Superoxide-anion triggers impairments of immune efficiency and stress response behaviors of Eisenia fetida earthworms.

Abstract

Superoxide-hydrogen peroxide (S-HP), triggered by Val16Ala-SOD2 human polymorphism, may influence the risk of depression. Therefore, it is plausible that higher basal S-anion levels and chronic inflammatory states associated with the VV-SOD2 genotype can negatively modulate the stress response associated with resilience in various species, from primitive species to humans. To test this hypothesis, Eisenia fetida earthworms were exposed for 24 h to 30 nM rotenone, which causes mitochondrial dysfunction by generating high S-anion levels (known as the "VV-like phenotype"), and 10 μM porphyrin, a SOD2-like compound, which generates elevated HP levels (known as the "AA-like phenotype"). The results suggested that both S-anion and HP acted as signaling molecules, differentially altering the immune function and acute hydric stressful response. Although the AA-like phenotype improved the immune and stress response efficiencies, the VV-like phenotype showed a downregulated expression of the toll-like receptor (EaTLR, JX898685) and antimicrobial peptide (AMP) (AF060552) genes, which triggered the impairment of encapsulation and earthworms extracellular trap (EET) processes used by earthworms to trap and destroy microorganisms. When exposed to adverse environments and dangerous hydric stress, VV-like earthworms exhibited an impulsive behavior and failed to quickly identify and migrate to a protected environment, unlike control earthworms and AA-like earthworms. All results corroborated that the S-anion imbalance could concomitantly induce alterations in immune function and stress behavior related to earthworm survival. From a human perspective, this information may corroborate the potential specific role of superoxide anion in the modulation of the stress response, resilience, and risk of depression.

• Authors: Ivo Emilio da Cruz Jung, Charles Elias Assmann, Moisés Henrique Mastella, Fernanda Barbisan, Ricardo Augusto Spilliari Ruaro, Isabel Roggia, Bárbara Osmarin Turra, Bruna Chitolina, Audrei de Oliveira Alves, Cibele Ferreira Teixeira, Verônica Farina Azzolin, Euler Esteves Ribeiro, Marta Maria Medeiros Frescura Duarte, Ivana Beatrice Mânica da Cruz
• Journal: Chemosphere (Chemosphere) Vol. 269 Pg. 128712 (Apr 2021) ISSN: 1879-1298 [Electronic] England
• PMID: 33189402 (Publication Type: Journal Article)
• Copyright: Copyright © 2020. Published by Elsevier Ltd.

Chemical References

• Soil Pollutants
• Superoxides
• Hydrogen Peroxide
• Superoxide Dismutase

Topics

• Animals
• Humans
• Hydrogen Peroxide
• Oligochaeta (genetics, metabolism)
• Oxidative Stress
• Soil Pollutants (toxicity)
• Superoxide Dismutase (metabolism)
• Superoxides