Metabolic and transcriptional responses of gilthead sea bream (Sparus aurata L.) to environmental stress: new insights in fish mitochondrial phenotyping

Azucena Bermejo-Nogales; Marit Nederlof; Laura Benedito-Palos; Gabriel F Ballester-Lozano; Ole Folkedal; Rolf Eric Olsen; Ariadna Sitjà-Bobadilla; Jaume Pérez-Sánchez

doi:10.1016/j.ygcen.2014.04.016

Metabolic and transcriptional responses of gilthead sea bream (Sparus aurata L.) to environmental stress: new insights in fish mitochondrial phenotyping

Gen Comp Endocrinol. 2014 Sep 1:205:305-15. doi: 10.1016/j.ygcen.2014.04.016. Epub 2014 Apr 30.

Authors

Azucena Bermejo-Nogales¹, Marit Nederlof², Laura Benedito-Palos³, Gabriel F Ballester-Lozano⁴, Ole Folkedal⁵, Rolf Eric Olsen⁶, Ariadna Sitjà-Bobadilla⁷, Jaume Pérez-Sánchez⁸

Affiliations

¹ Nutrigenomics and Fish Growth Endocrinology Group, Department of Marine Species Biology, Culture and Pathology, Institute of Aquaculture Torre de la Sal, IATS-CSIC, 12595 Ribera de Cabanes s/n, Castellón, Spain. Electronic address: a.bermejo.nogales@csic.es.
² Aquaculture and Fisheries Group, Wageningen University, De Elst, 6708 WD Wageningen, The Netherlands. Electronic address: majnederlof@gmail.com.
³ Nutrigenomics and Fish Growth Endocrinology Group, Department of Marine Species Biology, Culture and Pathology, Institute of Aquaculture Torre de la Sal, IATS-CSIC, 12595 Ribera de Cabanes s/n, Castellón, Spain. Electronic address: l.benedito@csic.es.
⁴ Nutrigenomics and Fish Growth Endocrinology Group, Department of Marine Species Biology, Culture and Pathology, Institute of Aquaculture Torre de la Sal, IATS-CSIC, 12595 Ribera de Cabanes s/n, Castellón, Spain. Electronic address: gabriel.ballester@csic.es.
⁵ Institute of Marine Research Matre, 5984 Matredal, Norway. Electronic address: ole.folkedal@imr.no.
⁶ Institute of Marine Research Matre, 5984 Matredal, Norway. Electronic address: rolf.erik.olsen@imr.no.
⁷ Fish Pathology Group, Department of Marine Species Biology, Culture and Pathology, Institute of Aquaculture Torre de la Sal, IATS-CSIC, 12595 Ribera de Cabanes s/n, Castellón, Spain. Electronic address: ariadna.sitja@csic.es.
⁸ Nutrigenomics and Fish Growth Endocrinology Group, Department of Marine Species Biology, Culture and Pathology, Institute of Aquaculture Torre de la Sal, IATS-CSIC, 12595 Ribera de Cabanes s/n, Castellón, Spain. Electronic address: jaime.perez.sanchez@csic.es.

PMID: 24792819
DOI: 10.1016/j.ygcen.2014.04.016

Abstract

The aim of the current study was to phenotype fish metabolism and the transcriptionally-mediated response of hepatic mitochondria of gilthead sea bream to intermittent and repetitive environmental stressors: (i) changes in water temperature (T-ST), (ii) changes in water level and chasing (C-ST) and (iii) multiple sensory perception stressors (M-ST). Gene expression profiling was done using a quantitative PCR array of 60 mitochondria-related genes, selected as markers of transcriptional regulation, oxidative metabolism, respiration uncoupling, antioxidant defense, protein import/folding/assembly, and mitochondrial dynamics and apoptosis. The mitochondrial phenotype mirrored changes in fish performance, haematology and lactate production. T-ST especially up-regulated transcriptional factors (PGC1α, NRF1, NRF2), rate limiting enzymes of fatty acid β-oxidation (CPT1A) and tricarboxylic acid cycle (CS), membrane translocases (Tim/TOM complex) and molecular chaperones (mtHsp10, mtHsp60, mtHsp70) to improve the oxidative capacity in a milieu of a reduced feed intake and impaired haematology. The lack of mitochondrial response, increased production of lactate and negligible effects on growth performance in C-ST fish were mostly considered as a switch from aerobic to anaerobic metabolism. A strong down-regulation of PGC1α, NRF1, NRF2, CPT1A, CS and markers of mitochondrial dynamics and apoptosis (BAX, BCLX, MFN2, MIRO2) occurred in M-ST fish in association with the greatest circulating cortisol concentration and a reduced lactate production and feed efficiency, which represents a metabolic condition with the highest allostatic load score. These findings evidence a high mitochondrial plasticity against stress stimuli, providing new insights to define the threshold level of stress condition in fish.

Keywords: Husbandry stress; Mitochondrial metabolism; Teleost; Thermal stress.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Environment*
Gene Expression Profiling
Gene Expression Regulation
Metabolomics
Mitochondria / genetics*
Mitochondria / metabolism*
Phenotype
Sea Bream / blood
Sea Bream / genetics*
Sea Bream / metabolism*
Sensation / physiology
Stress, Physiological*
Transcription, Genetic*