Cargando…

Contaminants from dredged sediments alter the transcriptome of Manila clam and induce shifts in microbiota composition

BACKGROUND: The reuse of dredged sediments in ports and lagoons is a big issue as it should not affect the quality and the equilibrium of ecosystems. In the lagoon of Venice, sediment management is of crucial importance as sediments are often utilized to built-up structures necessary to limit erosio...

Descripción completa

Detalles Bibliográficos
Autores principales: Bernardini, Ilaria, Quagliariello, Andrea, Peruzza, Luca, Martino, Maria Elena, Dalla Rovere, Giulia, Iori, Silvia, Asnicar, Davide, Ciscato, Maria, Fabrello, Jacopo, Corami, Fabiana, Cecchetto, Martina, Giubilato, Elisa, Carrer, Claudio, Bettiol, Cinzia, Semenzin, Elena, Marcomini, Antonio, Matozzo, Valerio, Bargelloni, Luca, Milan, Massimo, Patarnello, Tomaso
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10601118/
https://www.ncbi.nlm.nih.gov/pubmed/37880625
http://dx.doi.org/10.1186/s12915-023-01741-9
_version_ 1785126128873111552
author Bernardini, Ilaria
Quagliariello, Andrea
Peruzza, Luca
Martino, Maria Elena
Dalla Rovere, Giulia
Iori, Silvia
Asnicar, Davide
Ciscato, Maria
Fabrello, Jacopo
Corami, Fabiana
Cecchetto, Martina
Giubilato, Elisa
Carrer, Claudio
Bettiol, Cinzia
Semenzin, Elena
Marcomini, Antonio
Matozzo, Valerio
Bargelloni, Luca
Milan, Massimo
Patarnello, Tomaso
author_facet Bernardini, Ilaria
Quagliariello, Andrea
Peruzza, Luca
Martino, Maria Elena
Dalla Rovere, Giulia
Iori, Silvia
Asnicar, Davide
Ciscato, Maria
Fabrello, Jacopo
Corami, Fabiana
Cecchetto, Martina
Giubilato, Elisa
Carrer, Claudio
Bettiol, Cinzia
Semenzin, Elena
Marcomini, Antonio
Matozzo, Valerio
Bargelloni, Luca
Milan, Massimo
Patarnello, Tomaso
author_sort Bernardini, Ilaria
collection PubMed
description BACKGROUND: The reuse of dredged sediments in ports and lagoons is a big issue as it should not affect the quality and the equilibrium of ecosystems. In the lagoon of Venice, sediment management is of crucial importance as sediments are often utilized to built-up structures necessary to limit erosion. However, the impact of sediment reuse on organisms inhabiting this delicate area is poorly known. The Manila clam is a filter-feeding species of high economic and ecological value for the Venice lagoon experiencing a drastic decline in the last decades. In order to define the molecular mechanisms behind sediment toxicity, we exposed clams to sediments sampled from different sites within one of the Venice lagoon navigable canals close to the industrial area. Moreover, we investigated the impacts of dredged sediments on clam’s microbial communities. RESULTS: Concentrations of the trace elements and organic chemicals showed increasing concentrations from the city of Venice to sites close to the industrial area of Porto Marghera, where PCDD/Fs and PCBs concentrations were up to 120 times higher than the southern lagoon. While bioaccumulation of organic contaminants of industrial origin reflected sediments’ chemical concentrations, metal bioaccumulation was not consistent with metal concentrations measured in sediments probably due to the activation of ABC transporters. At the transcriptional level, we found a persistent activation of the mTORC1 signalling pathway, which is central in the coordination of cellular responses to chemical stress. Microbiota characterization showed the over-representation of potential opportunistic pathogens following exposure to the most contaminated sediments, leading to host immune response activation. Despite the limited acquisition of new microbial species from sediments, the latter play an important role in shaping Manila clam microbial communities. CONCLUSIONS: Sediment management in the Venice lagoon will increase in the next years to maintain and create new canals as well as to allow the operation of the new mobile gates at the three Venice lagoon inlets. Our data reveal important transcriptional and microbial changes of Manila clams after exposure to sediments, therefore reuse of dredged sediments represents a potential risk for the conservation of this species and possibly for other organisms inhabiting the Venice lagoon. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01741-9.
format Online
Article
Text
id pubmed-10601118
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-106011182023-10-27 Contaminants from dredged sediments alter the transcriptome of Manila clam and induce shifts in microbiota composition Bernardini, Ilaria Quagliariello, Andrea Peruzza, Luca Martino, Maria Elena Dalla Rovere, Giulia Iori, Silvia Asnicar, Davide Ciscato, Maria Fabrello, Jacopo Corami, Fabiana Cecchetto, Martina Giubilato, Elisa Carrer, Claudio Bettiol, Cinzia Semenzin, Elena Marcomini, Antonio Matozzo, Valerio Bargelloni, Luca Milan, Massimo Patarnello, Tomaso BMC Biol Research Article BACKGROUND: The reuse of dredged sediments in ports and lagoons is a big issue as it should not affect the quality and the equilibrium of ecosystems. In the lagoon of Venice, sediment management is of crucial importance as sediments are often utilized to built-up structures necessary to limit erosion. However, the impact of sediment reuse on organisms inhabiting this delicate area is poorly known. The Manila clam is a filter-feeding species of high economic and ecological value for the Venice lagoon experiencing a drastic decline in the last decades. In order to define the molecular mechanisms behind sediment toxicity, we exposed clams to sediments sampled from different sites within one of the Venice lagoon navigable canals close to the industrial area. Moreover, we investigated the impacts of dredged sediments on clam’s microbial communities. RESULTS: Concentrations of the trace elements and organic chemicals showed increasing concentrations from the city of Venice to sites close to the industrial area of Porto Marghera, where PCDD/Fs and PCBs concentrations were up to 120 times higher than the southern lagoon. While bioaccumulation of organic contaminants of industrial origin reflected sediments’ chemical concentrations, metal bioaccumulation was not consistent with metal concentrations measured in sediments probably due to the activation of ABC transporters. At the transcriptional level, we found a persistent activation of the mTORC1 signalling pathway, which is central in the coordination of cellular responses to chemical stress. Microbiota characterization showed the over-representation of potential opportunistic pathogens following exposure to the most contaminated sediments, leading to host immune response activation. Despite the limited acquisition of new microbial species from sediments, the latter play an important role in shaping Manila clam microbial communities. CONCLUSIONS: Sediment management in the Venice lagoon will increase in the next years to maintain and create new canals as well as to allow the operation of the new mobile gates at the three Venice lagoon inlets. Our data reveal important transcriptional and microbial changes of Manila clams after exposure to sediments, therefore reuse of dredged sediments represents a potential risk for the conservation of this species and possibly for other organisms inhabiting the Venice lagoon. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01741-9. BioMed Central 2023-10-25 /pmc/articles/PMC10601118/ /pubmed/37880625 http://dx.doi.org/10.1186/s12915-023-01741-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Bernardini, Ilaria
Quagliariello, Andrea
Peruzza, Luca
Martino, Maria Elena
Dalla Rovere, Giulia
Iori, Silvia
Asnicar, Davide
Ciscato, Maria
Fabrello, Jacopo
Corami, Fabiana
Cecchetto, Martina
Giubilato, Elisa
Carrer, Claudio
Bettiol, Cinzia
Semenzin, Elena
Marcomini, Antonio
Matozzo, Valerio
Bargelloni, Luca
Milan, Massimo
Patarnello, Tomaso
Contaminants from dredged sediments alter the transcriptome of Manila clam and induce shifts in microbiota composition
title Contaminants from dredged sediments alter the transcriptome of Manila clam and induce shifts in microbiota composition
title_full Contaminants from dredged sediments alter the transcriptome of Manila clam and induce shifts in microbiota composition
title_fullStr Contaminants from dredged sediments alter the transcriptome of Manila clam and induce shifts in microbiota composition
title_full_unstemmed Contaminants from dredged sediments alter the transcriptome of Manila clam and induce shifts in microbiota composition
title_short Contaminants from dredged sediments alter the transcriptome of Manila clam and induce shifts in microbiota composition
title_sort contaminants from dredged sediments alter the transcriptome of manila clam and induce shifts in microbiota composition
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10601118/
https://www.ncbi.nlm.nih.gov/pubmed/37880625
http://dx.doi.org/10.1186/s12915-023-01741-9
work_keys_str_mv AT bernardiniilaria contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT quagliarielloandrea contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT peruzzaluca contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT martinomariaelena contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT dallaroveregiulia contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT iorisilvia contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT asnicardavide contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT ciscatomaria contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT fabrellojacopo contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT coramifabiana contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT cecchettomartina contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT giubilatoelisa contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT carrerclaudio contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT bettiolcinzia contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT semenzinelena contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT marcominiantonio contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT matozzovalerio contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT bargelloniluca contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT milanmassimo contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition
AT patarnellotomaso contaminantsfromdredgedsedimentsalterthetranscriptomeofmanilaclamandinduceshiftsinmicrobiotacomposition