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Partnerships for enhanced engagement in research (PEER) SCIENCE
Cycle 2 (2012 Deadline)

Biodiversity and adaptations of CYP enzymes in the Amazon Loricariidae fishes

PI: Thiago Parente (, Fundação Oswaldo Cruz (Fiocruz), (formerly at Universidade Federal do Rio de Janeiro)
U.S. Partners: Mark Hahn and John Stegeman (Woods Hole Oceanographic Institution)
Project Dates: September 2013 to June 2016

Link to Project Blog

2-435 Zebra Fish
The Hypancistrus zebra, an endangered Loricariidae species. This specimen was provided by the local wildlife authorities, who had seized a large number of fish that had been illegally caught by poachers but were not suitable for release to the wild (Photo: Dr. Parente)
CYP1 enzymes are responsible for the biotransformation of natural compounds and anthropogenic pollutants. Usually the reactions catalyzed by CYP1 enzymes lead to detoxification, when the compound is eliminated from the body without causing harm. CYP1 enzymes, however, are also known to catalyze bioactivation reactions, in which one of the reaction products is more toxic than its parent compound. The equilibrium between the detoxification (beneficial) and bioactivation (detrimental) roles of CYP1 enzymes has been fine tuned for each and every vertebrate species over the course of evolution. This PEER Science project is closely aligned with the National Science Foundation-supported work of the U.S. partner, Dr. Mark Hahn, as both involve the study of different naturally evolved and selected solutions for the same issue: the balance between detoxification and bioactivation by CYP1 enzymes using fish species as vertebrate models. The adaptation of Killifish (studied by Dr. Hahn) is a well documented event classified as dramatic, rapid, convergent, and triggered by anthropogenic pollutants that balance the dual role of CYP1 enzymes at the gene expression level. However, the adaptation of Loricariidae fish is poorly known and most probably can have the opposite classification: gradual, slow, divergent, and triggered by chemicals naturally present in the fish microhabitat. The goals of this project are to determine whether the adaptations of CYP1 enzymes in Loricariidae fishes are convergent or divergent and how they change the susceptibility of this species to the toxic effects of petrogenic compounds.

Dr. Parente and his research team will sequence the CYP1 genes of 100 Loricariidae species from the Amazon, and these gene sequences will be used to determine the enzyme sequences, which in turn will be aligned and compared for amino acids substitutions and interaction with classical CYP1 substrates. Selected Loricariidae species will be used for biological assays to evaluate the toxic effects of petrogenic derivates and their molecular mechanisms of action. Due to the current and future prospects for crude oil drilling activities in the Amazon region, it is imperative to understand the metabolism of petrogenic hydrocarbons by Amazonian biota. This is especially true in the case of Loricariidae fishes, as it is already known that those species have CYP1 enzymes with distinct affinity for substrates. It needs to be determined whether these changes will unbalance the evolved equilibrium of CYP1 dual roles to the beneficial or to the detrimental side. This knowledge will be crucial to better evaluate the risks of oil drilling activities for Amazonian biodiversity.

Summary of Recent Activities

During the third quarter of 2015, the remaining 12 transcriptomes and mitogenomes were assembled and annotated. Phylogenetic analyses of Loricariidae subfamilies were performed using the complete sequences of all the 13 mitochondrial genes, and Dr. Parente and his colleagues are preparing a manuscript on the results. Three previously submitted manuscripts have been accepted so far, of which one has been published, another is available online, and the third is being processed by Elsevier for online publication. Another manuscript, entitled “The complete mitochondrial genome of Corydoras nattereri (Callichthyidae Siluriformes), is in the final stage of preparation and should be submitted to the journal Neotropical Ichthyology in November. Another manuscript on the species, Hoplosternum littorale, is also in preparation. During these recent months, Dr. Parente and his team have been actively communicating the data generated and analyzed so far, but a large amount of data remains to be analyzed. For example, they are analyzing a total of 1189 CYP transcripts covering more than 75 percent of their own zebrafish ortholog complete coding sequence (CDS) were sequenced on the 39 liver transcriptomes. A preliminary phylogenetic tree showing the relationships among those transcripts has been created.

Brazil Partnership Photo 1Brazil Partnership Photo B
The research team at the Andorinhas waterfall on the Roncador river in the district of Santo Alexio. Pictured are Paolo Buckup (top), Emmanuel Neuhaus (center), Thiago Parente (left foreground), and Jose Gomes (right foreground). (Photo: Carla Quijada).Labwork to obtain sequencing of genes (Photo: Dr. Parente).

The PI attended the international meeting PRiMO 18 (Pollutant Responses in Marine Organisms) in Trondheim, Norway, May 24-27, 2015, where he met with U.S. collaborators on the project. Dr. Parente, accompanied by the two undergraduate students and the computational biology specialist on the project, also attended the international meeting Evolution 2015, the joint annual meeting of the Society for the Study of Evolution, the Society of Systematic Biologists, and the American Society of Naturalists. This event, which took place in Guarujá, Brazil, June 26-30, marked the first time the conference had been held outside the United States. Dr. Parente and his team presented two posters and two flash talks.

In the coming months, plans call for completing data analyses for CYP biodiversity and molecular evolution in Loricariidae and investigating molecular biodiversity and adaptation on other gene families, for example the Flavin monooxigenases (FMO), in collaboration with Dr. Daniel Schlenk and his student from UC Riverside. An additional field visit to sample fish species in Guyana is also being organized, pending the receipt of the necessary permit, and after the trip the team will sequence and analyze transcriptomes from the Guyanese fish samples and evaluated adaptive responses for selected species. The excursion to Guyana will provide an opportunity to sample two particular species, Lithogenes sp. and Corymbophanes sp. In order to increase the chances to collect those species, and also for safety reasons, the excursion must happen in one of the few dry months in Guyana, which are September-October or February-March. On the outreach side, further interactions are expected with stakeholders from FIOCRUZ, IBAMA, ICMBio, the Brazilian Federal Police, the private (fish exporters) and third (NGO) sectors, and individual fishermen to promote the goal of managing wildlife populations of Loricariidae fish and making their commercial exploitation sustainable. A no-cost extension on this project has been issued through June 2016 to allow for more time to complete the field work and subsequent analyses.

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