Mucoid switch in Burkholderia cepacia complex bacteria: Triggers, molecular mechanisms and implications in pathogenesis

Ferreira, Mirela R.; Gomes, Sara; Moreira, Leonilde M.

doi:10.1016/bs.aambs.2019.03.001

Cited by 7 publications

(15 citation statements)

References 78 publications

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“…The third mechanism is a combination of both in which repression of bce genes expression could be achieved by lowering the number of regulatory proteins and by increasing of H-NS proteins at the promoter regions of those bce genes. So far, only two response regulators, OmpR and NtrC, from the signal transduction systems EnvZ/OmpR and NtrB/NtrC, respectively, have been implicated in the regulation of cepacian biosynthesis in Burkholderia (12,13,35), but it is unknown whether these regulators bind directly to the bce gene regions or not. The expression data presented here shows that neither ompR nor ntrC genes are differentially expressed in 17616nmv compared with the wild-type strain, suggesting that repression by Bmul_0158 H-NS-like protein at the bce promoters is the most likely mechanism for cepacian biosynthesis regulation.…”

Section: Discussionmentioning

confidence: 99%

“…Although the regulation of bce genes´ expression directing cepacian biosynthesis is not yet fully understood, the NtrBC signal transduction system and the alternative sigma factor σ 54 have been implicated in regulating their expression in B. cenocepacia H111. In B. multivorans, another signal transduction system, EnvZ/OmpR, was identified as responsible for EPS biosynthesis, as nonmucoid colonies obtained under stress conditions accumulated mutations in ompR gene (12,13). The possible involvement of sRNAs in cepacian biosynthesis regulation comes from the observation that a mutant in the B. contaminans IST408 RNA chaperone Hfq produces 50% less EPS than the wild-type strain, although no specific sRNA has been identified (14).…”

Section: Introductionmentioning

confidence: 99%

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A Histone-Like Nucleoid Structuring Protein Regulates Several Virulence Traits in Burkholderia multivorans

Gomes

Ferreira

Tavares

et al. 2021

Appl Environ Microbiol

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Burkholderia cepacia complex bacteria comprises opportunistic pathogens causing chronic respiratory infections in cystic fibrosis (CF) patients. These microorganisms produce an exopolysaccharide named cepacian, which is considered a virulence determinant. To find genes implicated in the regulation of cepacian biosynthesis, we characterized an evolved nonmucoid variant (17616nmv) derived from the ancestor, Burkholderia multivorans ATCC 17616, after prolonged stationary phase. Lack of cepacian biosynthesis was correlated with downregulation of the expression of bce genes implicated in its biosynthesis. Furthermore, genome sequencing of the variant identified the transposition of the mobile element IS406 upstream the coding sequence of an hns-like gene (Bmul_0158) encoding a histone-like nucleoid structuring protein, a known global transcriptional repressor. This IS element upregulated the expression of Bmul_0158 by 4-fold. Transcriptome analysis identified the global effects of this mutation on gene expression, with major changes in genes implicated in motility, pili synthesis, type VI secretion, and chromosome associated functions. Concomitant with these differences, the nonmucoid variant displays reduced adherence to a CF lung bronchial cell line, reduced surface hydrophobicity, forms smaller cellular aggregates, but has an increase in swimming and swarming motilities. Finally, analysis of the GC content of the upstream region of differentially expressed genes led to the identification of various genomic regions, possibly acquired by horizontal gene transfer, which were transcriptionally repressed by the increased expression of Bmul_0158 gene in the 17616nmv strain. Taken together, the results revealed a significant role for this H-NS protein in the regulation of B. multivorans persistence- and virulence-associated genes. IMPORTANCE Members of the histone-like nucleoid-structuring (H-NS) family of proteins, present in many bacteria, are important global regulators of gene expression. Many of the regulated genes were acquired horizontally and include pathogenicity islands and prophages, among others. Additionally, H-NS can play a structural role by bridging and compacting DNA, presenting a crucial role in cell physiology. Several virulence phenotypes have been frequently identified in several bacteria as dependent on H-NS activity. Here, we describe an H-NS-like protein of the opportunistic pathogen Burkholderia multivorans, a species commonly infecting the respiratory tract of cystic fibrosis patients. Our results indicate that this protein is involved in regulating virulence traits such as exopolysaccharide biosynthesis, adhesion to biotic surfaces, cellular aggregation, and motility. Furthermore, this H-NS-like protein, is one out of eight orthologs present in B. multivorans ATCC 17616 genome, posing relevant questions to be investigated on how these proteins coordinate the expression of virulence traits.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A Histone-Like Nucleoid Structuring Protein Regulates Several Virulence Traits in Burkholderia multivorans

Gomes

Ferreira

Tavares

et al. 2021

Appl Environ Microbiol

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“…Burkholderia gladioli contains a genome made up of 9.05 Mb, two chromosomes and four plasmids, suggesting that the size of its genome is related to its ability to colonize different ecological niches (Mannaa et al, 2018). In addition, Burkholderia sensu lato has different virulence factors such as type I, II, III, IV and V secretion systems, adhesins, pilis, siderophores, extracellular proteases, various polysaccharides, and quorum sensing molecules (Ferreira et al, 2019).…”

Section: Fully Bilingualmentioning

confidence: 99%

Polyphasic characterization of Burkholderia gladioli isolated from onion and evaluation of its potential pathogenicity for other crops

Serret-López

Aranda-Ocampo

Espinosa-Victoria

et al. 2020

RMF

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Los individuos del género Burkholderia, sensu lato, se caracterizan por colonizar diversos nichos ecológicos. Esta investigación tuvo como objetivos caracterizar morfológica, fisiológica, bioquímica y molecularmente a Burkholderia gladioli, aislada de bulbos podridos de cebolla blanca (Allium cepa), y determinar su potencial como patógeno de otras especies vegetales. Burkholderia gladioli promovió, igualmente, la pudrición blanda en bulbos de cebolla morada (A. cepa), tallos de puerro (A. ampeloprasum), inflorescencias de brócoli (Brassica oleracea), cladodios de nopal (Opuntia indica), raíces de zanahoria (Daucus carota) y esporocarpos de champiñón (Agaricus bisporus). Burkholderia gladioli colonizó plantas de frijol (Phaseolus vulgaris) en invernadero y mostró resistencia natural in vitro a productos a base de cobre: cuprimicin agrícola, cuprimicin 500, phyton, oxicloruro de cobre; antibióticos: bactrol, bactriomicin agrícola, kasumin, final bacter, quartz y biológicos: serenade polvo, fungifree y bacterbest. Este estudio reporta por primera vez la caracterización polifásica de B. gladioli en México. Este aislado bacteriano creció a pH 4.0 y 42 °C, lo que podría conferirle habilidad competitiva en suelos ácidos y condiciones semiáridas. Se demostró que tiene un amplio rango de hospederos en condiciones postcosecha, además de ser resistente a diferentes productos usados en campo para el control de fitopatógenos.

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“…In Burkholderia strains of the Burkholderia cepacia complex ( Bcc ), this is the main exopolysaccharide produced ( Cescutti et al, 2000 ; Conway et al, 2004 ; Ferreira et al, 2007 ; Cuzzi et al, 2014 ). In this group of opportunistic pathogens that can cause lung infections in cystic fibrosis (CF), immunocompromised or granulomatous disease patients, CEP was associated with bacterial persistence in the lung ( Conway et al, 2004 ; Cunha et al, 2004 ; Sousa et al, 2007 ; Zlosnik et al, 2011 ; Ferreira et al, 2019 ) and shown to act as a protective barrier against antibiotics and other stresses such as oxidative stress, desiccation, and metal ion stress ( Bylund et al, 2006 ; Benincasa et al, 2009 ; Ferreira et al, 2010 , 2011 ; Cuzzi et al, 2012 ). Importantly, many of these potentially pathogenic Bcc strains, which produce CEP, are also naturally associated with plants ( Coenye and Vandamme, 2003 ; Eberl and Vandamme, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

“…In Bcc members and other animal and plant pathogenic non- Bcc isolates, CEP is synthetized by two gene clusters ( bce -I and bce -II, for B. cepacia exopolysaccharide), which are separated by 130 to 314 kb ( Ferreira et al, 2010 ). Interestingly, in the genome of environmental strains previously belonging to the Burkholderia genus (e.g., P. phymatum STM815, P. xenovorans LB400, P. phytofirmans PsJN, P. graminis C4D1M, and Caballeronia glathei DSM 50014), the CEP genes are not separated, but are organized as a continuous gene cluster ( Moreira et al, 2003 ; Ferreira et al, 2010 , 2019 ).…”

Section: Introductionmentioning

confidence: 99%

The Exopolysaccharide Cepacian Plays a Role in the Establishment of the Paraburkholderia phymatum – Phaseolus vulgaris Symbiosis

et al. 2020

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Paraburkholderia phymatum is a rhizobial strain that belongs to the beta-proteobacteria, a group known to form efficient nitrogen-fixing symbioses within root nodules of several legumes, including the agriculturally important common bean. The establishment of the symbiosis requires the exchange of rhizobial and plant signals such as lipochitooligosaccharides (Nod factors), polysaccharides, and flavonoids. Inspection of the genome of the competitive rhizobium P. phymatum revealed the presence of several polysaccharide biosynthetic gene clusters. In this study, we demonstrate that bceN, a gene encoding a GDP-D-mannose 4,6-dehydratase, which is involved in the production of the exopolysaccharide cepacian, an important component of biofilms produced by closely related opportunistic pathogens of the Burkholderia cepacia complex (Bcc), is required for efficient plant colonization. Wild-type P. phymatum was shown to produce cepacian while a bceN mutant did not. Additionally, the bceN mutant produced a significantly lower amount of biofilm and formed less root nodules compared to the wild-type strain with Phaseolus vulgaris as host plant. Finally, expression of the operon containing bceN was induced by the presence of germinated P. vulgaris seeds under nitrogen limiting conditions suggesting a role of this polysaccharide in the establishment of this ecologically important symbiosis.

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Mucoid switch in Burkholderia cepacia complex bacteria: Triggers, molecular mechanisms and implications in pathogenesis

Cited by 7 publications

References 78 publications

A Histone-Like Nucleoid Structuring Protein Regulates Several Virulence Traits in Burkholderia multivorans

A Histone-Like Nucleoid Structuring Protein Regulates Several Virulence Traits in Burkholderia multivorans

Polyphasic characterization of Burkholderia gladioli isolated from onion and evaluation of its potential pathogenicity for other crops

The Exopolysaccharide Cepacian Plays a Role in the Establishment of the Paraburkholderia phymatum – Phaseolus vulgaris Symbiosis

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