Interspecific correlation between red blood cell mitochondrial ROS production, cardiolipin content and longevity in birds

Abstract

Mitochondrial respiration releases reactive oxygen species (ROS) as by-products that can damage the soma and may in turn accelerate ageing. Hence, according to "the oxidative stress theory of ageing", longer-lived organisms may have evolved mechanisms that improve mitochondrial function, reduce ROS production and/or increase cell resistance to oxidative damage. Cardiolipin, an important mitochondrial innermembrane phospholipid, has these properties by binding and stabilizing mitochondrial inner-membrane proteins. Here, we investigated whether ROS production, cardiolipin content and cell membrane resistance to oxidative attack in freshly collected red blood cells (RBCs) are associated with longevity (range 5-35 years) in 21 bird species belonging to seven Orders. After controlling for phylogeny, body size and oxygen consumption, variation in maximum longevity was significantly explained by mitochondrial ROS production and cardiolipin content, but not by membrane resistance to oxidative attack. RBCs of longer-lived species produced less ROS and contained more cardiolipin than RBCs of shorter-lived species did. These results support the oxidative stress theory of ageing and shed light on mitochondrial cardiolipin as an important factor linking ROS production to longevity.

How to measure mitochondrial function in birds using red blood cells: a case study in the king penguin and perspectives in ecology and evolution

“…; Delhaye et al . ). Interestingly, it is now possible to simultaneously record O 2 consumption and fluorescence signal, using the O2k‐fluorescence module (Oroboros Instruments, Innsbruck, Austria) that could be added to the O2k‐Oroboros device that we used in this study.…”

“…Assessing ROS production is challenging, but has already being done using fluorescent probes in non-mammalian vertebrate RBCs (e.g. Olsson et al 2008;Stier et al 2014a;Delhaye et al 2016). Interestingly, it is now possible to simultaneously record O 2 consumption and fluorescence signal, using the O2k-fluorescence module (Oroboros Instruments, Innsbruck, Austria) that could be added to the O2k-Oroboros device that we used in this study.…”

“…In animals more than 90% of the cellular energy is produced as adenosine triphosphate (ATP) during mitochondrial respiration (Nicholls & Ferguson 2002). Hence, our understanding of the evolutionary success of particular individuals requires insights into the factors that shape mitochondrial function (defined here as the ability to use O 2 to oxidize substrate and produce ATP and heat) and the downstream effects that mitochondrial function can exert on life histories (Salin et al 2012;Toews et al 2013;Hill 2014;Stier et al 2014a,b;Stier, Massemin & Criscuolo 2014c;Salin et al 2015;Schwartz, Arendsee & Bronikowski 2015;Bar-Yaacov et al 2015;Koch, Josefson & Hill 2016;Delhaye et al 2016).…”

Longevity and life history coevolve with oxidative stress in birds

“…According to our study, species with longer lifespan suffer less oxidative damage to lipids. This finding is probably the consequence of long‐lived species having membranes that are exposed to less ROS (Barja, ; Buttemer et al, ; Delhaye et al, ) and that are constitutively less vulnerable to oxidation insults due to their lower PUFA content (Buttemer et al, ; Galván et al, ; Hulbert et al, ; Naudí et al, ). This finding supports a cornerstone prediction of the OSTA and has important implications.…”

“…A lower ROS level has obvious physiological advantages, while lower PUFA content renders membranes higher resistance against peroxidative damage (Hulbert, Pamplona, Buffenstein, & Buttemer, 2007;Pamplona et al, 2002). Interspecific comparative studies demonstrated that cell cultures originating from long-lived species are more resistant against oxidative challenges than those of short-lived ones (Harper et al, 2011;Miller, Williams, & Kiklevich, 2011) and that longer lifespan coevolves with a lower rate of ROS generation (Delhaye et al, 2016;Lambert et al, 2007;Pamplona & Barja, 2011;Shi, Buffenstein, Pulliam, & Remmen, 2010) and lower membrane PUFA content (Barja, 2013;Buttemer, Battam, & Hulbert, 2008;Galván et al, 2015;Hulbert et al, 2007;Pamplona & Barja, 2011;Pamplona et al, 2002). A supposed consequence of lower ROS generation and lower membrane PUFA content of long-lived species is their lower level of oxidative lipid damage.…”