Role of cytoneme structures and extracellular vesicles in Trichomonas vaginalis parasite-parasite communication

  1. Nehuén Salas
  2. Manuela Blasco Pedreros
  3. Tuanne dos Santos Melo
  4. Vanina G Maguire
  5. Jihui Sha
  6. James A Wohlschlegel
  7. Antonio Pereira-Neves
  8. Natalia de Miguel

  • Curated by eLife

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    eLife assessment

    We believe this study has the potential to be fundamental for the field of microbial communication and compelling evidence with the chance of changing the current state-of-the-art in this area has been presented. This is will be of natural interest to the field of parasitology, but scientists in the general area of cell-to-cell communication will certainly benefit from this contribution too. A major strength of this manuscript is the clear demonstration of the role of cytoneme-like structures and extracellular vesicles in parasite communication using the Trichomonas vaginalis model. Given the potential of these findings, the authors could deepen their discussion and perspectives for other areas.

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Abstract

Trichomonas vaginalis, the etiologic agent of the most common non-viral sexually transmitted infection worldwide. With an estimated annual prevalence of 276 million new cases, mixed infections with different parasite strains are expected. Although it is known that parasites interact with their host to enhance their own survival and transmission, evidence of mixed infections call into question the extent to which unicellular parasites communicate with each other. Here, we demonstrated that different T. vaginalis strains can communicate through the formation of cytoneme-like membranous cell connections. We showed that cytonemes formation of an adherent parasite strain (CDC1132) is affected in the presence of a different strain (G3 or B7RC2). Our findings provide evidence that this effect is contact-independent and that extracellular vesicles (EVs) are responsible, at least in part, of the communication among strains. We found that EVs isolated from G3, B7RC2, and CDC1132 strains contain a highly distinct repertoire of proteins, some of them involved in signaling and communication, among other functions. Finally, we showed that parasite adherence to host cells is affected by communication between strains as binding of adherent T. vaginalis CDC1132 strain to prostate cells is significantly higher in the presence of G3 or B7RC2 strains. We also observed that a poorly adherent parasite strain (G3) adheres more strongly to prostate cells in the presence of an adherent strain. The study of signaling, sensing, and cell communication in parasitic organisms will enhance our understanding of the basic biological characteristics of parasites, which may have important consequences in pathogenesis.

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  1. Version published to 10.7554/elife.86067 on eLife
  2. eLife

    eLife assessment

    We believe this study has the potential to be fundamental for the field of microbial communication and compelling evidence with the chance of changing the current state-of-the-art in this area has been presented. This is will be of natural interest to the field of parasitology, but scientists in the general area of cell-to-cell communication will certainly benefit from this contribution too. A major strength of this manuscript is the clear demonstration of the role of cytoneme-like structures and extracellular vesicles in parasite communication using the Trichomonas vaginalis model. Given the potential of these findings, the authors could deepen their discussion and perspectives for other areas.

  3. eLife

    Reviewer #1 (Public Review):

    The manuscript Role of cytoneme-like structures and extracellular vesicles in Trichomonas vaginalis parasite: parasite communication by Salas N et al is an interesting manuscript with novel findings, clear strategies, and fine design of experiments. Despite the quality of the manuscript, it must be improved in order to deliver the best message in the area of cellular biology and molecular parasitology.

  4. eLife

    Reviewer #2 (Public Review):

    The manuscript is rigorous and clearly written; the experiments are well described, and the conclusions are consistent with the experimental results. Particularly interesting are the data demonstrating the role of cytoneme-like structures. The microscopy images supporting the experimental data are clear and fascinating.
    The work is, in my opinion, well conducted.

  5. eLife

    Reviewer #3 (Public Review):

    In this manuscript, the authors (Salas et al.) have investigated the communication strategies among various strains or species of Trichomonas vaginalis. T. vaginalis is a parasite that is responsible for non-viral sexually transmitted infections, worldwide. The authors have demonstrated that highly adherent parasite uses cytoneme-like membrane structures and extracellular vesicles (EVs) to communicate with poorly adherent isolates and mount a stronger response to hosts.

    The major strength of this work is the use of state-of-the microscopic techniques to analyze cytonemes and EVs. However, the weakness is the experiments shown in the manuscript are more descriptive than mechanistic. The significance of this work is high because it demonstrates the presence of a unique communication strategy in Trichomonas vaginalis. Trichomonas uses cytoneme-like elongated membrane structures and extracellular vesicles to interact with each other and induce a robust pathogenic response in host cells.

    The authors have used state-of-the-art cell biology techniques to conduct the study and the data analysis is solid.

    Overall, the experiments are solid and the authors were able to accomplish their objectives of demonstrating parasite communication in T. vaginalis.

  6. Version published to 10.1101/2023.01.18.524507v1 on bioRxiv