Thermal Limit for Metazoan Life in Question: In Vivo Heat Tolerance of the Pompeii Worm

Abstract

The thermal limit for metazoan life, expected to be around 50°C, has been debated since the discovery of the Pompeii worm Alvinella pompejana, which colonizes black smoker chimney walls at deep-sea vents. While indirect evidence predicts body temperatures lower than 50°C, repeated in situ temperature measurements depict an animal thriving at temperatures of 60°C and more. This controversy was to remain as long as this species escaped in vivo investigations, due to irremediable mortalities upon non-isobaric sampling. Here we report from the first heat-exposure experiments with live A. pompejana, following isobaric sampling and subsequent transfer in a laboratory pressurized aquarium. A prolonged (2 hours) exposure in the 50–55°C range was lethal, inducing severe tissue damages, cell mortalities and triggering a heat stress response, therefore showing that Alvinella’s upper thermal limit clearly is below 55°C. A comparison with hsp70 stress gene expressions of individuals analysed directly after sampling in situ confirms that Alvinella pompejana does not experience long-term exposures to temperature above 50°C in its natural environment. The thermal optimum is nevertheless beyond 42°C, which confirms that the Pompeii worm ranks among the most thermotolerant metazoans.

Antagonistic evolution of an antibiotic and its molecular chaperone: how to maintain a vital ectosymbiosis in a highly fluctuating habitat

“…The level of expression of the BRICHOS containing preproalvinellacin gene was evaluated under two stressful conditions previously shown to induce the synthesis of molecular chaperones (Heat shock proteins, Hsp) in Alvinella pompejana 48 . Both the preproalvinellacin and the Hsp70, quantified by RT-qPCR, produced exactly the same pattern of gene expression in worms submitted to various temperatures and pressure stresses (Fig.…”

Proteome evolution of deep-sea hydrothermal vent alvinellid polychaetes supports the ancestry of thermophily and subsequent adaptation to cold in some lineages

“…Out of the twelve species described so far, at least five live on the walls of “hot” vent chimneys. Two of these worms, A. pompejana and P. sulfincola , have been experimentally shown to be the most thermophilic metazoans known on Earth (Girguis and Lee 2006; Ravaux et al. 2013).…”

“…While it is known that a diversity of animals can live at temperatures up to 50° C, notably the scorpions Buthidae, the desert ants Cataglyphis , ostracods from geothermal settings, and alvinellids at hydrothermal vents (Wickstrom and Castenholz 1973; Gehring and Wehner 1995; Girguis and Lee 2006; Ravaux et al. 2013), we do not know whether these organisms exhibit specific residue patterns when compared with closely related mesophilic or psychrophilic species.…”

Fructose metabolism as a common evolutionary pathway of survival associated with climate change, food shortage and droughts

“…While often the focus is on those species that failed to survive, in many respects it is the survivors that deserve the most attention, for many of these animals have developed remarkable means of survival. Today, there are many examples of ‘extremophile’ species that can survive under remarkable situations, such as the Pompeii worm that can survive inferno (176°F) temperatures , or the occellated icefish that lives in the Antarctic seas in the absence of red blood cells , or the wood frog in northern Canada who freezes in winter, surviving because of the production of glycerol that acts as an antifreeze to allow slow circulation of blood in the freezing conditions .…”