Molecular mechanisms of zinc toxicity in the potworm Enchytraeus crypticus, analysed by high-throughput gene expression profiling

Susana I.L. Gomes; Tjalf E. de Boer; Cornelis A.M. van Gestel; Nico M. van Straalen; Amadeu M.V.M. Soares; Dick Roelofs; Mónica J.B. Amorim

doi:10.1016/j.scitotenv.2022.153975

Molecular mechanisms of zinc toxicity in the potworm Enchytraeus crypticus, analysed by high-throughput gene expression profiling

Susana I.L. Gomes, Tjalf E. de Boer, Cornelis A.M. van Gestel, Nico M. van Straalen, Amadeu M.V.M. Soares, Dick Roelofs, Mónica J.B. Amorim^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

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Abstract

Zinc (Zn) is known to be relatively toxic to some soil-living invertebrates including the ecologically important enchytraeid worms. To reveal the molecular mechanisms of zinc toxicity we assessed the gene expression profile of Enchytraeus crypticus (Enchytraeidae), exposed to the reproduction effect concentrations EC₁₀ and EC₅₀, over 4 consecutive days, using a high-throughput microarray (species customized). Three main mechanisms of toxicity to Zn were observed: 1) Zn trafficking (upregulation of zinc transporters, a defence response to regulate the cellular zinc level), 2) oxidative stress (variety of defence mechanisms, triggered by Reactive Oxygen Species (ROS)), and 3) effects on the nervous system (possibly the primary lesion explaining the avoidance behaviour and also why enchytraeids are relatively susceptible to Zn). The adverse outcome at the organism level (reproduction EC₅₀) could be predicted based on gene expression (male gonad development, oocyte maturation), with Zn at the EC₅₀ affecting processes related to higher stress levels. The gene expression response was time-dependent and reflected the cascade of events taking place over-time. The 1 to 4 days of exposure design was a good strategy as it captured the time for sequence of events towards zinc adverse outcomes in E. crypticus.

Original language	English
Article number	153975
Pages (from-to)	1-7
Number of pages	7
Journal	Science of the Total Environment
Volume	825
Early online date	17 Feb 2022
DOIs	https://doi.org/10.1016/j.scitotenv.2022.153975
Publication status	Published - 15 Jun 2022

Bibliographical note

Funding Information:
This study was supported by the European Commission Project H2020-NMBP-2017 BIORIMA (GA No. 760928 ), NanoInformaTIX (H2020-NMBP-14-2018, No. 814426 ) and NANORIGO (H2020-NMBP-13-2018, GA No. 814530 ). Further support was due to FCT / MCTES through national funds (PIDDAC), and the co-funding by the FEDER , within the PT2020 Partnership Agreement and Compete 2020 via “BEAUTY: Big gEnome wide Applications for an ecotoxicology soil model – a knowledge base to Unravel mechanisms (nanopesTY_cides)” ( PTDC/CTA-AMB/3970/2020 ) and via CESAM ( UIDP/50017/2020+UIDB/50017/2020+LA/P/0094/2020 ). S.I.L. Gomes is funded by national funds (OE), through FCT , I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19.

Publisher Copyright:
© 2022 Elsevier B.V.

Funding

This study was supported by the European Commission Project H2020-NMBP-2017 BIORIMA (GA No. 760928 ), NanoInformaTIX (H2020-NMBP-14-2018, No. 814426 ) and NANORIGO (H2020-NMBP-13-2018, GA No. 814530 ). Further support was due to FCT / MCTES through national funds (PIDDAC), and the co-funding by the FEDER , within the PT2020 Partnership Agreement and Compete 2020 via “BEAUTY: Big gEnome wide Applications for an ecotoxicology soil model – a knowledge base to Unravel mechanisms (nanopesTY_cides)” ( PTDC/CTA-AMB/3970/2020 ) and via CESAM ( UIDP/50017/2020+UIDB/50017/2020+LA/P/0094/2020 ). S.I.L. Gomes is funded by national funds (OE), through FCT , I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19.

Funders	Funder number
Horizon 2020 Framework Programme
European Commission	760928, 814426, H2020-NMBP-13-2018, 814530, H2020-NMBP-14-2018
Fundação para a Ciência e a Tecnologia
Ministério da Ciência, Tecnologia e Ensino Superior
European Regional Development Fund	LA/P/0094/2020, PTDC/CTA-AMB/3970/2020

Keywords

AOP (adverse outcome pathway)
Microarrays
Soil
Time series

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Molecular mechanisms of zinc toxicity in the potworm Enchytraeus crypticus_analysed by high-throughput gene expression profilingFinal published version, 1.3 MBLicence: Article 25fa Dutch Copyright Act

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Gomes, S. I. L., de Boer, T. E., van Gestel, C. A. M., van Straalen, N. M., Soares, A. M. V. M., Roelofs, D., & Amorim, M. J. B. (2022). Molecular mechanisms of zinc toxicity in the potworm Enchytraeus crypticus, analysed by high-throughput gene expression profiling. Science of the Total Environment, 825, 1-7. Article 153975. https://doi.org/10.1016/j.scitotenv.2022.153975

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abstract = "Zinc (Zn) is known to be relatively toxic to some soil-living invertebrates including the ecologically important enchytraeid worms. To reveal the molecular mechanisms of zinc toxicity we assessed the gene expression profile of Enchytraeus crypticus (Enchytraeidae), exposed to the reproduction effect concentrations EC10 and EC50, over 4 consecutive days, using a high-throughput microarray (species customized). Three main mechanisms of toxicity to Zn were observed: 1) Zn trafficking (upregulation of zinc transporters, a defence response to regulate the cellular zinc level), 2) oxidative stress (variety of defence mechanisms, triggered by Reactive Oxygen Species (ROS)), and 3) effects on the nervous system (possibly the primary lesion explaining the avoidance behaviour and also why enchytraeids are relatively susceptible to Zn). The adverse outcome at the organism level (reproduction EC50) could be predicted based on gene expression (male gonad development, oocyte maturation), with Zn at the EC50 affecting processes related to higher stress levels. The gene expression response was time-dependent and reflected the cascade of events taking place over-time. The 1 to 4 days of exposure design was a good strategy as it captured the time for sequence of events towards zinc adverse outcomes in E. crypticus.",

keywords = "AOP (adverse outcome pathway), Microarrays, Soil, Time series",

author = "Gomes, {Susana I.L.} and {de Boer}, {Tjalf E.} and {van Gestel}, {Cornelis A.M.} and {van Straalen}, {Nico M.} and Soares, {Amadeu M.V.M.} and Dick Roelofs and Amorim, {M{\'o}nica J.B.}",

note = "Funding Information: This study was supported by the European Commission Project H2020-NMBP-2017 BIORIMA (GA No. 760928 ), NanoInformaTIX (H2020-NMBP-14-2018, No. 814426 ) and NANORIGO (H2020-NMBP-13-2018, GA No. 814530 ). Further support was due to FCT / MCTES through national funds (PIDDAC), and the co-funding by the FEDER , within the PT2020 Partnership Agreement and Compete 2020 via “BEAUTY: Big gEnome wide Applications for an ecotoxicology soil model – a knowledge base to Unravel mechanisms (nanopesTY_cides)” ( PTDC/CTA-AMB/3970/2020 ) and via CESAM ( UIDP/50017/2020+UIDB/50017/2020+LA/P/0094/2020 ). S.I.L. Gomes is funded by national funds (OE), through FCT , I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19. Publisher Copyright: {\textcopyright} 2022 Elsevier B.V.",

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T1 - Molecular mechanisms of zinc toxicity in the potworm Enchytraeus crypticus, analysed by high-throughput gene expression profiling

AU - Gomes, Susana I.L.

AU - de Boer, Tjalf E.

AU - van Gestel, Cornelis A.M.

AU - van Straalen, Nico M.

AU - Soares, Amadeu M.V.M.

AU - Roelofs, Dick

AU - Amorim, Mónica J.B.

N1 - Funding Information: This study was supported by the European Commission Project H2020-NMBP-2017 BIORIMA (GA No. 760928 ), NanoInformaTIX (H2020-NMBP-14-2018, No. 814426 ) and NANORIGO (H2020-NMBP-13-2018, GA No. 814530 ). Further support was due to FCT / MCTES through national funds (PIDDAC), and the co-funding by the FEDER , within the PT2020 Partnership Agreement and Compete 2020 via “BEAUTY: Big gEnome wide Applications for an ecotoxicology soil model – a knowledge base to Unravel mechanisms (nanopesTY_cides)” ( PTDC/CTA-AMB/3970/2020 ) and via CESAM ( UIDP/50017/2020+UIDB/50017/2020+LA/P/0094/2020 ). S.I.L. Gomes is funded by national funds (OE), through FCT , I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19. Publisher Copyright: © 2022 Elsevier B.V.

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N2 - Zinc (Zn) is known to be relatively toxic to some soil-living invertebrates including the ecologically important enchytraeid worms. To reveal the molecular mechanisms of zinc toxicity we assessed the gene expression profile of Enchytraeus crypticus (Enchytraeidae), exposed to the reproduction effect concentrations EC10 and EC50, over 4 consecutive days, using a high-throughput microarray (species customized). Three main mechanisms of toxicity to Zn were observed: 1) Zn trafficking (upregulation of zinc transporters, a defence response to regulate the cellular zinc level), 2) oxidative stress (variety of defence mechanisms, triggered by Reactive Oxygen Species (ROS)), and 3) effects on the nervous system (possibly the primary lesion explaining the avoidance behaviour and also why enchytraeids are relatively susceptible to Zn). The adverse outcome at the organism level (reproduction EC50) could be predicted based on gene expression (male gonad development, oocyte maturation), with Zn at the EC50 affecting processes related to higher stress levels. The gene expression response was time-dependent and reflected the cascade of events taking place over-time. The 1 to 4 days of exposure design was a good strategy as it captured the time for sequence of events towards zinc adverse outcomes in E. crypticus.

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Molecular mechanisms of zinc toxicity in the potworm Enchytraeus crypticus, analysed by high-throughput gene expression profiling

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