Understanding drivers of biodiversity patterns is essential to evaluate the potential impact of deep-sea mining on ecosystems resilience. While the South West Pacific forms an independent biogeographic province for hydrothermal vent fauna, different degrees of connectivity among basins were previously reported for a variety of species depending on their ability to disperse. In this study, we compared phylogeographic patterns of several vent gastropods across South West Pacific back-arc basins and the newly-discovered La Scala site on the Woodlark Ridge by analysing their genetic divergence using a barcoding approach. We focused on six genera of vent gastropods widely distributed in the region: Lepetodrilus, Symmetromphalus, Lamellomphalus, Shinkailepas, Desbruyeresia and Provanna. A wide-range sampling was conducted at different vent fields across the Futuna Volcanic Arc, the Manus, Woodlark, North Fiji, and Lau Basins, during the CHUBACARC cruise in 2019. The Cox1-based genetic structure of geographic populations was examined for each taxon to delineate putative cryptic species and assess potential barriers or contact zones between basins. Results showed contrasted phylogeographic patterns among species, even between closely related species. While some species are widely distributed across basins (i.e. Shinkailepas tollmanni, Desbruyeresia melanioides and Lamellomphalus) without evidence of strong barriers to gene flow, others are restricted to one (i.e. Shinkailepas tufari complex of cryptic species, Desbruyeresia cancellata and D. costata). Other species showed intermediate patterns of isolation with different lineages separating the Manus Basin from the Lau/North Fiji Basins (i.e. Lepetodrilus schrolli, Provanna and Symmetromphalus spp.). Individuals from the Woodlark Basin were either endemic to this area (though possibly representing intermediate OTUs between the Manus Basin and the other eastern basins populations) or, coming into contact from these basins, highlighting the stepping-stone role of the Woodlark Basin in the dispersal of the South West Pacific vent fauna. Results are discussed according to the dispersal ability of species and the geological history of the South West Pacific.

The polychaete family Polynoidae (scale-worms) is well-represented at deep sea hydrothermal vents. Most species are free-living in a wide range of habitats: from high-temperature hydrothermal `chimney' walls to diffuse venting areas. Conversely, species of the genus Branchipolynoe live inside the mantle cavity of vent and seep mytilids. Specimens, morphologically close to Branchipolynoe seepensis, have been reported from all the known vent areas on the Mid-Atlantic Ridge (MAR), with varying infestation rates (0–6 individuals per host). Reproductive tract, gametogenesis and population structures were examined for specimens from the Lucky Strike vent field (MAR) in order to test whether this species displays dwarf males, protandric hermaphroditism or differential mortality between males and females. Observations of histological sections reveal the presence of fully developed ovaries in females which originate ventrally in segments 7–9 and of an unusual genital tract in which both sperm and mature oocytes are stored. Oogenesis is intraovarian and quasi-continuous. The vitellogenic oocytes are only free in the coelom at their terminal growing stage and are then transferred into an ovisac through spermathecae. The species displays an external sexual dimorphism in the number of genital papillae and the shape of the pygidial appendages. Sex ratios showed significant deviations from a 1:1 expected ratio, in favour of females. The modal decompositions of size–frequency histograms show the occurrence of three modes in females and only two modes in males, indicating discrete breeding periods. The two first modes were not significantly different between males and females. These results indicate that B. seepensis forms heterosexual pairs and uses internal fertilization to reproduce during discrete spawning periods. Differential mortality between males and females is likely to shape size-histograms as observed by preventing males from reaching the female proportions. Such an observation could be a result of either cannibalism on larger males, small sizes facilitating the male escape, or natural predation when males move from one bivalve to another to breed.

Antimicrobial peptides (AMPs) are natural antibiotics produced by all living organisms. In metazoans, they act as host defense factors by eliminating microbial pathogens. But they also help to select the colonizing bacterial symbionts while coping with specific environmental challenges. Although many AMPs share common structural characteristics, for example having an overall size between 10–100 amino acids, a net positive charge, a γ-core motif, or a high content of cysteines, they greatly differ in coding sequences as a consequence of multiple parallel evolution in the face of pathogens. The majority of AMPs is specific of certain taxa or even typifying species. This is especially the case of annelids (ringed worms). Even in regions with extreme environmental conditions (polar, hydrothermal, abyssal, polluted, etc.), worms have colonized all habitats on Earth and dominated in biomass most of them while co-occurring with a large number and variety of bacteria. This review surveys the different structures and functions of AMPs that have been so far encountered in annelids and nematodes. It highlights the wide diversity of AMP primary structures and their originality that presumably mimics the highly diverse life styles and ecology of worms. From the unique system that represents marine annelids, we have studied the effect of abiotic pressures on the selection of AMPs and demonstrated the promising sources of antibiotics that they could constitute.

Alvinella pompejana lives on the top of chimneys at deep–sea hydrothermal vents of the East Pacific Rise. It is thought to be one of the most thermotolerant and eurythermal metazoans. Our experimental approach combines methods of population genetics and biochemistry, considering temperature as a potential selective factor. Phosphoglucomutase (Pgm–1 locus) is one of the most polymorphic loci of A. pompejana and exhibits four alleles, from which alleles 90 and 100 dominate with frequencies of approximately 0.5 in populations. Results from previous studies suggested that allele 90 might be more thermostable than allele 100. Significant genetic differentiation was found by comparing contrasted microhabitats, especially the young, still hot, versus older and colder chimneys, with allele 90 being at highest frequency on young chimneys. Moreover the frequency of allele 90 was positively correlated with mean temperature at the opening of Alvinella tubes. In parallel, thermostability and thermal optimum experiments demonstrated that allele 90 is more thermostable and more active at higher temperatures than allele 100. This dataset supports an additive model of diversifying selection in which allele 90 is favoured on young hot chimneys but counterbalanced over the whole metapopulation by the dynamics of the vent ecosystem.

Background: Alvinella pompejana is a representative of Annelids, a key phylum for evo-devo studies that is still poorly studied at the sequence level. A. pompejana inhabits deep-sea hydrothermal vents and is currently known as one of the most thermotolerant Eukaryotes in marine environments, withstanding the largest known chemical and thermal ranges (from 5 to 105°C). This tube-dwelling worm forms dense colonies on the surface of hydrothermal chimneys and can withstand long periods of hypo/anoxia and long phases of exposure to hydrogen sulphides. A. pompejana specifically inhabits chimney walls of hydrothermal vents on the East Pacific Rise. To survive, Alvinella has developed numerous adaptations at the physiological and molecular levels, such as an increase in the thermostability of proteins and protein complexes. It represents an outstanding model organism for studying adaptation to harsh physicochemical conditions and for isolating stable macromolecules resistant to high temperatures. Results: We have constructed four full length enriched cDNA libraries to investigate the biology and evolution of this intriguing animal. Analysis of more than 75,000 high quality reads led to the identification of 15,858 transcripts and 9,221 putative protein sequences. Our annotation reveals a good coverage of most animal pathways and networks with a prevalence of transcripts involved in oxidative stress resistance, detoxification, anti-bacterial defence, and heat shock protection. Alvinella proteins seem to show a slow evolutionary rate and a higher similarity with proteins from Vertebrates compared to proteins from Arthropods or Nematodes. Their composition shows enrichment in positively charged amino acids that might contribute to their thermostability. The gene content of Alvinella reveals that an important pool of genes previously considered to be specific to Deuterostomes were in fact already present in the last common ancestor of the Bilaterian animals, but have been secondarily lost in model invertebrates. This pool is enriched in glycoproteins that play a key role in intercellular communication, hormonal regulation and immunity. Conclusions: Our study starts to unravel the gene content and sequence evolution of a deep-sea annelid, revealing key features in eukaryote adaptation to extreme environmental conditions and highlighting the proximity of Annelids and Vertebrates.

Background: Alvinella pompejana is an annelid worm that inhabits deep-sea hydrothermal vent sites in the Pacific Ocean. Living at a depth of approximately 2500 meters, these worms experience extreme environmental conditions, including high temperature and pressure as well as high levels of sulfide and heavy metals. A. pompejana is one of the most thermotolerant metazoans, making this animal a subject of great interest for studies of eukaryotic thermoadaptation. Results: In order to complement existing EST resources we performed deep sequencing of the A. pompejana transcriptome. We identified several thousand novel protein-coding transcripts, nearly doubling the sequence data for this annelid. We then performed an extensive survey of previously established prokaryotic thermoadaptation measures to search for global signals of thermoadaptation in A. pompejana in comparison with mesophilic eukaryotes. In an orthologous set of 457 proteins, we found that the best indicator of thermoadaptation was the difference in frequency of charged versus polar residues (CvP-bias), which was highest in A. pompejana. CvP-bias robustly distinguished prokaryotic thermophiles from prokaryotic mesophiles, as well as the thermophilic fungus Chaetomium thermophilum from mesophilic eukaryotes. Experimental values for thermophilic proteins supported higher CvP-bias as a measure of thermal stability when compared to their mesophilic orthologs. Proteome-wide mean CvP-bias also correlated with the body temperatures of homeothermic birds and mammals. Conclusions: Our work extends the transcriptome resources for A. pompejana and identifies the CvP-bias as a robust and widely applicable measure of eukaryotic thermoadaptation. Reviewer: This article was reviewed by Sándor Pongor, L. Aravind and Anthony M. Poole.