Long‐lasting effects of chronic exposure to chemical pollution on the hologenome of the Manila clam

Abstract Chronic exposure to pollutants affects natural populations, creating specific molecular and biochemical signatures. In the present study, we tested the hypothesis that chronic exposure to pollutants might have substantial effects on the Manila clam hologenome long after removal from contami...

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Main Authors: Mariangela Iannello, Marica Mezzelani, Giulia Dalla Rovere, Morgan Smits, Tomaso Patarnello, Claudio Ciofi, Lisa Carraro, Luciano Boffo, Serena Ferraresso, Massimiliano Babbucci, Sandro Mazzariol, Cinzia Centelleghe, Barbara Cardazzo, Claudio Carrer, Maurizio Varagnolo, Alessandro Nardi, Lucia Pittura, Maura Benedetti, Daniele Fattorini, Francesco Regoli, Fabrizio Ghiselli, Stefania Gorbi, Luca Bargelloni, Massimo Milan
Format: Article
Language:English
Published: Wiley 2021-12-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.13319
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author Mariangela Iannello
Marica Mezzelani
Giulia Dalla Rovere
Morgan Smits
Tomaso Patarnello
Claudio Ciofi
Lisa Carraro
Luciano Boffo
Serena Ferraresso
Massimiliano Babbucci
Sandro Mazzariol
Cinzia Centelleghe
Barbara Cardazzo
Claudio Carrer
Maurizio Varagnolo
Alessandro Nardi
Lucia Pittura
Maura Benedetti
Daniele Fattorini
Francesco Regoli
Fabrizio Ghiselli
Stefania Gorbi
Luca Bargelloni
Massimo Milan
author_facet Mariangela Iannello
Marica Mezzelani
Giulia Dalla Rovere
Morgan Smits
Tomaso Patarnello
Claudio Ciofi
Lisa Carraro
Luciano Boffo
Serena Ferraresso
Massimiliano Babbucci
Sandro Mazzariol
Cinzia Centelleghe
Barbara Cardazzo
Claudio Carrer
Maurizio Varagnolo
Alessandro Nardi
Lucia Pittura
Maura Benedetti
Daniele Fattorini
Francesco Regoli
Fabrizio Ghiselli
Stefania Gorbi
Luca Bargelloni
Massimo Milan
author_sort Mariangela Iannello
collection DOAJ
description Abstract Chronic exposure to pollutants affects natural populations, creating specific molecular and biochemical signatures. In the present study, we tested the hypothesis that chronic exposure to pollutants might have substantial effects on the Manila clam hologenome long after removal from contaminated sites. To reach this goal, a highly integrative approach was implemented, combining transcriptome, genetic and microbiota analyses with the evaluation of biochemical and histological profiles of the edible Manila clam Ruditapes philippinarum, as it was transplanted for 6 months from the polluted area of Porto Marghera (PM) to the clean area of Chioggia (Venice lagoon, Italy). One month post‐transplantation, PM clams showed several modifications to its resident microbiota, including an overrepresentation of the opportunistic pathogen Arcobacter spp. This may be related to the upregulation of several immune genes in the PM clams, potentially representing a host response to the increased abundance of deleterious bacteria. Six months after transplantation, PM clams demonstrated a lower ability to respond to environmental/physiological stressors related to the summer season, and the hepatopancreas‐associated microbiota still showed different compositions among PM and CH clams. This study confirms that different stressors have predictable effects in clams at different biological levels and demonstrates that chronic exposure to pollutants leads to long‐lasting effects on the animal hologenome. In addition, no genetic differentiation between samples from the two areas was detected, confirming that PM and CH clams belong to a single population. Overall, the obtained responses were largely reversible and potentially related to phenotypic plasticity rather than genetic adaptation. The results here presented will be functional for the assessment of the environmental risk imposed by chemicals on an economically important bivalve species.
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spelling doaj.art-9e8682b92e334619b22916f8ef564a542022-12-21T19:21:25ZengWileyEvolutionary Applications1752-45712021-12-0114122864288010.1111/eva.13319Long‐lasting effects of chronic exposure to chemical pollution on the hologenome of the Manila clamMariangela Iannello0Marica Mezzelani1Giulia Dalla Rovere2Morgan Smits3Tomaso Patarnello4Claudio Ciofi5Lisa Carraro6Luciano Boffo7Serena Ferraresso8Massimiliano Babbucci9Sandro Mazzariol10Cinzia Centelleghe11Barbara Cardazzo12Claudio Carrer13Maurizio Varagnolo14Alessandro Nardi15Lucia Pittura16Maura Benedetti17Daniele Fattorini18Francesco Regoli19Fabrizio Ghiselli20Stefania Gorbi21Luca Bargelloni22Massimo Milan23Department of Biological, Geological, and Environmental Sciences University of Bologna Bologna ItalyDepartment of Life and Environmental Sciences Polytechnic University of Marche Ancona ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyDepartment of Biology University of Florence Sesto Fiorentino ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyAssociazione “Vongola Verace di Chioggia” Chioggia ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro Italyc/o Magistrato alle Acque di Venezia Ufficio Tecnico Antinquinamento Laboratorio CSMO Padova ItalySocieta’ Agricola Kappa S. S. di Varagnolo Maurizio E. C. Chioggia ItalyDepartment of Life and Environmental Sciences Polytechnic University of Marche Ancona ItalyDepartment of Life and Environmental Sciences Polytechnic University of Marche Ancona ItalyDepartment of Life and Environmental Sciences Polytechnic University of Marche Ancona ItalyDepartment of Life and Environmental Sciences Polytechnic University of Marche Ancona ItalyDepartment of Life and Environmental Sciences Polytechnic University of Marche Ancona ItalyDepartment of Biological, Geological, and Environmental Sciences University of Bologna Bologna ItalyDepartment of Life and Environmental Sciences Polytechnic University of Marche Ancona ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyDepartment of Comparative Biomedicine and Food Science University of Padova Legnaro ItalyAbstract Chronic exposure to pollutants affects natural populations, creating specific molecular and biochemical signatures. In the present study, we tested the hypothesis that chronic exposure to pollutants might have substantial effects on the Manila clam hologenome long after removal from contaminated sites. To reach this goal, a highly integrative approach was implemented, combining transcriptome, genetic and microbiota analyses with the evaluation of biochemical and histological profiles of the edible Manila clam Ruditapes philippinarum, as it was transplanted for 6 months from the polluted area of Porto Marghera (PM) to the clean area of Chioggia (Venice lagoon, Italy). One month post‐transplantation, PM clams showed several modifications to its resident microbiota, including an overrepresentation of the opportunistic pathogen Arcobacter spp. This may be related to the upregulation of several immune genes in the PM clams, potentially representing a host response to the increased abundance of deleterious bacteria. Six months after transplantation, PM clams demonstrated a lower ability to respond to environmental/physiological stressors related to the summer season, and the hepatopancreas‐associated microbiota still showed different compositions among PM and CH clams. This study confirms that different stressors have predictable effects in clams at different biological levels and demonstrates that chronic exposure to pollutants leads to long‐lasting effects on the animal hologenome. In addition, no genetic differentiation between samples from the two areas was detected, confirming that PM and CH clams belong to a single population. Overall, the obtained responses were largely reversible and potentially related to phenotypic plasticity rather than genetic adaptation. The results here presented will be functional for the assessment of the environmental risk imposed by chemicals on an economically important bivalve species.https://doi.org/10.1111/eva.13319ecotoxicologyhologenomehost‐microbiota interactionsphenotypic plasticityRuditapes philippinarum
spellingShingle Mariangela Iannello
Marica Mezzelani
Giulia Dalla Rovere
Morgan Smits
Tomaso Patarnello
Claudio Ciofi
Lisa Carraro
Luciano Boffo
Serena Ferraresso
Massimiliano Babbucci
Sandro Mazzariol
Cinzia Centelleghe
Barbara Cardazzo
Claudio Carrer
Maurizio Varagnolo
Alessandro Nardi
Lucia Pittura
Maura Benedetti
Daniele Fattorini
Francesco Regoli
Fabrizio Ghiselli
Stefania Gorbi
Luca Bargelloni
Massimo Milan
Long‐lasting effects of chronic exposure to chemical pollution on the hologenome of the Manila clam
Evolutionary Applications
ecotoxicology
hologenome
host‐microbiota interactions
phenotypic plasticity
Ruditapes philippinarum
title Long‐lasting effects of chronic exposure to chemical pollution on the hologenome of the Manila clam
title_full Long‐lasting effects of chronic exposure to chemical pollution on the hologenome of the Manila clam
title_fullStr Long‐lasting effects of chronic exposure to chemical pollution on the hologenome of the Manila clam
title_full_unstemmed Long‐lasting effects of chronic exposure to chemical pollution on the hologenome of the Manila clam
title_short Long‐lasting effects of chronic exposure to chemical pollution on the hologenome of the Manila clam
title_sort long lasting effects of chronic exposure to chemical pollution on the hologenome of the manila clam
topic ecotoxicology
hologenome
host‐microbiota interactions
phenotypic plasticity
Ruditapes philippinarum
url https://doi.org/10.1111/eva.13319
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