Transcriptional portrait of M. bovis BCG during biofilm production shows genes differentially expressed during intercellular aggregation and substrate attachment

Abstract Mycobacterium tuberculosis and M. smegmatis form drug-tolerant biofilms through dedicated genetic programs. In support of a stepwise process regulating biofilm production in mycobacteria, it was shown elsewhere that lsr2 participates in intercellular aggregation, while groEL1 was required f...

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Autores principales: Mario Alberto Flores-Valdez, Michel de Jesús Aceves-Sánchez, Eliza J. R. Peterson, Nitin Baliga, Jorge Bravo-Madrigal, Miguel Ángel De la Cruz-Villegas, Miguel A. Ares, Sarah Born, Martin Voskuil, Nayeli Areli Pérez-Padilla, Mirna Burciaga-Flores, Tanya Amanda Camacho-Villegas, María Guadalupe Espinoza-Jorge
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spelling oai:doaj.org-article:2c128ef7180346aa9fd5d3b4273f0b572021-12-02T16:06:39ZTranscriptional portrait of M. bovis BCG during biofilm production shows genes differentially expressed during intercellular aggregation and substrate attachment10.1038/s41598-020-69152-22045-2322https://doaj.org/article/2c128ef7180346aa9fd5d3b4273f0b572020-07-01T00:00:00Zhttps://doi.org/10.1038/s41598-020-69152-2https://doaj.org/toc/2045-2322Abstract Mycobacterium tuberculosis and M. smegmatis form drug-tolerant biofilms through dedicated genetic programs. In support of a stepwise process regulating biofilm production in mycobacteria, it was shown elsewhere that lsr2 participates in intercellular aggregation, while groEL1 was required for biofilm maturation in M. smegmatis. Here, by means of RNA-Seq, we monitored the early steps of biofilm production in M. bovis BCG, to distinguish intercellular aggregation from attachment to a surface. Genes encoding for the transcriptional regulators dosR and BCG0114 (Rv0081) were significantly regulated and responded differently to intercellular aggregation and surface attachment. Moreover, a M. tuberculosis H37Rv deletion mutant in the Rv3134c-dosS-dosR regulon, formed less biofilm than wild type M. tuberculosis, a phenotype reverted upon reintroduction of this operon into the mutant. Combining RT-qPCR with microbiological assays (colony and surface pellicle morphologies, biofilm quantification, Ziehl–Neelsen staining, growth curve and replication of planktonic cells), we found that BCG0642c affected biofilm production and replication of planktonic BCG, whereas ethR affected only phenotypes linked to planktonic cells despite its downregulation at the intercellular aggregation step. Our results provide evidence for a stage-dependent expression of genes that contribute to biofilm production in slow-growing mycobacteria.Mario Alberto Flores-ValdezMichel de Jesús Aceves-SánchezEliza J. R. PetersonNitin BaligaJorge Bravo-MadrigalMiguel Ángel De la Cruz-VillegasMiguel A. AresSarah BornMartin VoskuilNayeli Areli Pérez-PadillaMirna Burciaga-FloresTanya Amanda Camacho-VillegasMaría Guadalupe Espinoza-JorgeNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 10, Iss 1, Pp 1-15 (2020)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Mario Alberto Flores-Valdez
Michel de Jesús Aceves-Sánchez
Eliza J. R. Peterson
Nitin Baliga
Jorge Bravo-Madrigal
Miguel Ángel De la Cruz-Villegas
Miguel A. Ares
Sarah Born
Martin Voskuil
Nayeli Areli Pérez-Padilla
Mirna Burciaga-Flores
Tanya Amanda Camacho-Villegas
María Guadalupe Espinoza-Jorge
Transcriptional portrait of M. bovis BCG during biofilm production shows genes differentially expressed during intercellular aggregation and substrate attachment
description Abstract Mycobacterium tuberculosis and M. smegmatis form drug-tolerant biofilms through dedicated genetic programs. In support of a stepwise process regulating biofilm production in mycobacteria, it was shown elsewhere that lsr2 participates in intercellular aggregation, while groEL1 was required for biofilm maturation in M. smegmatis. Here, by means of RNA-Seq, we monitored the early steps of biofilm production in M. bovis BCG, to distinguish intercellular aggregation from attachment to a surface. Genes encoding for the transcriptional regulators dosR and BCG0114 (Rv0081) were significantly regulated and responded differently to intercellular aggregation and surface attachment. Moreover, a M. tuberculosis H37Rv deletion mutant in the Rv3134c-dosS-dosR regulon, formed less biofilm than wild type M. tuberculosis, a phenotype reverted upon reintroduction of this operon into the mutant. Combining RT-qPCR with microbiological assays (colony and surface pellicle morphologies, biofilm quantification, Ziehl–Neelsen staining, growth curve and replication of planktonic cells), we found that BCG0642c affected biofilm production and replication of planktonic BCG, whereas ethR affected only phenotypes linked to planktonic cells despite its downregulation at the intercellular aggregation step. Our results provide evidence for a stage-dependent expression of genes that contribute to biofilm production in slow-growing mycobacteria.
format article
author Mario Alberto Flores-Valdez
Michel de Jesús Aceves-Sánchez
Eliza J. R. Peterson
Nitin Baliga
Jorge Bravo-Madrigal
Miguel Ángel De la Cruz-Villegas
Miguel A. Ares
Sarah Born
Martin Voskuil
Nayeli Areli Pérez-Padilla
Mirna Burciaga-Flores
Tanya Amanda Camacho-Villegas
María Guadalupe Espinoza-Jorge
author_facet Mario Alberto Flores-Valdez
Michel de Jesús Aceves-Sánchez
Eliza J. R. Peterson
Nitin Baliga
Jorge Bravo-Madrigal
Miguel Ángel De la Cruz-Villegas
Miguel A. Ares
Sarah Born
Martin Voskuil
Nayeli Areli Pérez-Padilla
Mirna Burciaga-Flores
Tanya Amanda Camacho-Villegas
María Guadalupe Espinoza-Jorge
author_sort Mario Alberto Flores-Valdez
title Transcriptional portrait of M. bovis BCG during biofilm production shows genes differentially expressed during intercellular aggregation and substrate attachment
title_short Transcriptional portrait of M. bovis BCG during biofilm production shows genes differentially expressed during intercellular aggregation and substrate attachment
title_full Transcriptional portrait of M. bovis BCG during biofilm production shows genes differentially expressed during intercellular aggregation and substrate attachment
title_fullStr Transcriptional portrait of M. bovis BCG during biofilm production shows genes differentially expressed during intercellular aggregation and substrate attachment
title_full_unstemmed Transcriptional portrait of M. bovis BCG during biofilm production shows genes differentially expressed during intercellular aggregation and substrate attachment
title_sort transcriptional portrait of m. bovis bcg during biofilm production shows genes differentially expressed during intercellular aggregation and substrate attachment
publisher Nature Portfolio
publishDate 2020
url https://doaj.org/article/2c128ef7180346aa9fd5d3b4273f0b57
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