Regulation of colony morphology and biofilm formation in <i>Shewanella algae</i>

Martín‐Rodríguez, Alberto J.; Villion, Katia; Yilmaz-Turan, Secil; Vilaplana, Francisco; Sjöling, Åsa; Römling, Ute

doi:10.1111/1751-7915.13788

Cited by 7 publications

(4 citation statements)

References 56 publications

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“…Colony growth on plates depends on many factors, including the composition of the media (for example, available nutrients), atmospheric conditions (for example, level of oxygenation), presence of inhibitory molecules (for example, antibiotics), pH, humidity and effects of other diffusible metabolites derived from nearby colonies [18][19][20] . Different colony morphologies are observed based on strain-specific physiological differences, influenced by cell shape, rigidity, motility and growth kinetics, as well as production of pigmented molecules or extracellular matrices and surfactants [9][10][11][12] . Although these colony traits are readily quantifiable, they are rarely documented during colony isolation.…”

Section: Data-driven Culturomics Using Phenotypes and Automationmentioning

confidence: 99%

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High-throughput microbial culturomics using automation and machine learning

et al. 2023

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Pure bacterial cultures remain essential for detailed experimental and mechanistic studies in microbiome research, and traditional methods to isolate individual bacteria from complex microbial ecosystems are labor-intensive, difficult-to-scale and lack phenotype–genotype integration. Here we describe an open-source high-throughput robotic strain isolation platform for the rapid generation of isolates on demand. We develop a machine learning approach that leverages colony morphology and genomic data to maximize the diversity of microbes isolated and enable targeted picking of specific genera. Application of this platform on fecal samples from 20 humans yields personalized gut microbiome biobanks totaling 26,997 isolates that represented >80% of all abundant taxa. Spatial analysis on >100,000 visually captured colonies reveals cogrowth patterns between Ruminococcaceae, Bacteroidaceae, Coriobacteriaceae and Bifidobacteriaceae families that suggest important microbial interactions. Comparative analysis of 1,197 high-quality genomes from these biobanks shows interesting intra- and interpersonal strain evolution, selection and horizontal gene transfer. This culturomics framework should empower new research efforts to systematize the collection and quantitative analysis of imaging-based phenotypes with high-resolution genomics data for many emerging microbiome studies.

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Section: Data-driven Culturomics Using Phenotypes and Automationmentioning

confidence: 99%

“…Microbes can be distinguished based on their diverse phenotypes, whether by their ability to grow in certain media or the metabolites they produce [9][10][11][12] . Growth-based selection can enhance the isolation of rare species, for example, with growth media containing different nutrients or antibiotics 1,2,13 .…”

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confidence: 99%

High-throughput microbial culturomics using automation and machine learning

et al. 2023

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“…PNPase affects the formation and structure of Listeria monocytogenes biofilms Colony morphology and motility are two interconnected phenotypes known to affect the formation of bacterial biofilms 43,44 . To determine if the altered morphotype and motility defects found in the PNPase-mutant of Listeria monocytogenes could affect biofilm formation, we next compared the amount of biofilm produced by the wild-type, ΔpnpA and complemented strains.…”

Section: Inactivation Of Pnpase Leads To Mutant Phenotypes Of Listeri...mentioning

confidence: 99%

The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells

Quendera¹,

Pinto²,

Pobre³

et al. 2023

npj Biofilms Microbiomes

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Biofilms provide an environment that protects microorganisms from external stresses such as nutrient deprivation, antibiotic treatments, and immune defences, thereby creating favorable conditions for bacterial survival and pathogenesis. Here we show that the RNA-binding protein and ribonuclease polynucleotide phosphorylase (PNPase) is a positive regulator of biofilm formation in the human pathogen Listeria monocytogenes, a major responsible for food contamination in food-processing environments. The PNPase mutant strain produces less biofilm biomass and exhibits an altered biofilm morphology that is more susceptible to antibiotic treatment. Through biochemical assays and microscopical analysis, we demonstrate that PNPase is a previously unrecognized regulator of the composition of the biofilm extracellular matrix, greatly affecting the levels of proteins, extracellular DNA, and sugars. Noteworthy, we have adapted the use of the fluorescent complex ruthenium red-phenanthroline for the detection of polysaccharides in Listeria biofilms. Transcriptomic analysis of wild-type and PNPase mutant biofilms reveals that PNPase impacts many regulatory pathways associated with biofilm formation, particularly by affecting the expression of genes involved in the metabolism of carbohydrates (e.g., lmo0096 and lmo0783, encoding PTS components), of amino acids (e.g., lmo1984 and lmo2006, encoding biosynthetic enzymes) and in the Agr quorum sensing-like system (lmo0048-49). Moreover, we show that PNPase affects mRNA levels of the master regulator of virulence PrfA and PrfA-regulated genes, and these results could help to explain the reduced bacterial internalization in human cells of the ΔpnpA mutant. Overall, this work demonstrates that PNPase is an important post-transcriptional regulator for virulence and adaptation to the biofilm lifestyle of Gram-positive bacteria and highlights the expanding role of ribonucleases as critical players in pathogenicity.

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“…Colony morphology has long been a powerful indicator of microbial physiology. Distinct colony morphologies between bacterial strains can be linked to differences in surface molecules, virulence, and biofilm formation ( Kansal et al, 1998 ; Martin-Rodriguez et al, 2021 ). Although PS150 and GR1009 are genetically similar to each other, GR1009 exhibits an impaired hypnotic effect.…”

Section: Introductionmentioning

confidence: 99%

Exopolysaccharide is the potential effector of Lactobacillus fermentum PS150, a hypnotic psychobiotic strain

Huang

Chu

Wu³

et al. 2023

Front. Microbiol.

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Psychobiotics are a class of probiotics that confer beneficial effects on the mental health of the host. We have previously reported hypnotic effects of a psychobiotic strain, Lactobacillus fermentum PS150 (PS150), which significantly shortens sleep latency in experimental mice, and effectively ameliorate sleep disturbances caused by either caffeine consumption or a novel environment. In the present study, we discovered a L. fermentum strain, GR1009, isolated from the same source of PS150, and found that GR1009 is phenotypically distinct but genetically similar to PS150. Compared with PS150, GR1009 have no significant hypnotic effects in the pentobarbital-induced sleep test in mice. In addition, we found that heat-killed PS150 exhibited hypnotic effects and altered the gut microbiota in a manner similar to live bacteria, suggesting that a heat-stable effector, such as exopolysaccharide (EPS), could be responsible for these effects. Our comparative genomics analysis also revealed distinct genetic characteristics in EPS biosynthesis between GR1009 and PS150. Furthermore, scanning electron microscopy imaging showed a sheet-like EPS structure in PS150, while GR1009 displayed no apparent EPS structure. Using the phenol-sulfate assay, we found that the sugar content value of the crude extract containing EPS (C-EPS) from PS150 was approximately five times higher than that of GR1009, indicating that GR1009 has a lower EPS production activity than PS150. Through the pentobarbital-induced sleep test, we confirmed the hypnotic effects of the C-EPS isolated from PS150, as evidenced by a significant reduction in sleep latency and recovery time following oral administration in mice. In summary, we utilized a comparative approach to delineate differences between PS150 and GR1009 and proposed that EPS may serve as a key factor that mediates the observed hypnotic effect.

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Regulation of colony morphology and biofilm formation in Shewanella algae

Cited by 7 publications

References 56 publications

High-throughput microbial culturomics using automation and machine learning

High-throughput microbial culturomics using automation and machine learning

The ribonuclease PNPase is a key regulator of biofilm formation in Listeria monocytogenes and affects invasion of host cells

Exopolysaccharide is the potential effector of Lactobacillus fermentum PS150, a hypnotic psychobiotic strain

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