Extracellular Vesicles: A Prevalent Tool for Microbial Gene Delivery?

Ben-Hur, Sharon; Biton, Mirit; Regev‐Rudzki, Neta

doi:10.1002/pmic.201800170

Cited by 7 publications

(5 citation statements)

References 55 publications

(72 reference statements)

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“…As neither species possesses a known Type IV or Type VI secretion system, transfer of DNA via these mechanisms is not possible. Chromosomal and plasmid DNA transfer via EVs is somewhat well documented in Gram − cells, minimally so in pathogenic Gram + cells ( 7 , 8 ), but not in Clostridium organisms. In the well-documented case ( 29 ) in the Gram + Streptococcus mutans, EVs are readily visible on the cell surface via SEM and are associated with profusely abundant eDNA nanowires visualized via SEM.…”

Section: Discussionmentioning

confidence: 99%

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DNA transfer between two different species mediated by heterologous cell fusion in Clostridium coculture

Charubin,

Hill,

Papoutsakis

2024

mBio

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Prokaryotic evolution is driven by random mutations and horizontal gene transfer (HGT). HGT occurs via transformation, transduction, or conjugation. We have previously shown that in syntrophic cocultures of Clostridium acetobutylicum and Clostridium ljungdahlii , heterologous cell fusion leads to a large-scale exchange of proteins and RNA between the two organisms. Here, we present evidence that heterologous cell fusion facilitates the exchange of DNA between the two organisms. Using selective subculturing, we isolated C. acetobutylicum cells which acquired and integrated into their genome portions of plasmid DNA from a plasmid-carrying C. ljungdahlii strain. Limiting-dilution plating and DNA methylation data based on PacBio Single-Molecule Real Time (SMRT) sequencing support the existence of hybrid C. acetobutylicum / C. ljungdahlii cells. These findings expand our understanding of multi-species microbiomes, their survival strategies, and evolution. IMPORTANCE Investigations of natural multispecies microbiomes and synthetic microbial cocultures are attracting renewed interest for their potential application in biotechnology, ecology, and medical fields. Previously, we have shown the syntrophic coculture of C. acetobutylicum and C. ljungdahlii undergoes heterologous cell-to-cell fusion, which facilitates the exchange of cytoplasmic protein and RNA between the two organisms. We now show that heterologous cell fusion between the two Clostridium organisms can facilitate the exchange of DNA. By applying selective pressures to this coculture system, we isolated clones of wild-type C. acetobutylicum which acquired the erythromycin resistance (erm) gene from the C. ljungdahlii strain carrying a plasmid with the erm gene. Single-molecule real-time sequencing revealed that the erm gene was integrated into the genome in a mosaic fashion. Our data also support the persistence of hybrid C. acetobutylicum / C. ljungdahlii cells displaying hybrid DNA-methylation patterns.

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Section: Discussionmentioning

confidence: 99%

“…The most-studied mechanisms of HGT between bacteria include transformation, transduction, and conjugation. Additional mechanisms of HGT have been identified including nanotube formation ( 6 ) and potential transfer via extracellular vesicles ( 7 , 8 ).…”

Section: Introductionmentioning

confidence: 99%

DNA transfer between two different species mediated by heterologous cell fusion in Clostridium coculture

Charubin,

Hill,

Papoutsakis

2024

mBio

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“…SsrA, RsaC, and RNAIII Not determined (Joshi et al, 2020) Streptococcus pyogenes rRNA tRNA Not evaluated (Resch et al, 2016) Streptococcus sanguinis msRNA Not evaluated (Choi et al, 2018) Treponema denticola msRNA Inhibits IL-5, IL-13, and IL-15 secretion in Jurkat T-cells (Choi et al, 2017b) Vibrio cholerae sRNA mRNA ncRNA Not evaluated (Sjöström et al, 2015) Vibrio fischeri sRNA SsrA Upregulates genes coding for immune and antimicrobial activity, and reduced host cell robustness was observed (Moriano-Gutierrez et al, 2020) which are Dnase resistant and can target host cells, which can be helpful when targeting a specific microbial population or subpopulation (Ben-Hur et al, 2019). The role of vesicular-DNA in cell-to-cell communication and environmental tolerance is yet to be fully understood.…”

Section: Listeria Monocytogenesmentioning

confidence: 99%

Bacterial extracellular vesicles and their novel therapeutic applications in health and cancer

Hosseini-Giv

Basas

Hicks

et al. 2022

Front. Cell. Infect. Microbiol.

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Bacterial cells communicate with host cells and other bacteria through the release of membrane vesicles known as bacterial extracellular vesicles (BEV). BEV are established mediators of intracellular signaling, stress tolerance, horizontal gene transfer, immune stimulation and pathogenicity. Both Gram-positive and Gram-negative bacteria produce extracellular vesicles through different mechanisms based on cell structure. BEV contain and transfer different types of cargo such as nucleic acids, proteins and lipids, which are used to interact with and affect host cells such as cytotoxicity and immunomodulation. The role of these membranous microvesicles in host communication, intra- and inter-species cell interaction and signaling, and contribution to various diseases have been well demonstrated. Due to their structure, these vesicles can be easily engineered to be utilized for clinical application, as shown with its role in vaccine therapy, and could be used as a diagnostic and cancer drug delivery tool in the future. However, like other novel therapeutic approaches, further investigation and standardization is imperative for BEV to become a routine vector or a conventional treatment method.

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“…For example, macrophages are induced to release inflammatory cytokines after taking up exosomes that were released from other macrophages infected with Mycobacterium avium (Bhatnagar and Schorey, 2007). EVs from a wide variety of other pathogens have important activity during infections, such as those produced by Giardia, Chlamydia, Trichomonas, and Cryptococcus (Benchimol, 2004;Rodrigues et al, 2008;Frohlich et al, 2012;Twu et al, 2013). Similarly, intracellular protozoan parasites also have an impact on the host, by altering its immune response.…”

Section: Ev Characteristics During Pathogen Infectionmentioning

confidence: 99%

“…For instance, great apes, and even humans, can host several species of Plasmodia parasites (Prugnolle et al, 2010). EVs could mediate communication by facilitating horizontal transfer of genetic information between different Plasmodia species (Regev-Rudzki et al, 2013;Kawamura et al, 2017;Otto et al, 2018;Ben-Hur et al, 2019;Plenderleith et al, 2019). Several lines of evidence support this possibility.…”

Section: The Possible Role Of Evs In Evolution By Horizontal Gene Tramentioning

confidence: 99%

Extracellular Vesicles Could Carry an Evolutionary Footprint in Interkingdom Communication

Corrêa

Caballero

León

et al. 2020

Front. Cell. Infect. Microbiol.

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Extracellular vesicles (EVs) are minute particles secreted by the cells of living organisms. Although the functional role of EVs is not yet clear, recent work has highlighted their role in intercellular communication. Here, we expand on this view by suggesting that EVs can also mediate communication among interacting organisms such as hosts, pathogens and vectors. This inter-kingdom communication via EVs is likely to have important evolutionary consequences ranging from adaptation of parasites to specialized niches in the host, to host resistance and evolution and maintenance of parasite virulence and transmissibility. A potential system to explore these consequences is the interaction among the human host, the mosquito vector and Plasmodium parasite involved in the malaria disease. Indeed, recent studies have found that EVs derived from Plasmodium infected red blood cells in humans are likely mediating the parasite's transition from the asexual to sexual stage, which might facilitate transmission to the mosquito vector. However, more work is needed to establish the adaptive consequences of this EV signaling among different taxa. We suggest that an integrative molecular approach, including a comparative phylogenetic analysis of the molecules (e.g., proteins and nucleic acids) derived from the EVs of interacting organisms (and their closely-related species) in the malaria system will prove useful for understanding interkingdom communication. Such analyses will also shed light on the evolution and persistence of host, parasite and vector interactions, with implications for the control of vector borne infectious diseases.

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Extracellular Vesicles: A Prevalent Tool for Microbial Gene Delivery?

Cited by 7 publications

References 55 publications

DNA transfer between two different species mediated by heterologous cell fusion in Clostridium coculture

DNA transfer between two different species mediated by heterologous cell fusion in Clostridium coculture

Bacterial extracellular vesicles and their novel therapeutic applications in health and cancer

Extracellular Vesicles Could Carry an Evolutionary Footprint in Interkingdom Communication

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