Abstract
The emblematic hydrothermal worm Alvinella pompejana is one of the most thermo tolerant animal known on Earth. It relies on a symbiotic association offering a unique opportunity to discover biochemical adaptations that allow animals to thrive in such a hostile habitat. Here, by studying the Pompeii worm, we report on the discovery of the first antibiotic peptide from a deep-sea organism, namely alvinellacin. After purification and peptide sequencing, both the gene and the peptide tertiary structures were elucidated. As epibionts are not cultivated so far and because of lethal decompression effects upon Alvinella sampling, we developed shipboard biological assays to demonstrate that in addition to act in the first line of defense against microbial invasion, alvinellacin shapes and controls the worm's epibiotic microflora. Our results provide insights into the nature of an abyssal antimicrobial peptide (AMP) and into the manner in which an extremophile eukaryote uses it to interact with the particular microbial community of the hydrothermal vent ecosystem. Unlike earlier studies done on hydrothermal vents that all focused on the microbial side of the symbiosis, our work gives a view of this interaction from the host side.
Highlights
Alvinella pompejana is a polychaetous annelid that inhabits active deep-sea hydrothermal vents along the East Pacific Rise, where it colonizes the walls of actively venting high-temperature chimneys [1]
Nature of Alvinella antimicrobial peptide (AMP) and evolutionary link with AMPs from coastal species To date, only one AMP isolated from marine species belongs to an AMP family already characterized in terrestrial species [11]
The anatomy of annelids is characterized by the presence of a coelom, a compartment that includes mobile cells, named coelomocytes that sterilize the coelomic fluid by releasing humoral factors such as antimicrobial peptides (AMPs) [26]
Summary
Alvinella pompejana is a polychaetous annelid that inhabits active deep-sea hydrothermal vents along the East Pacific Rise, where it colonizes the walls of actively venting high-temperature chimneys [1]. The environment of the worm is characterized by extreme physicochemical gradients, high pressure and bursts of elevated temperatures which can be as high as 105uC [2]. Numerous studies, including metagenomic analyses, evidenced that the microflora is composed of a multispecies complex of 12 to 15 phylotypes of which .98% are Epsilonproteobacteria, a dominating taxonomic group in hydrothermal vents [7]. These bacteria have been suggested to provide
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