Biofilm-derived spores of Clostridioides (Clostridium) difficile exhibit increased thermotolerance compared to planktonic spores

Pickering, D.S.; Wilcox, Mark H.; Chilton, Caroline H.

doi:10.1016/j.anaerobe.2018.10.003

Cited by 7 publications

(5 citation statements)

References 17 publications

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“…estimates could suggest than in average one table spoon full of meal in every 13 (260 grams of meal) could be contaminated with CD, if not cooked properly. Basic recommendations emphasizing food safety practices updated to CD (using >85 • C for 10 min, or even better, boiling temperatures) (28,53,56,119,120), could prevent inadvertent exposure especially if patients are affected with debilitating conditions that increase the risk for CD intestinal colonization and infection. Future publications should include in their design and reporting descriptors for climate, ambient temperature, season and latitude.…”

Section: Discussionmentioning

confidence: 99%

Global and Historical Distribution of Clostridioides difficile in the Human Diet (1981–2019): Systematic Review and Meta-Analysis of 21886 Samples Reveal Sources of Heterogeneity, High-Risk Foods, and Unexpected Higher Prevalence Toward the Tropic

Rodriguez-Palacios

Shah

et al. 2020

Front. Med.

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Clostridioides difficile (CD) is a spore-forming bacterium that causes life-threatening intestinal infections in humans. Although formerly regarded as exclusively nosocomial, there is increasing genomic evidence that person-to-person transmission accounts for only <25% of cases, supporting the culture-based hypothesis that foods may be routine sources of CD-spore ingestion in humans. To synthesize the evidence on the risk of CD exposure via foods, we conducted a systematic review and meta-analysis of studies reporting the culture prevalence of CD in foods between January 1981 and November 2019. Meta-analyses, risk-ratio estimates, and meta-regression were used to estimate weighed-prevalence across studies and food types to identify laboratory and geographical sources of heterogeneity. In total, 21886 food samples were tested for CD between 1981 and 2019 (96.4%, n = 21084, 2007-2019; 232 food-sample-sets; 79 studies; 25 countries). Culture methodology, sample size and type, region, and latitude were sources of heterogeneity (p < 0.05). Although non-strictly-anaerobic methods were reported in some studies, and we confirmed experimentally that improper anaerobiosis of media/sample-handling affects CD recovery in agar (Fisher, p < 0.01), most studies (>72%) employed the same (one-of-six) culture strategy. Because the prevalence was also meta-analytically similar across six culture strategies reported, all studies were integrated using three meta-analytical methods. At the study level (n = 79), the four-decade global cumulative-prevalence of CD in the human diet was 4.1% (95%CI = −3.71, 11.91). At the food-set level (n = 232, mean 12.9 g/sample, similar across regions p > 0.2; 95%CI = 9.7-16.2), the weighted prevalence ranged between Rodriguez-Palacios et al. Clostridium difficile in Human Diet 4.5% (95%CI = 3-6%; all studies) and 8% (95%CI = 7-8%; only CD-positive-studies). Risk-ratio ranking and meta-regression showed that milk was the least likely source of CD, while seafood, leafy green vegetables, pork, and poultry carried higher risks (p < 0.05). Across regions, the risk of CD in foods for foodborne exposure reproducibly decreased with Earth latitude (p < 0.001). In conclusion, CD in the human diet is a global non-random-source of foodborne exposure that occurs independently of laboratory culture methods, across regions, and at a variable level depending on food type and latitude. The latitudinal trend (high CD-food-prevalence toward tropic) is unexpectedly inverse to the epidemiological observations of CD-infections in humans (frequent in temperate regions). Findings suggest the plausible hypothesis that ecologically-richer microbiomes in the tropic might protect against intestinal CD colonization/infections despite CD ingestion.

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Section: Discussionmentioning

confidence: 99%

Global and Historical Distribution of Clostridioides difficile in the Human Diet (1981–2019): Systematic Review and Meta-Analysis of 21886 Samples Reveal Sources of Heterogeneity, High-Risk Foods, and Unexpected Higher Prevalence Toward the Tropic

Rodriguez-Palacios

Shah

et al. 2020

Front. Med.

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“…Furthermore, Semenyuk and colleagues found that spores from biofilm cultures had a reduced germination efficiency compared to conventionally cultured spores [7]. Differences observed in the exosporium structure of spores from planktonic and biofilm cultures may contribute to increased thermotolerance and reduced germination efficiency in biofilm-derived spores [7,13,14]. Collectively, although we lack direct evidence from infection, these findings suggest that C. difficile biofilms can serve as a niche for generating modified spores, which favour maintenance of a dormant population, aiding bacterial persistence and disease recurrence.…”

Section: Biofilms-a Niche For C Difficile Spore Formation?mentioning

confidence: 99%

Clostridioides difficile biofilms: A mechanism of persistence in the gut?

2021

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Biofilms are structured bacterial communities encased in an extracellular matrix. The structure and complexity of biofilms depend on the microorganism and the local environment [1,2]. Biofilms form on tissues and foreign implants during human infections and confer pathogens resistance to drugs and immune responses, making biofilm-associated infections extremely difficult to treat [1]. Clostridioides difficile, a major healthcare-associated gastrointestinal pathogen, causes C. difficile infection (CDI), which is associated with high rates of recurrence, especially in the elderly [3]. CDI is strongly associated with long-term antibiotic therapy, which results in disruption of the native gut microbiota. In recent years, C. difficile biofilms have been considered to be important for persistence of the bacterium in the gut and for recurrent infections. Here we review the current knowledge on C. difficile biofilms in the context of the gut environment and infection. C. difficile forms biofilms in vitro Biofilm formation by C. difficile was first reported by Donelli and colleagues where they identified the role of polymicrobial biofilms in clogging of biliary stents using confocal and field emission scanning electron microscopy [4]. Soon after, biofilm formation by C. difficile strains of clinical origin (strains 630, R20291) on abiotic surfaces was reported, as quantitated by crystal violet staining [5,6]. Viable cell counts, as well as LIVE/DEAD viability staining showed that bacterial viability was higher in 1-to 3-day-old biofilms and decreased in 6-day-old biofilms [4-7]. C. difficile biofilms are multilayered, encased in a thick matrix composed of bacterial proteins, extracellular DNA (eDNA), and polysaccharide II; however, it is noteworthy that the composition and structure of biofilms are both time-and strain-dependent [5,7]. Numerous C. difficile factors which modulate biofilm formation have been identified, including pili, flagella proteins, the S-layer, Cwp84, quorum sensing, germination receptor SleC, and sporulation. Mutants deficient in stress-related proteins including the SOS response regulator, LexA, the RNA chaperone, Hfq, and the heat stress-associated chaperone, DnaK, have been associated with increased biofilm formation [8-10]. Interestingly, the toxins TcdA and TcdB were identified in the biofilm matrix of 3-and 6-day-old biofilms, suggesting that biofilms may play a role in C. difficile virulence [7]. Cyclic di-GMP (c-di-GMP) is thought to play an important role in the motile to sessile biofilm state shift through repression of flagellar synthesis and induction of pili [11]. In a recent global gene expression analysis of microfermentor biofilms, several genes controlled by the SinR-like regulators CD2214 and CD2215, including pilA1, were differentially expressed in biofilms, although pilA1 appeared to contribute to biofilm/ aggregate formation only in c-di-GMP overexpressing strains [12]. Thus, C. difficile forms complex biofilms in vitro which involves multiple regulatory pathways and several vir...

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“…The ability to interact with intestinal mucus constitutes an important colonization factor for several enteric pathogens. − In vitro , C. difficile has been shown to adhere to intestinal mucins, − and in vivo C. difficile has been observed within the mucus of mice − and humans. , C. difficile and other mucosa-associated microbes grow as microcolonies or intestinal biofilms in the mucus layer, indicating that mucus is likely the colonization site for C. difficile . ,− Intestinal mucus is primarily composed of a MUC2 core protein that is secreted from goblet cells. , MUC2 is highly O-glycosylated, which accounts for up to 80% of the mucin molecular weight. O -Glycans contain branched carbohydrates including N -acetyl-galactosamine (GalNAc), N -acetyl-glucosamine (GlcNAc), galactose, fucose, and sialic acid (NANA). − Additionally, MUC2 is N-glycosylated, consisting primarily of linked mannose residues .…”

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confidence: 99%

Mucin-Degrading Microbes Release Monosaccharides That Chemoattract Clostridioides difficile and Facilitate Colonization of the Human Intestinal Mucus Layer

Engevik

et al. 2020

ACS Infect. Dis.

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It is widely accepted that the pathogen Clostridioides difficile exploits an intestinal environment with an altered microbiota, but the details of these microbe–microbe interactions are unclear. Adherence and colonization of mucus has been demonstrated for several enteric pathogens and it is possible that mucin-associated microbes may be working in concert with C. difficile. We showed that C. difficile ribotype-027 adheres to MUC2 glycans and using fecal bioreactors, we identified that C. difficile associates with several mucin-degrading microbes. C. difficile was found to chemotax toward intestinal mucus and its glycan components, demonstrating that C. difficile senses the mucus layer. Although C. difficile lacks the glycosyl hydrolases required to degrade mucin glycans, coculturing C. difficile with the mucin-degrading Akkermansia muciniphila, Bacteroides thetaiotaomicron, and Ruminococcus torques allowed C. difficile to grow in media that lacked glucose but contained purified MUC2. Collectively, these studies expand our knowledge on how intestinal microbes support C. difficile.

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Biofilm-derived spores of Clostridioides (Clostridium) difficile exhibit increased thermotolerance compared to planktonic spores

Cited by 7 publications

References 17 publications

Global and Historical Distribution of Clostridioides difficile in the Human Diet (1981–2019): Systematic Review and Meta-Analysis of 21886 Samples Reveal Sources of Heterogeneity, High-Risk Foods, and Unexpected Higher Prevalence Toward the Tropic

Global and Historical Distribution of Clostridioides difficile in the Human Diet (1981–2019): Systematic Review and Meta-Analysis of 21886 Samples Reveal Sources of Heterogeneity, High-Risk Foods, and Unexpected Higher Prevalence Toward the Tropic

Clostridioides difficile biofilms: A mechanism of persistence in the gut?

Mucin-Degrading Microbes Release Monosaccharides That Chemoattract Clostridioides difficile and Facilitate Colonization of the Human Intestinal Mucus Layer

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