strains differ. Here, we show how mixed infections can also prove challenging for other diagnostic procedures, even outside settings where mixed infections are traditionally expected. We show how an unnoticed mixed infection in an HIV-positive patient diagnosed in Madrid, Spain, with differences in the representativeness of the coinfecting strains in different sputum samples, markedly complicated the resolution of a laboratory cross-contamination false positivity alert.

ACS Style

Laura Pérez-Lago; Marta Herranz; Yurena Navarro; María Jesús Ruiz Serrano; Pilar Miralles; Emilio Bouza; Darío García-De-Viedma. Clonal Complexity in Mycobacterium tuberculosis Can Hamper Diagnostic Procedures. Journal of Clinical Microbiology 2017, 55, 1388 -1395.

AMA Style

Laura Pérez-Lago, Marta Herranz, Yurena Navarro, María Jesús Ruiz Serrano, Pilar Miralles, Emilio Bouza, Darío García-De-Viedma. Clonal Complexity in Mycobacterium tuberculosis Can Hamper Diagnostic Procedures. Journal of Clinical Microbiology. 2017; 55 (5):1388-1395.

Chicago/Turabian Style

Laura Pérez-Lago; Marta Herranz; Yurena Navarro; María Jesús Ruiz Serrano; Pilar Miralles; Emilio Bouza; Darío García-De-Viedma. 2017. "Clonal Complexity in Mycobacterium tuberculosis Can Hamper Diagnostic Procedures." Journal of Clinical Microbiology 55, no. 5: 1388-1395.

Original research article
Published: 24 April 2017 in Frontiers in Microbiology
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The role of clonal complexity has gradually been accepted in infection by Mycobacterium tuberculosis (MTB), although analyses of this issue are limited. We performed an in-depth study of a case of recurrent MTB infection by integrating genotyping, whole genome sequencing, analysis of gene expression and infectivity in in vitro and in vivo models. Four different clonal variants were identified from independent intrapatient evolutionary branches. One of the single-nucleotide polymorphisms in the variants mapped in mce3R, which encodes a repressor of an operon involved in virulence, and affected expression of the operon. Competitive in vivo and in vitro coinfection assays revealed higher infective efficiency for one of the clonal variants. A new clonal variant, which had not been observed in the clinical isolates, emerged in the infection assays and showed higher fitness than its parental strain. The analysis of other patients involved in the same transmission cluster revealed new clonal variants acquired through novel evolutionary routes, indicating a high tendency toward microevolution in some strains that is not host-dependent. Our study highlights the need for integration of various approaches to advance our knowledge of the role and significance of microevolution in tuberculosis.

ACS Style

Yurena Navarro; Laura Pérez-Lago; Marta Herranz; Olalla Sierra; Iñaki Comas; Javier Sicilia; Emilio Bouza; Darío García De Viedma. In-Depth Characterization and Functional Analysis of Clonal Variants in a Mycobacterium tuberculosis Strain Prone to Microevolution. Frontiers in Microbiology 2017, 8, 694 .

AMA Style

Yurena Navarro, Laura Pérez-Lago, Marta Herranz, Olalla Sierra, Iñaki Comas, Javier Sicilia, Emilio Bouza, Darío García De Viedma. In-Depth Characterization and Functional Analysis of Clonal Variants in a Mycobacterium tuberculosis Strain Prone to Microevolution. Frontiers in Microbiology. 2017; 8 ():694.

Chicago/Turabian Style

Yurena Navarro; Laura Pérez-Lago; Marta Herranz; Olalla Sierra; Iñaki Comas; Javier Sicilia; Emilio Bouza; Darío García De Viedma. 2017. "In-Depth Characterization and Functional Analysis of Clonal Variants in a Mycobacterium tuberculosis Strain Prone to Microevolution." Frontiers in Microbiology 8, no. : 694.

Journal article
Published: 01 November 2016 in Veterinary Microbiology
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Human Mycobacterium bovis infections are considered to be due to reactivations, when involve elderly people, or to recent transmissions, when exposure is occupational. We determined the cause of M. bovis infections by genotyping M. bovis isolates in a population-based study integrating human and animal databases. Among the 1,586 tuberculosis (TB) cases in Asturias, Northern Spain (1,080,000 inhabitants), 1,567 corresponded to M. tuberculosis and 19 to M. bovis. The number of human isolates sharing genotype with cattle isolates was higher than expected (47%) for a setting with low prevalence of bovine TB and efficient control programs in cattle. The risk of exposure to infected animals was probable/possible in most of these matched cases (77.7%). Recent transmission was the likely explanation of most M. bovis infections in elderly people. A potential human-to-human transmission was found. Our study illustrates a model of collaboration between human and animal health professionals to provide a precise snapshot of the transmission of M. bovis in the human-animal interface.

ACS Style

Juan José Palacios; Yurena Navarro; Beatriz Romero; Ana Penedo; Ángela Menéndez González; M. Dolores Pérez Hernández; Ana Fernández-Verdugo; Francisca Copano; Aurora Torreblanca; Emilio Bouza; Lucas Domínguez; Lucía de Juan; Darío García-De-Viedma. Molecular and epidemiological population-based integrative analysis of human and animal Mycobacterium bovis infections in a low-prevalence setting. Veterinary Microbiology 2016, 195, 30 -36.

AMA Style

Juan José Palacios, Yurena Navarro, Beatriz Romero, Ana Penedo, Ángela Menéndez González, M. Dolores Pérez Hernández, Ana Fernández-Verdugo, Francisca Copano, Aurora Torreblanca, Emilio Bouza, Lucas Domínguez, Lucía de Juan, Darío García-De-Viedma. Molecular and epidemiological population-based integrative analysis of human and animal Mycobacterium bovis infections in a low-prevalence setting. Veterinary Microbiology. 2016; 195 ():30-36.

Chicago/Turabian Style

Juan José Palacios; Yurena Navarro; Beatriz Romero; Ana Penedo; Ángela Menéndez González; M. Dolores Pérez Hernández; Ana Fernández-Verdugo; Francisca Copano; Aurora Torreblanca; Emilio Bouza; Lucas Domínguez; Lucía de Juan; Darío García-De-Viedma. 2016. "Molecular and epidemiological population-based integrative analysis of human and animal Mycobacterium bovis infections in a low-prevalence setting." Veterinary Microbiology 195, no. : 30-36.

Journal article
Published: 01 February 2016 in Veterinary Microbiology
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Various studies have analyzed microevolution events leading to the emergence of clonal variants in human infections by Mycobacterium tuberculosis. However, microevolution events in animal tuberculosis remain unknown. We performed a systematic analysis of microevolution events in eight herds that were chronically infected by M. bovis for more than 12 months. We analyzed 88 animals using a systematic screening procedure based on discriminatory MIRU-VNTR genotyping at sequential time points during the infection. Microevolution was detected in half of the herds studied. Emergence of clonal variants did not require long infection periods or a high number of infected animals in the herd. Microevolution was not restricted to strains from specific spoligotypes, and the subtle variations detected involved different MIRU loci. The genetic locations of the subtle genotypic variations recorded in the clonal variants indicated potential functional significance. This finding was consistent with the dynamics of some clonal variants, which outcompeted the original strains, suggesting an advantageous phenotype. Our data constitute a first step in defining the thresholds of variability to be tolerated in molecular epidemiology studies of M. bovis. We could therefore ensure that related clonal variants emerging as a result of microevolution events are not going to be misinterpreted as unrelated isolates.

ACS Style

Yurena Navarro; Beatriz Romero; Emilio Bouza; Lucas Domínguez; Lucía de Juan; Darío García-De-Viedma. Detailed chronological analysis of microevolution events in herds infected persistently by Mycobacterium bovis. Veterinary Microbiology 2016, 183, 97 -102.

AMA Style

Yurena Navarro, Beatriz Romero, Emilio Bouza, Lucas Domínguez, Lucía de Juan, Darío García-De-Viedma. Detailed chronological analysis of microevolution events in herds infected persistently by Mycobacterium bovis. Veterinary Microbiology. 2016; 183 ():97-102.

Chicago/Turabian Style

Yurena Navarro; Beatriz Romero; Emilio Bouza; Lucas Domínguez; Lucía de Juan; Darío García-De-Viedma. 2016. "Detailed chronological analysis of microevolution events in herds infected persistently by Mycobacterium bovis." Veterinary Microbiology 183, no. : 97-102.

Letters to the editor
Published: 01 November 2015 in Emerging Infectious Diseases
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ACS Style

Laura Pérez-Lago; Miguel Martínez Lirola; Yurena Navarro; Marta Herranz; María Jesús Ruiz-Serrano; Emilio Bouza; Darío García-De-Viedma. Co-infection with Drug-Susceptible and Reactivated Latent Multidrug-ResistantMycobacterium tuberculosis. Emerging Infectious Diseases 2015, 21, 2098 -2100.

AMA Style

Laura Pérez-Lago, Miguel Martínez Lirola, Yurena Navarro, Marta Herranz, María Jesús Ruiz-Serrano, Emilio Bouza, Darío García-De-Viedma. Co-infection with Drug-Susceptible and Reactivated Latent Multidrug-ResistantMycobacterium tuberculosis. Emerging Infectious Diseases. 2015; 21 (11):2098-2100.

Chicago/Turabian Style

Laura Pérez-Lago; Miguel Martínez Lirola; Yurena Navarro; Marta Herranz; María Jesús Ruiz-Serrano; Emilio Bouza; Darío García-De-Viedma. 2015. "Co-infection with Drug-Susceptible and Reactivated Latent Multidrug-ResistantMycobacterium tuberculosis." Emerging Infectious Diseases 21, no. 11: 2098-2100.

Case reports
Published: 01 November 2015 in Journal of Clinical Microbiology
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The strains involved in tuberculosis outbreaks are considered highly virulent and transmissible. We analyzed the case of a patient in Madrid, Spain, who was persistently infected over an 8-year period by the same Beijing Mycobacterium tuberculosis strain. The strain was responsible for a severe outbreak on Gran Canaria Island. The case provides us with a unique opportunity to challenge our assumptions about M. tuberculosis Beijing strains. No clinical/radiological findings consistent with a virulent strain were documented, and the in vitro growth rate of the strain in macrophages was only moderate. No secondary cases stemming from this prolonged active case were detected in the host population. The strain did not acquire resistance mutations, despite constant treatment interruptions, and it remained extremely stable, as demonstrated by the lack of single-nucleotide-polymorphism (SNP)-based differences between the sequential isolates. Our data suggest that the general assumption about M. tuberculosis Beijing strains having advantageous properties (in terms of virulence, transmissibility, and the tendency to acquire mutations and resistance) is not always accurate.

ACS Style

Laura Pérez-Lago; Yurena Navarro; Pedro Montilla; Iñaki Comas; Marta Herranz; Carlos Rodríguez-Gallego; María Jesús Ruiz Serrano; Emilio Bouza; Darío García de Viedma. Persistent Infection by a Mycobacterium tuberculosis Strain That Was Theorized To Have Advantageous Properties, as It Was Responsible for a Massive Outbreak. Journal of Clinical Microbiology 2015, 53, 3423 -3429.

AMA Style

Laura Pérez-Lago, Yurena Navarro, Pedro Montilla, Iñaki Comas, Marta Herranz, Carlos Rodríguez-Gallego, María Jesús Ruiz Serrano, Emilio Bouza, Darío García de Viedma. Persistent Infection by a Mycobacterium tuberculosis Strain That Was Theorized To Have Advantageous Properties, as It Was Responsible for a Massive Outbreak. Journal of Clinical Microbiology. 2015; 53 (11):3423-3429.

Chicago/Turabian Style

Laura Pérez-Lago; Yurena Navarro; Pedro Montilla; Iñaki Comas; Marta Herranz; Carlos Rodríguez-Gallego; María Jesús Ruiz Serrano; Emilio Bouza; Darío García de Viedma. 2015. "Persistent Infection by a Mycobacterium tuberculosis Strain That Was Theorized To Have Advantageous Properties, as It Was Responsible for a Massive Outbreak." Journal of Clinical Microbiology 53, no. 11: 3423-3429.

Journal article
Published: 01 January 2015 in Veterinary Microbiology
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The combination of new genotyping tools and a more exhaustive sampling policy in the analysis of infection by Mycobacterium tuberculosis has shown that infection by this pathogen is more complex than initially expected. Mixed infections, coexistence of clonal variants from a parental strain, and compartmentalized infections are all different modalities of this clonal complexity. Until recently, genotyping of Mycobacterium bovis in animal populations was based on spoligotyping and analysis of a single isolate per infection; therefore, clonal complexity is probably underdetected. We used multiple sampling combined with highly discriminatory MIRU-VNTR to study compartmentalized infections by M. bovis in a low-tuberculosis prevalence setting. We spoligotyped the M. bovis isolates from two or more anatomic locations sampled from 55 animals on 39 independent farms. Compartmentalized infections, with two different strains infecting independent lymph nodes in the same animal, were found in six cases (10.9%). MIRU-VNTR analysis confirmed that the compartmentalization was strict and that only one strain was present in each infected node. MIRU-VNTR analysis of additional infected animals on one of the farms confirmed that the compartmentalized infection was a consequence of superinfection, since the two strains were independently infecting other animals. This same analysis revealed the emergence of a microevolved clonal variant in one of the lymph nodes of the compartmentalized animal. Clonal complexity must also be taken into consideration in M. bovis infection, even in low-prevalence settings, and analyses must be adapted to detect it and increase the accuracy of molecular epidemiology studies.

ACS Style

Yurena Navarro; Beatriz Romero; María Francisca Copano; Emilio Bouza; Lucas Domínguez; Lucia De Juan; Darío García-De-Viedma. Multiple sampling and discriminatory fingerprinting reveals clonally complex and compartmentalized infections by M. bovis in cattle. Veterinary Microbiology 2015, 175, 99 -104.

AMA Style

Yurena Navarro, Beatriz Romero, María Francisca Copano, Emilio Bouza, Lucas Domínguez, Lucia De Juan, Darío García-De-Viedma. Multiple sampling and discriminatory fingerprinting reveals clonally complex and compartmentalized infections by M. bovis in cattle. Veterinary Microbiology. 2015; 175 (1):99-104.

Chicago/Turabian Style

Yurena Navarro; Beatriz Romero; María Francisca Copano; Emilio Bouza; Lucas Domínguez; Lucia De Juan; Darío García-De-Viedma. 2015. "Multiple sampling and discriminatory fingerprinting reveals clonally complex and compartmentalized infections by M. bovis in cattle." Veterinary Microbiology 175, no. 1: 99-104.

Review
Published: 01 October 2014 in Research in Veterinary Science
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Mycobacterium bovis is both the causative agent of bovine tuberculosis (TB) and a zoonotic pathogen. In humans, considerably fewer cases of TB are caused by M. bovis than M. tuberculosis; nevertheless, diagnostic limitations mean that currently available data on prevalence grossly underestimate the true dimension of the problem. The routes of transmission from animals to humans are well known and include direct exposure to infected animals or consumption of contaminated animal products. Application of fingerprinting tools facilitates analysis of the molecular epidemiology of M. bovis in animal-to-human and human-to-human transmission. Apart from cattle and M. bovis, other animal species and members within the M. tuberculosis complex can contribute to the zoonosis. Improvements in diagnostic techniques, application of more advanced discriminatory genotyping tools, and collaboration between veterinary and human health care researchers are key to our understanding of this zoonosis.

ACS Style

Laura Pérez-Lago; Yurena Navarro; Darío García-De-Viedma. Current knowledge and pending challenges in zoonosis caused by Mycobacterium bovis: A review. Research in Veterinary Science 2014, 97, S94 -S100.

AMA Style

Laura Pérez-Lago, Yurena Navarro, Darío García-De-Viedma. Current knowledge and pending challenges in zoonosis caused by Mycobacterium bovis: A review. Research in Veterinary Science. 2014; 97 ():S94-S100.

Chicago/Turabian Style

Laura Pérez-Lago; Yurena Navarro; Darío García-De-Viedma. 2014. "Current knowledge and pending challenges in zoonosis caused by Mycobacterium bovis: A review." Research in Veterinary Science 97, no. : S94-S100.

Journal article
Published: 01 June 2014 in Research in Veterinary Science
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Spoligotyping is the most widely used method for genotyping Mycobacterium bovis (M. bovis). However, its discriminatory power varies widely between countries. MIRU-VNTR typing could be a promising alternative, although it generally requires the time consuming and laborious simplex PCR assays using standard agarose gel electrophoresis. The accuracy of this approach depends on good standardization and a certain degree of expertise. This study presents a version of MIRU-VNTR based on three triplex PCRs with automatic allelic assignation of the products analyzed in capillary electrophoresis. The technique was prospectively applied to 44 M. bovis and two Mycobacterium caprae (M. caprae) isolates, and 22 different MIRU-VNTRtypes were obtained; with spoligotyping, only 14 different types were obtained. The proposal makes it possible to shorten response times, automate procedures, and increase accuracy, thus minimizing errors in assigning genotypes. It would enable the switch from a standard limited method of genotyping M. bovis to a high-throughput discriminatory fingerprinting approach.

ACS Style

Yurena Navarro; M. Herranz; B. Romero; Emilio Bouza; L. Domínguez; L. De Juan; D. García-De-Viedma. High-throughput multiplex MIRU-VNTR typing of Mycobacterium bovis. Research in Veterinary Science 2014, 96, 422 -425.

AMA Style

Yurena Navarro, M. Herranz, B. Romero, Emilio Bouza, L. Domínguez, L. De Juan, D. García-De-Viedma. High-throughput multiplex MIRU-VNTR typing of Mycobacterium bovis. Research in Veterinary Science. 2014; 96 (3):422-425.

Chicago/Turabian Style

Yurena Navarro; M. Herranz; B. Romero; Emilio Bouza; L. Domínguez; L. De Juan; D. García-De-Viedma. 2014. "High-throughput multiplex MIRU-VNTR typing of Mycobacterium bovis." Research in Veterinary Science 96, no. 3: 422-425.

Journal article
Published: 01 December 2013 in International Journal of Medical Microbiology
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Clonal variants of Mycobacterium tuberculosis can emerge as a result of microevolution in a single host or after sequential infection of different hosts. The significance of subtle genotypic variations is still unknown. In three of the four loci analyzed from clonal variants differing in only one MIRU-VNTR locus, we found that the expression of the adjacent genes was modulated differently. These data highlight the potential advantages that acquisition of subtle variability may have in M. tuberculosis.

ACS Style

Laura Pérez-Lago; Yurena Navarro; Marta Herranz; Emilio Bouza; Darío García-De-Viedma. Differences in gene expression between clonal variants of Mycobacterium tuberculosis emerging as a result of microevolution. International Journal of Medical Microbiology 2013, 303, 674 -677.

AMA Style

Laura Pérez-Lago, Yurena Navarro, Marta Herranz, Emilio Bouza, Darío García-De-Viedma. Differences in gene expression between clonal variants of Mycobacterium tuberculosis emerging as a result of microevolution. International Journal of Medical Microbiology. 2013; 303 (8):674-677.

Chicago/Turabian Style

Laura Pérez-Lago; Yurena Navarro; Marta Herranz; Emilio Bouza; Darío García-De-Viedma. 2013. "Differences in gene expression between clonal variants of Mycobacterium tuberculosis emerging as a result of microevolution." International Journal of Medical Microbiology 303, no. 8: 674-677.

Journal article
Published: 01 December 2013 in International Journal of Medical Microbiology
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Clonal variants of Mycobacterium tuberculosis can emerge as a result of microevolution phenomena. The functional significance of these subtle genetic rearrangements is normally disregarded. We show that clonal variants from two patients had different infective behaviours in some in vitro cellular infection models but not in others. Microevolution may have a subtle impact on infectivity, but specific experimental conditions are needed to unmask it.

ACS Style

Yurena Navarro; Laura Pérez-Lago; Fernanda Sislema; Marta Herranz; Lucia De Juan; Emilio Bouza; Darío García-De-Viedma. Unmasking subtle differences in the infectivity of microevolved Mycobacterium tuberculosis variants coinfecting the same patient. International Journal of Medical Microbiology 2013, 303, 693 -696.

AMA Style

Yurena Navarro, Laura Pérez-Lago, Fernanda Sislema, Marta Herranz, Lucia De Juan, Emilio Bouza, Darío García-De-Viedma. Unmasking subtle differences in the infectivity of microevolved Mycobacterium tuberculosis variants coinfecting the same patient. International Journal of Medical Microbiology. 2013; 303 (8):693-696.

Chicago/Turabian Style

Yurena Navarro; Laura Pérez-Lago; Fernanda Sislema; Marta Herranz; Lucia De Juan; Emilio Bouza; Darío García-De-Viedma. 2013. "Unmasking subtle differences in the infectivity of microevolved Mycobacterium tuberculosis variants coinfecting the same patient." International Journal of Medical Microbiology 303, no. 8: 693-696.

Journal article
Published: 28 August 2013 in Journal of Clinical Microbiology
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Mycobacterium bovis populations in countries with persistent bovine tuberculosis usually show a prevalent spoligotype with a wide geographical distribution. This study applied mycobacterial interspersed repetitive-unit–variable-number tandem-repeat (MIRU-VNTR) typing to a random panel of 115 M. bovis isolates that are representative of the most frequent spoligotype in the Iberian Peninsula, SB0121. VNTR typing targeted nine loci: ETR-A (alias VNTR2165), ETR-B (VNTR2461), ETR-D (MIRU4, VNTR580), ETR-E (MIRU31, VNTR3192), MIRU26 (VNTR2996), QUB11a (VNTR2163a), QUB11b (VNTR2163b), QUB26 (VNTR4052), and QUB3232 (VNTR3232). We found a high degree of diversity among the studied isolates (discriminatory index [D] = 0.9856), which were split into 65 different MIRU-VNTR types. An alternative short-format MIRU-VNTR typing targeting only the four loci with the highest variability values was found to offer an equivalent discriminatory index. Minimum spanning trees using the MIRU-VNTR data showed the hypothetical evolution of an apparent clonal group. MIRU-VNTR analysis was also applied to the isolates of 176 animals from 15 farms infected by M. bovis SB0121; in 10 farms, the analysis revealed the coexistence of two to five different MIRU types differing in one to six loci, which highlights the frequency of undetected heterogeneity.

ACS Style

Sabrina Rodriguez-Campos; Yurena Navarro; Beatriz Romero; Lucía De Juan; Javier Bezos; Ana Mateos; Paul Golby; Noel H. Smith; Glyn R. Hewinson; Lucas Domínguez; Ana Isabel Mateos Garcia; Alicia Aranaz. Splitting of a Prevalent Mycobacterium bovis Spoligotype by Variable-Number Tandem-Repeat Typing Reveals High Heterogeneity in an Evolving Clonal Group. Journal of Clinical Microbiology 2013, 51, 3658 -3665.

AMA Style

Sabrina Rodriguez-Campos, Yurena Navarro, Beatriz Romero, Lucía De Juan, Javier Bezos, Ana Mateos, Paul Golby, Noel H. Smith, Glyn R. Hewinson, Lucas Domínguez, Ana Isabel Mateos Garcia, Alicia Aranaz. Splitting of a Prevalent Mycobacterium bovis Spoligotype by Variable-Number Tandem-Repeat Typing Reveals High Heterogeneity in an Evolving Clonal Group. Journal of Clinical Microbiology. 2013; 51 (11):3658-3665.

Chicago/Turabian Style

Sabrina Rodriguez-Campos; Yurena Navarro; Beatriz Romero; Lucía De Juan; Javier Bezos; Ana Mateos; Paul Golby; Noel H. Smith; Glyn R. Hewinson; Lucas Domínguez; Ana Isabel Mateos Garcia; Alicia Aranaz. 2013. "Splitting of a Prevalent Mycobacterium bovis Spoligotype by Variable-Number Tandem-Repeat Typing Reveals High Heterogeneity in an Evolving Clonal Group." Journal of Clinical Microbiology 51, no. 11: 3658-3665.

Journal article
Published: 14 August 2013 in Journal of Infectious Diseases
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It has been accepted that the infection by Mycobacterium tuberculosis (M. tuberculosis) can be more heterogeneous than considered. The emergence of clonal variants caused by microevolution events leading to population heterogeneity is a phenomenon largely unexplored. Until now, we could only superficially analyze this phenomenon by standard fingerprinting (RFLP and VNTR). In this study we applied whole genome sequencing for a more in-depth analysis of the scale of microevolution both at the intrapatient and interpatient scenarios. We found that the amount of variation accumulated within a patient can be as high as that observed between patients along a chain of transmission. Intrapatient diversity was found both at the extrapulmonary and respiratory sites, meaning that this variability can be transmitted and impact on the inference of transmission events. One of the events studied allowed us to track for a single strain the complete process of (i) interpatient microevolution, (ii) intrapatient respiratory variation, and (iii) isolation of different variants at different infected sites of this patient. Our study adds new data to the understanding of variability in M. tuberculosis in a wide clinical scenario and alerts about the difficulties of establishing thresholds to differentiate relatedness in M. tuberculosis with epidemiological purposes.

ACS Style

Laura Pérez-Lago; Iñaki Comas; Yurena Navarro; Fernando González-Candelas; Marta Herranz; Emilio Bouza; Darío García-De-Viedma. Whole Genome Sequencing Analysis of Intrapatient Microevolution in Mycobacterium tuberculosis: Potential Impact on the Inference of Tuberculosis Transmission. Journal of Infectious Diseases 2013, 209, 98 -108.

AMA Style

Laura Pérez-Lago, Iñaki Comas, Yurena Navarro, Fernando González-Candelas, Marta Herranz, Emilio Bouza, Darío García-De-Viedma. Whole Genome Sequencing Analysis of Intrapatient Microevolution in Mycobacterium tuberculosis: Potential Impact on the Inference of Tuberculosis Transmission. Journal of Infectious Diseases. 2013; 209 (1):98-108.

Chicago/Turabian Style

Laura Pérez-Lago; Iñaki Comas; Yurena Navarro; Fernando González-Candelas; Marta Herranz; Emilio Bouza; Darío García-De-Viedma. 2013. "Whole Genome Sequencing Analysis of Intrapatient Microevolution in Mycobacterium tuberculosis: Potential Impact on the Inference of Tuberculosis Transmission." Journal of Infectious Diseases 209, no. 1: 98-108.

Journal article
Published: 01 June 2013 in Infection, Genetics and Evolution
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Microevolved Mycobacterium tuberculosis (MTB) clonal variants from a parental strain can emerge within a single patient infection and during transmission events. Genotypic rearrangements may involve functional changes conferring advantages to favor strain adaptation to the host. In the present study, we analyzed in depth some genotypic characteristics of a strain with a high tendency to microevolve that generated 6 clonal variants during transmission of sequential hosts. In order to identify genetic features potentially associated to microevolution in MTB, we analyzed 56 3R genes and the IS6110 insertion sites from this strain and identified an SNP in alkA and an IS6110 copy located upstream of a transposase (Rv0755A). These markers could be involved in mechanisms leading to genotypic variation. Both features were shared by strains from our collection that were also involved in microevolution, suggesting their putative association with these events.

ACS Style

Laura Pérez-Lago; Yurena Navarro; Marta Herranz; Emilio Bouza; Darío García-De-Viedma. Genetic features shared by Mycobacterium tuberculosis strains involved in microevolution events. Infection, Genetics and Evolution 2013, 16, 326 -329.

AMA Style

Laura Pérez-Lago, Yurena Navarro, Marta Herranz, Emilio Bouza, Darío García-De-Viedma. Genetic features shared by Mycobacterium tuberculosis strains involved in microevolution events. Infection, Genetics and Evolution. 2013; 16 ():326-329.

Chicago/Turabian Style

Laura Pérez-Lago; Yurena Navarro; Marta Herranz; Emilio Bouza; Darío García-De-Viedma. 2013. "Genetic features shared by Mycobacterium tuberculosis strains involved in microevolution events." Infection, Genetics and Evolution 16, no. : 326-329.

Journal article
Published: 28 September 2011 in Journal of Clinical Microbiology
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Clonally complex infections by Mycobacterium tuberculosis are progressively more accepted. Studies of their dimension in epidemiological scenarios where the infective pressure is not high are scarce. Our study systematically searched for clonally complex infections (mixed infections by more than one strain and simultaneous presence of clonal variants) by applying mycobacterial interspersed repetitive-unit (MIRU)-variable-number tandem-repeat (VNTR) analysis to M. tuberculosis isolates from two population-based samples of respiratory (703 cases) and respiratory-extrapulmonary (R+E) tuberculosis (TB) cases (71 cases) in a context of moderate TB incidence. Clonally complex infections were found in 11 (1.6%) of the respiratory TB cases and in 10 (14.1%) of those with R+E TB. Among the 21 cases with clonally complex TB, 9 were infected by 2 independent strains and the remaining 12 showed the simultaneous presence of 2 to 3 clonal variants. For the 10 R+E TB cases with clonally complex infections, compartmentalization (different compositions of strains/clonal variants in independent infected sites) was found in 9 of them. All the strains/clonal variants were also genotyped by IS6110-based restriction fragment length polymorphism analysis, which split two MIRU-defined clonal variants, although in general, it showed a lower discriminatory power to identify the clonal heterogeneity revealed by MIRU-VNTR analysis. The comparative analysis of IS6110 insertion sites between coinfecting clonal variants showed differences in the genes coding for a cutinase, a PPE family protein, and two conserved hypothetical proteins. Diagnostic delay, existence of previous TB, risk for overexposure, and clustered/orphan status of the involved strains were analyzed to propose possible explanations for the cases with clonally complex infections. Our study characterizes in detail all the clonally complex infections by M. tuberculosis found in a systematic survey and contributes to the characterization that these phenomena can be found to an extent higher than expected, even in an unselected population-based sample lacking high infective pressure.

ACS Style

Y. Navarro; M. Herranz; L. Perez-Lago; M. Martinez Lirola; M. J. Ruiz-Serrano; E. Bouza; D. Garcia de Viedma; on behalf of Indal-Tb. Systematic Survey of Clonal Complexity in Tuberculosis at a Populational Level and Detailed Characterization of the Isolates Involved. Journal of Clinical Microbiology 2011, 49, 4131 -4137.

AMA Style

Y. Navarro, M. Herranz, L. Perez-Lago, M. Martinez Lirola, M. J. Ruiz-Serrano, E. Bouza, D. Garcia de Viedma, on behalf of Indal-Tb. Systematic Survey of Clonal Complexity in Tuberculosis at a Populational Level and Detailed Characterization of the Isolates Involved. Journal of Clinical Microbiology. 2011; 49 (12):4131-4137.

Chicago/Turabian Style

Y. Navarro; M. Herranz; L. Perez-Lago; M. Martinez Lirola; M. J. Ruiz-Serrano; E. Bouza; D. Garcia de Viedma; on behalf of Indal-Tb. 2011. "Systematic Survey of Clonal Complexity in Tuberculosis at a Populational Level and Detailed Characterization of the Isolates Involved." Journal of Clinical Microbiology 49, no. 12: 4131-4137.

Comparative study
Published: 01 March 2011 in Clinical Microbiology and Infection
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Genotypic analysis of Mycobacterium tuberculosis (MTB) has enabled the definition of several lineages. The Beijing family, which is considered highly virulent and transmissible, has been associated with resistance in certain settings and involved in severe outbreaks, making it one of the most closely-monitored lineages. Therefore, rapid prospective identification of Beijing MTB strains could be relevant. In the present study, we evaluate a real-time PCR followed by high-resolution melting (HRM) based on the identification of a single nucleotide polymorphism (SNP) in the Rv2629 gene which defines Beijing lineage (A191C for Beijing genotype and A191A for non-Beijing genotype). This combined methodology efficiently differentiated Beijing and non-Beijing strains in 100% of the isolates from a collection of reference strains without requiring specific DNA probes. Additionally, HRM was able to assign a Beijing/non-Beijing genotype in 90.9% of the respiratory specimens assayed. Its applicability was tested on a Peruvian sample of circulating MTB strains, in which it identified 10.7% as belonging to the Beijing genotype; this proportion reached 20% in the North Lima area. HRM analysis of the A191C SNP is a rapid, reliable, and sensitive method for the efficient prospective survey of high-risk Beijing MTB strains, even in developing settings where MTB culture is often not available.

ACS Style

M. Alonso; Yurena Navarro; F. Barletta; Miguel José Martinez-Lirola; E. Gotuzzo; Emilio Bouza; D. García De Viedma. A novel method for the rapid and prospective identification of Beijing Mycobacterium tuberculosis strains by high-resolution melting analysis. Clinical Microbiology and Infection 2011, 17, 349 -357.

AMA Style

M. Alonso, Yurena Navarro, F. Barletta, Miguel José Martinez-Lirola, E. Gotuzzo, Emilio Bouza, D. García De Viedma. A novel method for the rapid and prospective identification of Beijing Mycobacterium tuberculosis strains by high-resolution melting analysis. Clinical Microbiology and Infection. 2011; 17 (3):349-357.

Chicago/Turabian Style

M. Alonso; Yurena Navarro; F. Barletta; Miguel José Martinez-Lirola; E. Gotuzzo; Emilio Bouza; D. García De Viedma. 2011. "A novel method for the rapid and prospective identification of Beijing Mycobacterium tuberculosis strains by high-resolution melting analysis." Clinical Microbiology and Infection 17, no. 3: 349-357.