Transcriptome Sequencing Reveals Wide Expression Reprogramming of Basal and Unknown Genes in <named-content content-type="genus-species">Leptospira biflexa</named-content> Biofilms

ABSTRACT The genus Leptospira is composed of pathogenic and saprophytic spirochetes. Pathogenic Leptospira is the etiological agent of leptospirosis, a globally spread neglected disease. A key ecological feature of some pathogenic species is their ability to survive both within and outside the host....

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Autores principales: Gregorio Iraola, Lucía Spangenberg, Bruno Lopes Bastos, Martín Graña, Larissa Vasconcelos, Áurea Almeida, Gonzalo Greif, Carlos Robello, Paula Ristow, Hugo Naya
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Publicado: American Society for Microbiology 2016
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spelling oai:doaj.org-article:809b6b2802f544bfb9ca793f2c83ad9e2021-11-15T15:21:22ZTranscriptome Sequencing Reveals Wide Expression Reprogramming of Basal and Unknown Genes in <named-content content-type="genus-species">Leptospira biflexa</named-content> Biofilms10.1128/mSphere.00042-162379-5042https://doaj.org/article/809b6b2802f544bfb9ca793f2c83ad9e2016-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00042-16https://doaj.org/toc/2379-5042ABSTRACT The genus Leptospira is composed of pathogenic and saprophytic spirochetes. Pathogenic Leptospira is the etiological agent of leptospirosis, a globally spread neglected disease. A key ecological feature of some pathogenic species is their ability to survive both within and outside the host. For most leptospires, the ability to persist outside the host is associated with biofilm formation, a most important bacterial strategy to face and overcome hostile environmental conditions. The architecture and biochemistry of leptospiral biofilms are rather well understood; however, the genetic program underpinning biofilm formation remains mostly unknown. In this work, we used the saprophyte Leptospira biflexa as a model organism to assess over- and underrepresented transcripts during the biofilm state, using transcriptome sequencing (RNA-seq) technology. Our results showed that some basal biological processes like DNA replication and cell division are downregulated in the mature biofilm. Additionally, we identified significant expression reprogramming for genes involved in motility, sugar/lipid metabolism, and iron scavenging, as well as for outer membrane-encoding genes. A careful manual annotation process allowed us to assign molecular functions to many previously uncharacterized genes that are probably involved in biofilm metabolism. We also provided evidence for the presence of small regulatory RNAs in this species. Finally, coexpression networks were reconstructed to pinpoint functionally related gene clusters that may explain how biofilm maintenance is regulated. Beyond elucidating some genetic aspects of biofilm formation, this work reveals a number of pathways whose functional dissection may impact our understanding of leptospiral biology, in particular how these organisms adapt to environmental changes. IMPORTANCE In this work, we describe the first transcriptome based on RNA-seq technology focused on studying transcriptional changes associated with biofilm growth in a member of the genus Leptospira. As many pathogenic species of this genus can survive inside the host but also persist in environmental water, mostly forming biofilms, identifying the molecular basis of this capacity can impact the understanding of how leptospires are able to fulfill a complete life cycle that alternates between adaptation to the host and adaptation to hostile external environmental conditions. We identified several genes and regulatory networks that can be the kickoff for deepening understanding of the molecular mechanisms involving bacterial persistence via biofilm formation; understanding this is important for the future development of tools for controlling leptospirosis.Gregorio IraolaLucía SpangenbergBruno Lopes BastosMartín GrañaLarissa VasconcelosÁurea AlmeidaGonzalo GreifCarlos RobelloPaula RistowHugo NayaAmerican Society for MicrobiologyarticleLeptospiraRNA sequencingbiofilmsgene expressiontranscriptomicsMicrobiologyQR1-502ENmSphere, Vol 1, Iss 2 (2016)
institution DOAJ
collection DOAJ
language EN
topic Leptospira
RNA sequencing
biofilms
gene expression
transcriptomics
Microbiology
QR1-502
spellingShingle Leptospira
RNA sequencing
biofilms
gene expression
transcriptomics
Microbiology
QR1-502
Gregorio Iraola
Lucía Spangenberg
Bruno Lopes Bastos
Martín Graña
Larissa Vasconcelos
Áurea Almeida
Gonzalo Greif
Carlos Robello
Paula Ristow
Hugo Naya
Transcriptome Sequencing Reveals Wide Expression Reprogramming of Basal and Unknown Genes in <named-content content-type="genus-species">Leptospira biflexa</named-content> Biofilms
description ABSTRACT The genus Leptospira is composed of pathogenic and saprophytic spirochetes. Pathogenic Leptospira is the etiological agent of leptospirosis, a globally spread neglected disease. A key ecological feature of some pathogenic species is their ability to survive both within and outside the host. For most leptospires, the ability to persist outside the host is associated with biofilm formation, a most important bacterial strategy to face and overcome hostile environmental conditions. The architecture and biochemistry of leptospiral biofilms are rather well understood; however, the genetic program underpinning biofilm formation remains mostly unknown. In this work, we used the saprophyte Leptospira biflexa as a model organism to assess over- and underrepresented transcripts during the biofilm state, using transcriptome sequencing (RNA-seq) technology. Our results showed that some basal biological processes like DNA replication and cell division are downregulated in the mature biofilm. Additionally, we identified significant expression reprogramming for genes involved in motility, sugar/lipid metabolism, and iron scavenging, as well as for outer membrane-encoding genes. A careful manual annotation process allowed us to assign molecular functions to many previously uncharacterized genes that are probably involved in biofilm metabolism. We also provided evidence for the presence of small regulatory RNAs in this species. Finally, coexpression networks were reconstructed to pinpoint functionally related gene clusters that may explain how biofilm maintenance is regulated. Beyond elucidating some genetic aspects of biofilm formation, this work reveals a number of pathways whose functional dissection may impact our understanding of leptospiral biology, in particular how these organisms adapt to environmental changes. IMPORTANCE In this work, we describe the first transcriptome based on RNA-seq technology focused on studying transcriptional changes associated with biofilm growth in a member of the genus Leptospira. As many pathogenic species of this genus can survive inside the host but also persist in environmental water, mostly forming biofilms, identifying the molecular basis of this capacity can impact the understanding of how leptospires are able to fulfill a complete life cycle that alternates between adaptation to the host and adaptation to hostile external environmental conditions. We identified several genes and regulatory networks that can be the kickoff for deepening understanding of the molecular mechanisms involving bacterial persistence via biofilm formation; understanding this is important for the future development of tools for controlling leptospirosis.
format article
author Gregorio Iraola
Lucía Spangenberg
Bruno Lopes Bastos
Martín Graña
Larissa Vasconcelos
Áurea Almeida
Gonzalo Greif
Carlos Robello
Paula Ristow
Hugo Naya
author_facet Gregorio Iraola
Lucía Spangenberg
Bruno Lopes Bastos
Martín Graña
Larissa Vasconcelos
Áurea Almeida
Gonzalo Greif
Carlos Robello
Paula Ristow
Hugo Naya
author_sort Gregorio Iraola
title Transcriptome Sequencing Reveals Wide Expression Reprogramming of Basal and Unknown Genes in <named-content content-type="genus-species">Leptospira biflexa</named-content> Biofilms
title_short Transcriptome Sequencing Reveals Wide Expression Reprogramming of Basal and Unknown Genes in <named-content content-type="genus-species">Leptospira biflexa</named-content> Biofilms
title_full Transcriptome Sequencing Reveals Wide Expression Reprogramming of Basal and Unknown Genes in <named-content content-type="genus-species">Leptospira biflexa</named-content> Biofilms
title_fullStr Transcriptome Sequencing Reveals Wide Expression Reprogramming of Basal and Unknown Genes in <named-content content-type="genus-species">Leptospira biflexa</named-content> Biofilms
title_full_unstemmed Transcriptome Sequencing Reveals Wide Expression Reprogramming of Basal and Unknown Genes in <named-content content-type="genus-species">Leptospira biflexa</named-content> Biofilms
title_sort transcriptome sequencing reveals wide expression reprogramming of basal and unknown genes in <named-content content-type="genus-species">leptospira biflexa</named-content> biofilms
publisher American Society for Microbiology
publishDate 2016
url https://doaj.org/article/809b6b2802f544bfb9ca793f2c83ad9e
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