title: Could thermal sensitivity of mitochondria determine species distribution in a changing climate?
abstract: For many aquatic species, the upper thermal limit (Tmax) and the heart failure temperature (THF) are only a few degrees away from the species' current environmental temperatures. While the mechanisms mediating temperature-induced heart failure (HF) remain unresolved, energy flow and/or oxygen supply disruptions to cardiac mitochondria may be impacted by heat stress. Recent work using a New Zealand wrasse (Notolabrus celidotus) found that ATP synthesis capacity of cardiac mitochondria collapses prior to T(HF). However, whether this effect is limited to one species from one thermal habitat remains unknown. The present study confirmed that cardiac mitochondrial dysfunction contributes to heat stress-induced HF in two additional wrasses that occupy cold temperate (Notolabrus fucicola) and tropical (Thalassoma lunare) habitats. With exposure to heat stress, T. lunare had the least scope to maintain heart function with increasing temperature. Heat-exposed fish of all species showed elevated plasma succinate, and the heart mitochondria from the cold temperate N. fucicola showed decreased phosphorylation efficiencies (depressed respiratory control ratio, RCR), cytochrome c oxidase (CCO) flux and electron transport system (ETS) flux. In situ assays conducted across a range of temperatures using naive tissues showed depressed complex II (CII) and CCO capacity, limited ETS reserve capacities and lowered efficiencies of pyruvate uptake in T. lunare and N. celidotus. Notably, alterations of mitochondrial function were detectable at saturating oxygen levels, indicating that cardiac mitochondrial insufficiency can occur prior to HF without oxygen limitation. Our data support the view that species distribution may be related to the thermal limits of mitochondrial stability and function, which will be important as oceans continue to warm.
authors.affiliation: Applied Surgery and Metabolism Group, School of Biological Sciences, University of Auckland, Auckland 1142, New Zealand.
authors.forename: Fathima I
authors.initials: FI
authors.lastname: Iftikar
authors.affiliation: Applied Surgery and Metabolism Group, School of Biological Sciences, University of Auckland, Auckland 1142, New Zealand.
authors.forename: Julia R
authors.initials: JR
authors.lastname: MacDonald
authors.affiliation: International Centre for Sturgeon Studies, Vancouver Island University, Nanaimo, BC, Canada, V9R 5S5.
authors.forename: Daniel W
authors.initials: DW
authors.lastname: Baker
authors.affiliation: School of Physiotherapy and Exercise Science, Griffith University, Gold Coast, QLD 9726, Australia.
authors.forename: Gillian M C
authors.initials: GM
authors.lastname: Renshaw
authors.affiliation: Applied Surgery and Metabolism Group, School of Biological Sciences, University of Auckland, Auckland 1142, New Zealand a.hickey@auckland.ac.nz.
authors.forename: Anthony J R
authors.initials: AJ
authors.lastname: Hickey
mesh_terms: D000818:Animals; D019069:Cell Respiration; D057231:Climate Change; D017753:Ecosystem; D004579:Electron Transport; D003576:Electron Transport Complex IV / Q000235:genetics / Q000378:metabolism; D029941:Fish Proteins / Q000235:genetics / Q000378:metabolism; D006321:Heart / Q000503:physiopathology*; D018869:Heat-Shock Response; D008929:Mitochondria, Heart / Q000378:metabolism*; D010473:Perciformes / Q000502:physiology*; D013045:Species Specificity; D019802:Succinic Acid / Q000097:blood
chemical_list: D029941:Fish Proteins; D019802:Succinic Acid; D003576:Electron Transport Complex IV
keywords: Cardiac mitochondria; Fish; Heart failure; Oxidative phosphorylation; Thermal limits