Moderately lower temperatures greatly extend the lifespan of Brachionus manjavacas (Rotifera): Thermodynamics or gene regulation?

Abstract

Environmental temperature greatly affects lifespan in a wide variety of animals, but the exact mechanisms underlying this effect are still largely unknown. A moderate temperature decrease from 22°C to 16°C extends the lifespan of the monogonont rotifer Brachionus manjavacas by up to 163%. Thermodynamic effects on metabolism contribute to this increase in longevity, but are not the only cause. When rotifers are exposed to 16°C for four days and then transfered to 22°C, they survive until day 13 at nearly identical rates as rotifers maintained at 16°C continuously. This persistence of the higher survival for nine days after transfer to 22°C suggests that low temperature exposure alters the expression of genes that affect the rate of aging. The relative persistence of the gene regulation effect suggests that it may play an even larger role in slowing aging than the thermodynamic effects. The life extending effects of these short-term low temperature treatments are largest when the exposure happens early in the life cycle, demonstrating the importance of early development. There is no advantage to lowering the temperature below 16°C to 11° or 5°C. Rotifers exposed to 16°C also displayed increased resistance to heat, starvation, oxidative and osmotic stress. Reproductive rates at 16°C were lower than those at 22°C, but because they reproduce longer, there is no significant change in the lifetime fecundity of females. To investigate which genes contribute to these effects, the expression of specific temperature sensing genes was knocked down using RNAi. Of 12 genes tested, RNAi knockdown of four eliminated the survival enhancing effects of the four-day cold treatment: TRP7, forkhead box C, Y-box factor, and ribosomal protein S6. This demonstrates that active gene regulation is an important factor in temperature mediated life extension, and that these particular genes play an integral role in these pathways. As a thermoresponsive sensor, TRP7 may be responsible for triggering the signaling cascade contributing to temperature mediated life extension. The TRP genes may also provide especially promising candidates for targeted gene manipulations or pharmacological interventions capable of mimicking the effects of low temperature exposure. These results support recent theories of aging that claim rate of aging is determined by an actively regulated genetic mechanism rather than an accumulation of molecular damage.

Variation in the life cycle of monogonont rotifers: Commitment to sex and emergence from diapause

“…This possibility may be more likely in temperate than in tropical or polar regions. Lifespan in some rotifers is extended by low temperature (Halbach, ; Johnston & Snell, ; Snell, ; Snell & King, ), dietary restriction (Gribble & Mark Welch, ; Halbach & Halbach‐Keup, ; Kirk, ; Weithoff, ), and hypoxia (Snell, Johnston, & Jones, ). The study by Johnston & Snell on the effect of temperature on survival, reproduction, and stress tolerance in B. manjavaca s ( B. plicatilis species complex) is particularly instructive.…”

When males outlive females: Sex‐specific effects of temperature on lifespan in a cyclic parthenogen

“…Their different responses to temperature manipulation might be expected, as there seems to be a link between nutrient and thermal sensing, metabolism, and longevity (Horikawa et al., ). Recently, Johnston and Snell () observed that lifespans of closely related rotifer species respond differently to temperature manipulation. Even more closely, Henning‐Lucass, Cordellier, Streit, and Schwenk (), studying the response to temperature in Daphnia galeata clones of different age (i.e., hatched from resting eggs of different age), found no overall effect of temperature on Daphnia survival rate, as individuals from clones of different age reacted differently.…”

“…The temperature effect on lifespan is not merely a passive process, but is under gene regulation (Johnston & Snell, 2016;Keil et al, 2015;Xiao et al, 2013). Hence, intraspecific differences in how genotypes and phenotypes, here sexes, respond in lifespan to temperature change are very much expected.…”

“…Zhang et al (2016) showed temperature differentially regulates the nematode lifespan at different life stages via a single pathway. Results obtained in a recent study using rotifers suggested that multiple pathways are involved in temperature mediated life extension, among them a complex signaling cascade regulated by a sensory receptor (Johnston & Snell, 2016). In Daphnia, temperature changes patterns of heat shock protein expression in a sex-specific manner (Mikulski et al, 2011), which may have consequences for their lifespans (Schumpert, Anderson, Dudycha, & Patel, 2016).…”

“…() observed Daphnia males choose deeper water strata than females and, in consequence, experience temperatures even 4°C colder than females. Similar differences lead to increased lifespan of planktonic ectotherms (e.g., rotifers: Bosque, Hernandez, Perez, Todolı, & Oltra, ; Johnston & Snell, ; copepods: Brugnano, Guglielmo, Ianora, & Zagami, ; Kiørboe, Ceballos, & Thygesen, ; cladocerans: Orcutt & Porter, ; Engert et al., ), both via physical effect of decreased metabolic rate and via changes in gene expression (Johnston & Snell, ; see also a review by Keil, Cummings, & de Magalhães, ). Indeed, Daphnia choosing deeper, and thus colder, strata have been shown to live longer (Pietrzak et al., ).…”