Molecular and cellular insight into Escherichia coli SslE and its role during biofilm maturation

Corsini, Paula M.; Wang, Sunjun; Rehman, Saima; Fenn, Katherine; Sagar, Amin; Sirovica, Slobodan; Cleaver, Leanne; Edwards-Gayle, Charlotte J. C.; Mastroianni, Giulia; Dorgan, Ben; Sewell, Lee; Lynham, Steven; Iuga, Dinu; Franks, W. Trent; Jarvis, James A.; Carpenter, Guy; Curtis, Michael A.; Bernadó, Pau; Darbari, Vidya C.; Garnett, James A.

doi:10.1038/s41522-022-00272-5

Cited by 11 publications

(5 citation statements)

References 74 publications

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“…E. histolytica is exposed to a complex bacterial flora in the gut, including biofilm-forming bacteria like E. coli 53 . Our findings that EhCPs can degrade B. subtilis biofilm, and the proteinous nature of both E. coli and B. subtilis biofilms, led us to test whether EhCPs can degrade E. coli biofilm.…”

Section: Resultsmentioning

confidence: 99%

Digestive exophagy of biofilms by intestinal amoeba and its impact on stress tolerance and cytotoxicity

Zanditenas,

Trebicz-Geffen,

Kolli

et al. 2023

npj Biofilms Microbiomes

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The human protozoan parasite Entamoeba histolytica is responsible for amebiasis, a disease endemic to developing countries. E. histolytica trophozoites colonize the large intestine, primarily feeding on bacteria. However, in the gastrointestinal tract, bacterial cells form aggregates or structured communities called biofilms too large for phagocytosis. Remarkably, trophozoites are still able to invade and degrade established biofilms, utilizing a mechanism that mimics digestive exophagy. Digestive exophagy refers to the secretion of digestive enzymes that promote the digestion of objects too large for direct phagocytosis by phagocytes. E. histolytica cysteine proteinases (CPs) play a crucial role in the degradation process of Bacillus subtilis biofilm. These proteinases target TasA, a major component of the B. subtilis biofilm matrix, also contributing to the adhesion of the parasite to the biofilm. In addition, they are also involved in the degradation of biofilms formed by Gram-negative and Gram-positive enteric pathogens. Furthermore, biofilms also play an important role in protecting trophozoites against oxidative stress. This specific mechanism suggests that the amoeba has adapted to prey on biofilms, potentially serving as an untapped reservoir for novel therapeutic approaches to treat biofilms. Consistently, products derived from the amoeba have been shown to restore antibiotic sensitivity to biofilm cells. In addition, our findings reveal that probiotic biofilms can act as a protective shield for mammalian cells, hindering the progression of the parasite towards them.

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Section: Resultsmentioning

confidence: 99%

Digestive exophagy of biofilms by intestinal amoeba and its impact on stress tolerance and cytotoxicity

Zanditenas,

Trebicz-Geffen,

Kolli

et al. 2023

npj Biofilms Microbiomes

View full text Add to dashboard Cite

show abstract

“…E. histolytica is exposed to a complex bacterial flora in the gut, including biofilm-forming bacteria like E. coli EPEC 44 . Our findings that EhCPs can degrade B. subtilis biofilm, and the proteinous nature of both E. coli and B. subtilis biofilms, led us to test whether EhCPs can degrade E. coli biofilm.…”

Section: Resultsmentioning

confidence: 99%

“…E. histolytica is exposed to a complex bacterial flora in the gut, including biofilm-forming bacteria like E. coli EPEC 44…”

Section: The Role Of the Bacterial Matrix Protein Tasa As A Substrate...mentioning

confidence: 99%

Digestive exophagy of Bacterial Biofilms by an Amoeba Predator is Mediated by Specific Biofilm Recognition

Zanditenas

Trebicz-Geffen

Domínguez-García

et al. 2022

Preprint

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The human protozoan parasite Entamoeba histolytica is responsible for amebiasis, a disease endemic to developing countries. E. histolytica trophozoites are released from the cysts to colonize the large intestine, where they primarily feed on bacterial cells. In these scenarios, bacterial cells form aggregates or structured communities too large for phagocytosis. Our results show that E. histolytica can degrade pre-established biofilms of Bacillus subtilis and Escherichia coli in a dose- and time-dependent manner. Surprisingly, trophozoites incubated with B. subtilis biofilm exhibit a unique transcriptome signature compared to those incubated with planktonic cells or without bacteria. Biofilm-induced genes include cysteine proteases (CPs), and the general inhibition of CPs by E64D or by the use of specific small-RNA (sRNA)-based RNA interference impairs the degradation of biofilms by E. histolytica. The degradation of B. subtilis extracellular matrix (ECM) protein TasA by CPs is associated with partial biofilm digestion and activation of the stress response in the interacting B. subtilis cells. The interaction with B. subtilis biofilms was also associated with lower levels of oxidoreductases. Oxidoreductase downregulation can be a readout of the embedding of E. histolytica trophozoites within the biofilm-produced extracellular matrix, reducing their exposure to oxidative stress (OS). Our results indicate that parasites may digest biofilms by a controlled mechanism of digestive exophagy as secretion of digestive enzymes as a conserved mechanism for biofilm degradation allows phagocytic digestion of biofilm cells. Furthermore, the partially digested biofilms can serve as an unexpected shield protecting parasites from oxidative environments and thereby may regulate the persistence and virulence of the parasite.

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“…An invasive biofilm, which harbors the opportunistic pathogen Bacteroides fragilis as a crucial species, has been shown to be detected in patients with IBD [ 165 ]. Biofilm formations have also been observed in common antibiotic-resistant foodborne bacteria such as E. coli , S. aureus, S. Typhimurium, and L. monocytogenes [ 166 , 167 ]. The SslE protein, secreted by E. coli , degrades intestinal mucins, including MUC2, MUC3, and MUC5AC and accelerates biofilm maturation, which is a significant factor in the infection process of highly virulent species [ 167 ].…”

Section: Nanoencapsulated Eos As a Promising Option For Animal Produc...mentioning

confidence: 99%

“…Biofilm formations have also been observed in common antibiotic-resistant foodborne bacteria such as E. coli , S. aureus, S. Typhimurium, and L. monocytogenes [ 166 , 167 ]. The SslE protein, secreted by E. coli , degrades intestinal mucins, including MUC2, MUC3, and MUC5AC and accelerates biofilm maturation, which is a significant factor in the infection process of highly virulent species [ 167 ]. Enterotoxigenic E. coli , a virulent strain, causes severe infections and diarrheal diseases in animals, including weaned pigs, and is closely related to increased mortality and severe impairments in production [ 20 ].…”

Section: Nanoencapsulated Eos As a Promising Option For Animal Produc...mentioning

confidence: 99%

Potential of Aromatic Plant-Derived Essential Oils for the Control of Foodborne Bacteria and Antibiotic Resistance in Animal Production: A Review

Zhang

Gao

et al. 2022

Antibiotics

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Antibiotic resistance has become a severe public threat to human health worldwide. Supplementing antibiotic growth promoters (AGPs) at subtherapeutic levels has been a commonly applied method to improve the production performance of livestock and poultry, but the misuse of antibiotics in animal production plays a major role in the antibiotic resistance crisis and foodborne disease outbreaks. The addition of AGPs to improve production performance in livestock and poultry has been prohibited in some countries, including Europe, the United States and China. Moreover, cross-resistance could result in the development of multidrug resistant bacteria and limit therapeutic options for human and animal health. Therefore, finding alternatives to antibiotics to maintain the efficiency of livestock production and reduce the risk of foodborne disease outbreaks is beneficial to human health and the sustainable development of animal husbandry. Essential oils (EOs) and their individual compounds derived from aromatic plants are becoming increasingly popular as potential antibiotic alternatives for animal production based on their antibacterial properties. This paper reviews recent studies in the application of EOs in animal production for the control of foodborne pathogens, summarizes their molecular modes of action to increase the susceptibility of antibiotic-resistant bacteria, and provides a promising role for the application of nanoencapsulated EOs in animal production to control bacteria and overcome antibiotic resistance.

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Molecular and cellular insight into Escherichia coli SslE and its role during biofilm maturation

Cited by 11 publications

References 74 publications

Digestive exophagy of biofilms by intestinal amoeba and its impact on stress tolerance and cytotoxicity

Digestive exophagy of biofilms by intestinal amoeba and its impact on stress tolerance and cytotoxicity

Digestive exophagy of Bacterial Biofilms by an Amoeba Predator is Mediated by Specific Biofilm Recognition

Potential of Aromatic Plant-Derived Essential Oils for the Control of Foodborne Bacteria and Antibiotic Resistance in Animal Production: A Review

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