Inactivation of the Response Regulator AgrA Has a Pleiotropic Effect on Biofilm Formation, Pathogenesis and Stress Response in Staphylococcus lugdunensis

Aubourg, Marion; Pottier, Marine; Léon, Albertine; Bernay, Benoı̂t; Dhalluin, Anne; Cacaci, Margherita; Torelli, Riccardo; Ledormand, Pierre; Martini, Cécilia; Sanguinetti, Maurizio; Auzou, Michel; Gravey, François; Giard, Jean‐Christophe

doi:10.1128/spectrum.01598-21

Cited by 14 publications

(11 citation statements)

References 71 publications

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“…These broad patterns of DEGs support previous studies showing that SigB, Agr, and WalKR can have broad transcriptional control in Staphylococcus species and that mutations in these global regulators can dramatically alter transcriptional networks within these species (52,(82)(83)(84)(85)(86).…”

Section: Rna-seq Reveals Decreased Expression Of Key Metabolic Pathwa...supporting

confidence: 87%

Species interactions promote parallel evolution of global transcriptional regulators in a widespreadStaphylococcusspecies

Cosetta

Niccum

Kamkari

et al. 2022

Preprint

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Experimental studies of microbial evolution have largely focused on monocultures of model organisms, but most microbes live in communities where interactions with other species may impact rates and modes of evolution. Using the cheese rind model microbial community, we determined how species interactions shape the evolution of the widespread food- and animal-associated bacterium Staphylococcus xylosus. We evolved S. xylosus for 450 generations alone or in co-culture with one of three microbes: the yeast Debaryomyces hansenii, the bacterium Brevibacterium aurantiacum, and the mold Penicillium solitum. We used the frequency of colony morphology mutants (pigment and colony texture phenotypes) and whole-genome sequencing of isolates to quantify phenotypic and genomic evolution after 15 weeks of the evolution. The yeast D. hansenii strongly promoted diversification of S. xylosus; by the end of the experiment, all populations co-cultured with the yeast were dominated by pigment and colony morphology mutant phenotypes. Populations of S. xylosus grown alone, with Brevibacterium, or with Penicillium did not evolve novel phenotypic diversity. Whole-genome sequencing of individual mutant isolates across all four treatments revealed numerous unique mutations in the operons for the SigB, Agr, and WalKR global regulators, but only in the D. hansenii treatment. Phenotyping and RNA-seq experiments demonstrated that these mutations altered pigment and biofilm production, spreading, stress tolerance, and metabolism of S. xylosus. Fitness experiments revealed trade-offs of these mutations across biotic environments caused by antagonistic pleiotropy, where beneficial mutations that evolved in the presence of the yeast Debaryomyces had strong negative fitness effects in other biotic environments.

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Section: Rna-seq Reveals Decreased Expression Of Key Metabolic Pathwa...supporting

confidence: 87%

Species interactions promote parallel evolution of global transcriptional regulators in a widespreadStaphylococcusspecies

Cosetta

Niccum

Kamkari

et al. 2022

Preprint

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“…Inhibiting the function of AgrB could suppress AIP released into the extracellular environment [ 17 ]. The AgrA [ 20 ], AgrD [ 21 ], and AgrC [ 22 ] deletion mutants produced less biofilm. The lack of AgrA also impacted the ability to deal with osmotic and oxidative stress in Staphylococcus lugdunensis [ 20 ].…”

Section: Discussionmentioning

confidence: 99%

“…The AgrA [ 20 ], AgrD [ 21 ], and AgrC [ 22 ] deletion mutants produced less biofilm. The lack of AgrA also impacted the ability to deal with osmotic and oxidative stress in Staphylococcus lugdunensis [ 20 ]. High-temperature adaptation would increase biofilm formation [ 23 ].…”

Section: Discussionmentioning

confidence: 99%

Integrative Multiomics Analysis of the Heat Stress Response of Enterococcus faecium

Wang

Qiao

et al. 2023

Biomolecules

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A continuous heat-adaptation test was conducted for one Enterococcus faecium (E. faecium) strain wild-type (WT) RS047 to obtain a high-temperature-resistant strain. After domestication, the strain was screened with a significantly higher ability of heat resistance. which is named RS047-wl. Then a multi-omics analysis of transcriptomics and metabolomics was used to analyze the mechanism of the heat resistance of the mutant. A total of 98 differentially expressed genes (DEGs) and 115 differential metabolites covering multiple metabolic processes were detected in the mutant, which indicated that the tolerance of heat resistance was regulated by multiple mechanisms. The changes in AgrB, AgrC, and AgrA gene expressions were involved in quorum-sensing (QS) system pathways, which regulate biofilm formation. Second, highly soluble osmotic substances such as putrescine, spermidine, glycine betaine (GB), and trehalose-6P were accumulated for the membrane transport system. Third, organic acids metabolism and purine metabolism were down-regulated. The findings can provide target genes for subsequent genetic modification of E. faecium, and provide indications for screening heat-resistant bacteria, so as to improve the heat-resistant ability of E. faecium for production.

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“…Although all strains carried the ica locus, it is probably not the only cause of biofilm production. In staphylococci, several molecules other than polysaccharide intracellular adhesin (encoded by the ica operon) molecules have been shown to play an important role in biofilm formation, such as major autolysin Atl ( atlL ), the enzyme for D-alanine esterification of teichoic acids DltA ( dltA ), the iron-regulated surface determinant IsdC ( isdC ) under iron-limited conditions, and also the agr system, which is a component of the quorum-sensing agr system and is known to be a major element in the regulation of pathogenicity [ 30 , 31 , 32 ]. All tested S. lugdunensis strains possessed atlL , dltA , isdC , and agr genes.…”

Section: Discussionmentioning

confidence: 99%

May Staphylococcus lugdunensis Be an Etiological Factor of Chronic Maxillary Sinuses Infection?

Kosecka-Strojek

Wolska-Gębarzewska

Podbielska‐Kubera³

et al. 2022

IJMS

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Staphylococcus lugdunensis is an opportunistic pathogen found in the healthy human skin microbiome bacterial community that is able to cause infections of diverse localization, manifestation, and course, including laryngological infections, such as necrotizing sinusitis. Chronic maxillary sinusitis is a disease present in up to one third of European and American populations, and its etiology is not fully described. Within this study, we aimed to characterize 18 S. lugdunensis strains recovered from maxillary sinuses and evaluate them as etiological agents of chronic disease. We performed MLST analysis, the complex analysis of both phenotypic and genetic virulence factors, antibiotic susceptibility profiles, and biofilm formation assay for the detection of biofilm-associated genes. Altogether, S. lugdunensis strains were clustered into eight different STs, and we demonstrated several virulence factors associated with the chronic disease. All tested strains were able to produce biofilm in vitro with numerous strains with a very strong ability, and overall, they were mostly susceptible to antibiotics, although we found resistance to fosfomycin, erythromycin, and clindamycin in several strains. We believe that further in-depth analysis of S. lugdunensis strains from different niches, including the nasal one, should be performed in the future in order to reduce infection rate and broaden the knowledge about this opportunistic pathogen that is gaining attention.

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Inactivation of the Response Regulator AgrA Has a Pleiotropic Effect on Biofilm Formation, Pathogenesis and Stress Response in Staphylococcus lugdunensis

Cited by 14 publications

References 71 publications

Species interactions promote parallel evolution of global transcriptional regulators in a widespreadStaphylococcusspecies

Species interactions promote parallel evolution of global transcriptional regulators in a widespreadStaphylococcusspecies

Integrative Multiomics Analysis of the Heat Stress Response of Enterococcus faecium

May Staphylococcus lugdunensis Be an Etiological Factor of Chronic Maxillary Sinuses Infection?

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