Nutrient Availability and Biofilm Polysaccharide Shape the Bacillaene-Dependent Antagonism of Bacillus subtilis against Salmonella Typhimurium

Podnar, Eli; Erega, Andi; Danevčič, Tjaša; Kovačec, Eva; Lories, Bram; Steenackers, Hans; Mandić-Mulec, Ines

doi:10.1128/spectrum.01836-22

Cited by 11 publications

(5 citation statements)

References 77 publications

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“…9A). The increase in bacillaene concentration at this latter stage could also result from an increase in bacillaene production induced by the proximal presence of E. coli, as B. subtilis was previously shown to upregulate bacillaene biosynthetic genes in the presence of competitors (22,33). This multifunctionality of bacillaene makes it belong to the list of antibiotics shown to alter cellular processes or bacterial behaviours -including biofilm formation-at sub-MIC concentrations (20,36,37).…”

Section: Discussionmentioning

confidence: 95%

“…The copyright holder for this preprint (which this version posted July 9, 2023. ; https://doi.org/10.1101/2023.07.06.547952 doi: bioRxiv preprint formation by Campylobacter jejuni and Salmonella Typhimurium (22,23). How bacillaene affects biofilm formation by these microorganisms has, however, remained unclear.…”

Section: Discussionmentioning

confidence: 99%

“…We found that B. subtilis NCIB 3610 (abbreviated as 3610) strongly inhibits the production of curli amyloid fibers and hence impairs morphogenesis of E. coli W3110 biofilms. This inhibitory action on curli was found to be mediated by bacillaene, a hybrid non-ribosomal peptide (NRP)/polyketide (PK) metabolite first reported as a bacteriostatic antibiotic (21) and more recently shown to also affect biofilm formation by certain bacterial species (22,23). We found that bacillaene combines both antibiotic and the novel anti-curli functions in a concentration-dependent manner, highlighting bacillaene as a metabolite naturally optimized for microbial inhibition.…”

Section: Introductionmentioning

confidence: 91%

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Selective inhibition of the amyloid matrix ofEscherichia colibiofilms by a bifunctional microbial metabolite

Cordisco

Zanor

Moreno

et al. 2023

Preprint

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The propensity of bacteria to grow collectively in communities known as biofilms and their ability to overcome clinical treatments in this condition has become a major medical problem, emphasizing the need for anti-biofilm strategies. Antagonistic microbial interactions have extensively served as searching platforms for antibiotics, but their potential as sources for anti-biofilm compounds has barely been exploited. By screening for microorganisms that in agar-set pairwise interactions could antagonize Escherichia coli’s ability to form macrocolony biofilms, we found that the soil bacterium Bacillus subtilis strongly inhibits the synthesis of amyloid fibers –known as curli-, which are the primary extracellular matrix (ECM) components of E. coli biofilms. We identified bacillaene, a B. subtilis hybrid non-ribosomal peptide/polyketide metabolite, previously described as a bacteriostatic antibiotic, as the effector molecule. We found that bacillaene combines both antibiotic and anti-curli functions in a concentration-dependent order that potentiates the ecological competitiveness of B. subtilis, highlighting bacillaene as a metabolite naturally optimized for microbial inhibition. Our studies revealed that bacillaene inhibits curli by directly impeding the assembly of the CsgB and CsgA curli subunits into amyloid fibers. Moreover, we found that curli inhibition occurs despite E. coli attempts to reinforce its protective ECM by inducing curli genes via a RpoS-mediated competition sensing response trigged by the threatening presence of B. subtilis. Overall, our findings illustrate the relevance of exploring microbial interactions not only for finding compounds with novel and unique activities, but for uncovering additional functions of compounds previously categorized as antibiotics.

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Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 91%

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Selective inhibition of the amyloid matrix ofEscherichia colibiofilms by a bifunctional microbial metabolite

Cordisco

Zanor

Moreno

et al. 2023

Preprint

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“…The genus Bacillus contains many member species containing antimicrobial polyketide synthases ( pks ) ( Olishevska et al, 2019 ). B. subtilis pks has been shown to produce substances that inhibit Salmonella growth in co-culture ( Podnar et al, 2022 ). It has been long established that prophylactic use of antibiotics, even at sub-therapeutic levels, can adversely affect Salmonella colonization in several animal species, including chickens ( Sieburth, 1957 ; Evangelisti et al, 1975 ; Smith and Tucker, 1975 ).…”

Section: Discussionmentioning

confidence: 99%

Peeling back the many layers of competitive exclusion

Maurer,

Cheng,

Pedroso

et al. 2024

Front. Microbiol.

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Baby chicks administered a fecal transplant from adult chickens are resistant to Salmonella colonization by competitive exclusion. A two-pronged approach was used to investigate the mechanism of this process. First, Salmonella response to an exclusive (Salmonella competitive exclusion product, Aviguard®) or permissive microbial community (chicken cecal contents from colonized birds containing 7.85 Log10Salmonella genomes/gram) was assessed ex vivo using a S. typhimurium reporter strain with fluorescent YFP and CFP gene fusions to rrn and hilA operon, respectively. Second, cecal transcriptome analysis was used to assess the cecal communities’ response to Salmonella in chickens with low (≤5.85 Log10 genomes/g) or high (≥6.00 Log10 genomes/g) Salmonella colonization. The ex vivo experiment revealed a reduction in Salmonella growth and hilA expression following co-culture with the exclusive community. The exclusive community also repressed Salmonella’s SPI-1 virulence genes and LPS modification, while the anti-virulence/inflammatory gene avrA was upregulated. Salmonella transcriptome analysis revealed significant metabolic disparities in Salmonella grown with the two different communities. Propanediol utilization and vitamin B12 synthesis were central to Salmonella metabolism co-cultured with either community, and mutations in propanediol and vitamin B12 metabolism altered Salmonella growth in the exclusive community. There were significant differences in the cecal community’s stress response to Salmonella colonization. Cecal community transcripts indicated that antimicrobials were central to the type of stress response detected in the low Salmonella abundance community, suggesting antagonism involved in Salmonella exclusion. This study indicates complex community interactions that modulate Salmonella metabolism and pathogenic behavior and reduce growth through antagonism may be key to exclusion.

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“…B. subtilis is a versatile soil-dwelling bacterium capable of thriving in a wide range of environments, including terrestrial and aquatic environments, as well as humans and other animals. B. subtilis is widely used in the industrial production of enzymes and antibiotics 23 , controlling plant diseases and promoting plant growth 24 , improving gut health [25][26][27] , boosting immunity in mammals 28 , and promoting overall wellness of humans and animals [29][30][31] . B. subtilis species form highly resistant spores that can withstand exposure to UV, heat, desiccation, and lack of nutrients 32 .…”

Section: Introductionmentioning

confidence: 99%

Ecology of prophage-like elements inBacillus subtilisat global and local geographical scale

Stefanič,

Stare,

Floccari

et al. 2024

Preprint

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SummaryProphages account for a substantial part of most bacterial genomes, but the impacts on hosts remain poorly understood. Here, we combined computational and laboratory experiments to explore the abundance, distribution, and activity of prophage elements inBacillus subtilis. NCBI database genome sequences and isolates from 1 cm3riverbank soil samples were analyzed to provide insights at global and local geographical scales, respectively. Most prophages in wildB. subtilisisolates were related to mobile genetic elements previously identified in laboratory strains. Some large groups of prophages were closely related to completely uncharacterized yet functional Bacillus phages, or completely unknown. As certain prophage groups were unique to local isolates, we explored factors influencing prophages within a single genome. Phylogenetic relatedness was a slightly better predictor of host prophage repertoire than geographical origin. We show that cryptic phages can play a major role in acquisition and/or maintenance of other prophage elements both via strong antagonism or by co-dependence. Laboratory experiments showed that most predicted prophages may be cryptic, since they failed to induce under DNA-damaging stress conditions. Interestingly, the magnitude of stress responses remained proportional to the total number of prophage elements predicted, suggesting their importance in host physiology. This study highlights the diversity, integration patterns, and co-occurrence of prophages inB. subtilisand their potential impact on host evolution and physiology. Understanding these dynamics provides insight into bacterial genome evolution and prophage-host interactions, laying the groundwork for future experimental studies on the roles of phages in the ecology and evolution of this bacterial species.

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Nutrient Availability and Biofilm Polysaccharide Shape the Bacillaene-Dependent Antagonism of Bacillus subtilis against Salmonella Typhimurium

Cited by 11 publications

References 77 publications

Selective inhibition of the amyloid matrix ofEscherichia colibiofilms by a bifunctional microbial metabolite

Selective inhibition of the amyloid matrix ofEscherichia colibiofilms by a bifunctional microbial metabolite

Peeling back the many layers of competitive exclusion

Ecology of prophage-like elements inBacillus subtilisat global and local geographical scale

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