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Contrasting genes conferring short- and long-term biofilm adaptation in Listeria.

ABSTRACT: Listeria monocytogenes is an opportunistic food-borne bacterium that is capable of infecting humans with high rates of hospitalization and mortality. Natural populations are genotypically and phenotypically variable, with some lineages being responsible for most human infections. The success of L. monocytogenes is linked to its capacity to persist on food and in the environment. Biofilms are an important feature that allow these bacteria to persist and infect humans, so understanding the genetic basis of biofilm formation is key to understanding transmission. We sought to investigate the biofilm-forming ability of L. monocytogenes by identifying genetic variation that underlies biofilm formation in natural populations using genome-wide association studies (GWAS). Changes in gene expression of specific strains during biofilm formation were then investigated using RNA sequencing (RNA-seq). Genetic variation associated with enhanced biofilm formation was identified in 273 genes by GWAS and differential expression in 220 genes by RNA-seq. Statistical analyses show that the number of overlapping genes flagged by either type of experiment is less than expected by random sampling. This novel finding is consistent with an evolutionary scenario where rapid adaptation is driven by variation in gene expression of pioneer genes, and this is followed by slower adaptation driven by nucleotide changes within the core genome.

SUBMITTER: Monteith W

PROVIDER: S-EPMC10634452 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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Contrasting genes conferring short- and long-term biofilm adaptation in Listeria.

Monteith William W Pascoe Ben B Mourkas Evangelos E Clark Jack J Hakim Maliha M Hitchings Matthew D MD McCarthy Noel N Yahara Koji K Asakura Hiroshi H Sheppard Samuel K SK

Microbial genomics 20231001 10

Listeria monocytogenes is an opportunistic food-borne bacterium that is capable of infecting humans with high rates of hospitalization and mortality. Natural populations are genotypically and phenotypically variable, with some lineages being responsible for most human infections. The success of L. monocytogenes is linked to its capacity to persist on food and in the environment. Biofilms are an important feature that allow these bacteria to persist and infect humans, so understandi ...[more]

PMID: 37850975

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Project description:Listeria monocytogenes is a foodborne pathogen that can cause invasive severe human illness (listeriosis) in susceptible patients. Most human listeriosis cases appear to be caused by consumption of refrigerated ready-to-eat foods. Although initial contamination levels in foods are usually low, the ability of these bacteria to survive and multiply at low temperatures allows it to reach levels high enough to cause disease. This study explores the set of proteins that might have an association with L. monocytogenes adaptation to different temperatures. Cultures were grown in biofilm, the most widespread mode of growth in natural and industrial realms. Protein extractions were performed from three different growth temperatures (10, 25, and 37°C) and two growth phases (early stage and mature biofilm). L. monocytogenes subproteomes were targeted using three extraction methods: trypsin-enzymatic shaving, biotin-labeling and cell fractionation. The different subproteomes obtained were separated and analyzed by shotgun proteomics using high-performance liquid chromatography combined with tandem mass spectrometry (LC-OrbiTrap LTQVelos, ThermoFisher Scientific). A total of 141 (biotinylation), 98 (shaving) and 910 (fractionation) proteins were identified. Throughout the 920 unique proteins identified, many are connected to basic cell functions, but some are linked with thermoregulation. We observed some noteworthy protein abundance shifts associated with the major adaptation to cold mechanisms present in L. monocytogenes, namely: the role of ribosomes and the stressosome with a higher abundance of the general stress protein Ctc (Rl25) and the general stress transcription factor sigma B (σB), changes in cell fluidity and motility seen by higher levels of foldase protein PrsA2 and flagellin (FlaA), the uptake of osmolytes with a higher abundance of glycine betaine (GbuB) and carnitine transporters (OpucA), and the relevance of the overexpression of chaperone proteins such as cold shock proteins (CspLA and Dps). As for 37°C, we observed a significantly higher percentage of proteins associated with transcriptional or translational activity present in higher abundance upon comparison with the colder settings. These contrasts of protein expression throughout several conditions will enrich databases and help to model the regulatory circuitry that drives adaptation of L. monocytogenes to environments.

Project description:BackgroundSaccharomyces cerevisiae senses hyperosmotic conditions via the HOG signaling network that activates the stress-activated protein kinase, Hog1, and modulates metabolic fluxes and gene expression to generate appropriate adaptive responses. The integral control mechanism by which Hog1 modulates glycerol production remains uncharacterized. An additional Hog1-independent mechanism retains intracellular glycerol for adaptation. Candida albicans also adapts to hyperosmolarity via a HOG signaling network. However, it remains unknown whether Hog1 exerts integral or proportional control over glycerol production in C. albicans.ResultsWe combined modeling and experimental approaches to study osmotic stress responses in S. cerevisiae and C. albicans. We propose a simple ordinary differential equation (ODE) model that highlights the integral control that Hog1 exerts over glycerol biosynthesis in these species. If integral control arises from a separation of time scales (i.e. rapid HOG activation of glycerol production capacity which decays slowly under hyperosmotic conditions), then the model predicts that glycerol production rates elevate upon adaptation to a first stress and this makes the cell adapts faster to a second hyperosmotic stress. It appears as if the cell is able to remember the stress history that is longer than the timescale of signal transduction. This is termed the long-term stress memory. Our experimental data verify this. Like S. cerevisiae, C. albicans mimimizes glycerol efflux during adaptation to hyperosmolarity. Also, transient activation of intermediate kinases in the HOG pathway results in a short-term memory in the signaling pathway. This determines the amplitude of Hog1 phosphorylation under a periodic sequence of stress and non-stressed intervals. Our model suggests that the long-term memory also affects the way a cell responds to periodic stress conditions. Hence, during osmohomeostasis, short-term memory is dependent upon long-term memory. This is relevant in the context of fungal responses to dynamic and changing environments.ConclusionsOur experiments and modeling have provided an example of identifying integral control that arises from time-scale separation in different processes, which is an important functional module in various contexts.

Dataset Information

Contrasting genes conferring short- and long-term biofilm adaptation in Listeria.

Publications

Contrasting genes conferring short- and long-term biofilm adaptation in <i>Listeria</i>.

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