Submitted to: Aquatic Toxicology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/21/2012
Publication Date: N/A
Interpretive Summary: In nature, organisms are usually exposed to multiple stressors including biological, chemical and physical entities. Within environmental and health sciences, research typically focuses on the impact of single stressors, disregarding the cumulative risks arising from aggregate exposure to multiple stressors. Currently we have little understanding of how organisms deal with the demands placed on them by cumulative exposure, what strategies they follow to adapt to the impact of multiple stressors, and whether and how they prioritize stressors. The aim of the present study was to examine how young-of-the-year rainbow trout respond to an infectious agent (T. bryosalmone, the parasite causing PKD), to a prototype estrogen (17b-estradiol, E2) and to combinations of both stressors. The treatment effects were compared at the gene expression level by measuring liver gene expression using microarray technology. Liver was selected as target organ as the liver of fish is highly sensitive to various types of environmental stressors and plays an important role in both innate and adaptive immunity. The relation between the response to the two stressors and the fish’s ability to cope with the parasite was assessed by determining intensity of infection with T. bryosalmonae and cumulative mortality of trout. This study provides evidence that under combined exposure to PKD and E2 the hepatic transcriptome of rainbow trout either shows an intermediate or additive response where fish prioritized the PKD impact over the E2 impact. The hierarchy at the transcriptome level was reflected at the systemic level, where estrogen exposure did not modulate disease manifestation. The obvious ability of the organism to take a targeted instead of an additive strategy highlights the need to improve our understanding of organism’s responses to combined effects of chemical, physical and biological stressors.
Technical Abstract: BACKGROUND: Organisms often experience concurrent exposure to multiple environmental stressors. Currently there exists little understanding how organisms deal with the demands placed on them by such cumulative exposure. OBJECTIVES: The aim of the present study was to examine: a) the transcriptomic response of rainbow trout to combined impact of two environmental stressors, the prototype estrogenic-active compound 17b-estradiol (E2) and an infectious agent, the myxozoan parasite Tetracapsuloides bryosalmonae; and b) how the molecular response relates to the fish’s ability to cope with the parasitic disease. METHODS: In order to be able to detect unexpected and multifaceted transcriptomic responses as they may result from the combined exposure, we used a trout cDNA microarray platform. Additionally, intensity of host infection with the parasite and cumulative mortality were recorded. RESULTS: The microarray analysis of the hepatic transcriptome revealed distinct response patterns or transcription modules (TMs). Combined treatment of rainbow trout with PKD and E2 resulted in either an intermediate or additive response, as it was the case in TM1, 2 and 4, or it resulted in a clear hierarchy between the two stressors, as in the immune gene-enriched TM 3 for which the fish prioritized the impact of the infectious agent over the E2 impact. Additionally, the estrogenic diet had neither a significant influence on the intensity of parasitic infection nor on PKD-related mortality. CONCLUSION: These findings indicate that under cumulative impact of multiple stressors the organism can respond in a flexible way depending on the nature of the stressor and the pathway affected.