Tracing the origins of extracellular DNA in bacterial biofilms: story of death and predation to community benefit

Campoccia, Davide; Montanaro, Lucio; Arciola, Carla Renata

doi:10.1080/08927014.2021.2002987

Cited by 27 publications

(25 citation statements)

References 120 publications

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“…While eDNA has been shown in the past to be a major component of the biofilm matrix that plays a role in overall biofilm architecture for different species (Okshevsky & Meyer, 2015, Campoccia et al ., 2021), we previously reported a novel role for this molecule, as an environmental cue to sense deleterious environments in a biofilm and promote cell dispersion in C. crescentus (Berne et al ., 2010). We showed that cell death and eDNA release increase during biofilm formation and that eDNA prevents newborn swarmer cell from attaching to surfaces and settling into a biofilm by binding specifically to and inhibiting the adhesiveness of the holdfast.…”

Section: Discussionmentioning

confidence: 99%

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eDNA-stimulated cell dispersion fromCaulobacter crescentusbiofilms upon oxygen limitation is dependent on a toxin-antitoxin system

Berne

Zappa

Brun

2022

Preprint

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In their natural environment, most bacteria preferentially live as complex surface-attached multicellular colonies called biofilms. Biofilms begin with a few cells adhering to a surface, where they multiply to form a mature colony. When conditions deteriorate, cells can leave the biofilm. This dispersion is thought to be an important process that modifies the overall biofilm architecture and that promotes colonization of new environments. In Caulobacter crescentus biofilms, extracellular DNA (eDNA) is released upon cell death and prevents newborn cells from joining the established biofilm. Thus, eDNA promotes the dispersal of newborn cells and the subsequent colonization of new environments. These observations suggest that eDNA is a cue for sensing detrimental environmental conditions in the biofilm. Here we show that the toxin-antitoxin ParDE4 stimulates cell death in areas of a biofilm with decreased O2 availability. In conditions where O2 availability is low, eDNA concentration is correlated with cell death. Cell dispersal away from biofilms is decreased when parDE4 is deleted, probably due to the lower local eDNA concentration. Expression of parDE4 is positively regulated by O2 and the expression of this operon is decreased in biofilms where O2 availability is low. Thus, PCD by an O2-regulated toxin-antitoxin system stimulates dispersal away from areas of a biofilm with decreased O2 availability and favors colonization of a new, more hospitable environment.

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Section: Discussionmentioning

confidence: 99%

“…In some bacterial species, extracellular DNA (eDNA) plays a stabilizing role in the biofilm matrix (Okshevsky & Meyer, 2015, Campoccia et al ., 2021). In contrast, we previously showed that C. crescentus eDNA produced via cell lysis negatively regulates biofilm formation and stimulates cell dispersal.…”

Section: Introductionmentioning

confidence: 99%

eDNA-stimulated cell dispersion fromCaulobacter crescentusbiofilms upon oxygen limitation is dependent on a toxin-antitoxin system

Berne

Zappa

Brun

2022

Preprint

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“…The EPS functions as a barrier and boundary between the microbial community and the external environment, and it plays a central role in bacterial attachment. Additionally, eDNA released from the lysis of a subpopulation of bacterial cells is involved in the attachment, aggregation, and stabilization of the biofilms [490]. eDNA may even facilitate adhesion to highly hydrophobic surfaces [491].…”

Section: Biofilmsmentioning

confidence: 99%

“…eDNA may even facilitate adhesion to highly hydrophobic surfaces [491]. Some autolysins are important for the release of eDNA and the consequent biofilm formation [490,[492][493][494][495]. The biofilms have a high water content that allows the flow of nutrients required for bacterial survival within the biofilms [4].…”

Section: Biofilmsmentioning

confidence: 99%

Targeting the Holy Triangle of Quorum Sensing, Biofilm Formation, and Antibiotic Resistance in Pathogenic Bacteria

Sionov

Steinberg

2022

Microorganisms

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Chronic and recurrent bacterial infections are frequently associated with the formation of biofilms on biotic or abiotic materials that are composed of mono- or multi-species cultures of bacteria/fungi embedded in an extracellular matrix produced by the microorganisms. Biofilm formation is, among others, regulated by quorum sensing (QS) which is an interbacterial communication system usually composed of two-component systems (TCSs) of secreted autoinducer compounds that activate signal transduction pathways through interaction with their respective receptors. Embedded in the biofilms, the bacteria are protected from environmental stress stimuli, and they often show reduced responses to antibiotics, making it difficult to eradicate the bacterial infection. Besides reduced penetration of antibiotics through the intricate structure of the biofilms, the sessile biofilm-embedded bacteria show reduced metabolic activity making them intrinsically less sensitive to antibiotics. Moreover, they frequently express elevated levels of efflux pumps that extrude antibiotics, thereby reducing their intracellular levels. Some efflux pumps are involved in the secretion of QS compounds and biofilm-related materials, besides being important for removing toxic substances from the bacteria. Some efflux pump inhibitors (EPIs) have been shown to both prevent biofilm formation and sensitize the bacteria to antibiotics, suggesting a relationship between these processes. Additionally, QS inhibitors or quenchers may affect antibiotic susceptibility. Thus, targeting elements that regulate QS and biofilm formation might be a promising approach to combat antibiotic-resistant biofilm-related bacterial infections.

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“…Besides the proteinaceous components, extracellular DNA (eDNA) works in biofilm as an electrostatic net, thus stabilizing and strengthening the matrix [ 112 , 113 , 114 , 115 , 116 ]. Studies on the mechanism of eDNA production and release have revealed that bacteria produce eDNA either through altruistic suicide or fratricide killing and that bacterial autolysis is mediated by murein hydrolase [ 117 ].…”

Section: Staphylococcal Biofilm Development On the Surface Of Biomate...mentioning

confidence: 99%

Colonization and Infection of Indwelling Medical Devices by Staphylococcus aureus with an Emphasis on Orthopedic Implants

Pietrocola

Campoccia

Motta

et al. 2022

IJMS

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The use of indwelling medical devices has constantly increased in recent years and has revolutionized the quality of life of patients affected by different diseases. However, despite the improvement of hygiene conditions in hospitals, implant-associated infections remain a common and serious complication in prosthetic surgery, mainly in the orthopedic field, where infection often leads to implant failure. Staphylococcus aureus is the most common cause of biomaterial-centered infection. Upon binding to the medical devices, these bacteria proliferate and develop dense communities encased in a protective matrix called biofilm. Biofilm formation has been proposed as occurring in several stages—(1) attachment; (2) proliferation; (3) dispersal—and involves a variety of host and staphylococcal proteinaceous and non-proteinaceous factors. Moreover, biofilm formation is strictly regulated by several control systems. Biofilms enable staphylococci to avoid antimicrobial activity and host immune response and are a source of persistent bacteremia as well as of localized tissue destruction. While considerable information is available on staphylococcal biofilm formation on medical implants and important results have been achieved on the treatment of biofilms, preclinical and clinical applications need to be further investigated. Thus, the purpose of this review is to gather current studies about the mechanism of infection of indwelling medical devices by S. aureus with a special focus on the biochemical factors involved in biofilm formation and regulation. We also provide a summary of the current therapeutic strategies to combat biomaterial-associated infections and highlight the need to further explore biofilm physiology and conduct research for innovative anti-biofilm approaches.

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Tracing the origins of extracellular DNA in bacterial biofilms: story of death and predation to community benefit

Cited by 27 publications

References 120 publications

eDNA-stimulated cell dispersion fromCaulobacter crescentusbiofilms upon oxygen limitation is dependent on a toxin-antitoxin system

eDNA-stimulated cell dispersion fromCaulobacter crescentusbiofilms upon oxygen limitation is dependent on a toxin-antitoxin system

Targeting the Holy Triangle of Quorum Sensing, Biofilm Formation, and Antibiotic Resistance in Pathogenic Bacteria

Colonization and Infection of Indwelling Medical Devices by Staphylococcus aureus with an Emphasis on Orthopedic Implants

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