Biological rhythms in the deep-sea hydrothermal mussel Bathymodiolus azoricus

Audrey M Mat,Christine Dubreuil,Gabriel V Markov,Marjolaine Matabos,Arnaud Tanguy,Vincent Apremont,Caroline Fabioux,Pierre-Marie Sarradin,Arnaud Huvet,Jozée Sarrazin,Christophe Klopp,Camille Eché

doi:10.1038/s41467-020-17284-4

Abstract

Biological rhythms are a fundamental property of life. The deep ocean covers 66% of our planet surface and is one of the largest biomes. The deep sea has long been considered as an arrhythmic environment because sunlight is totally absent below 1,000 m depth. In the present study, we have sequenced the temporal transcriptomes of a deep-sea species, the ecosystem-structuring vent mussel Bathymodiolus azoricus. We reveal that tidal cycles predominate in the transcriptome and physiology of mussels fixed directly at hydrothermal vents at 1,688 m depth at the Mid-Atlantic Ridge, whereas daily cycles prevail in mussels sampled after laboratory acclimation. We identify B. azoricus canonical circadian clock genes, and show that oscillations observed in deep-sea mussels could be either a direct response to environmental stimulus, or be driven endogenously by one or more biological clocks. This work generates in situ insights into temporal organisation in a deep-sea organism.

Highlights

Biological rhythms are a fundamental property of life
The Dutilleul multifrequential periodogram analysis (MFPA) revealed that 12.5 h and 26.3 h were the dominant periods in the percentage of opened mussels (p-value < 0.05)
Because a progressive diversification from shallow- to deep-water species has been suggested for vent species[45], we investigated in parallel mussels’ physiology in the lab under a 12 h:12 h L:D schedule to determine whether B. azoricus could still respond to light

Summary

Introduction

Biological rhythms are a fundamental property of life. The deep ocean covers 66% of our planet surface and is one of the largest biomes. We have sequenced the temporal transcriptomes of a deep-sea species, the ecosystem-structuring vent mussel Bathymodiolus azoricus. We identify B. azoricus canonical circadian clock genes, and show that oscillations observed in deep-sea mussels could be either a direct response to environmental stimulus, or be driven endogenously by one or more biological clocks. This work generates in situ insights into temporal organisation in a deep-sea organism These oscillators temporally shape living systems from the molecular to the organismal level, generating biological rhythms that are ubiquitous across taxa[1]. A circadian clock has only been shown in a deep-sea species by exposing Nephrops norvegicus living naturally between and 500 m depth to experimental L:D cycles and constant conditions in the laboratory[18]; clock genes candidates were identified[19]. There is evidence of lunar rhythms and seasonal cycles in the reproduction of deep-water invertebrates in the field and in the laboratory[23]

Methods

Results

Conclusion