Contrasted phylogeographic patterns of hydrothermal vent gastropods along South West Pacific: Woodlark Basin, a possible contact zone and/or stepping-stone.

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.

Origin, diversity, and biogeography of Antarctic scale worms (Polychaeta: Polynoidae): a wide-scale barcoding approach.

The Antarctic marine environment hosts diversified and highly endemic benthos owing to its unique geologic and climatic history. Current warming trends have increased the urgency of understanding Antarctic species history to predict how environmental changes will impact ecosystem functioning. Antarctic benthic lineages have traditionally been examined under three hypotheses: (1) high endemism and local radiation, (2) emergence of deep-sea taxa through thermohaline circulation, and (3) species migrations across the Polar Front. In this study, we investigated which hypotheses best describe benthic invertebrate origins by examining Antarctic scale worms (Polynoidae). We amassed 691 polynoid sequences from the Southern Ocean and neighboring areas: the Kerguelen and Tierra del Fuego (South America) archipelagos, the Indian Ocean, and waters around New Zealand. We performed phylogenetic reconstructions to identify lineages across geographic regions, aided by mitochondrial markers cytochrome c oxidase subunit I (Cox1) and 16S ribosomal RNA (16S). Additionally, we produced haplotype networks at the species scale to examine genetic diversity, biogeographic separations, and past demography. The Cox1 dataset provided the most illuminating insights into the evolution of polynoids, with a total of 36 lineages identified. Eunoe sp. was present at Tierra del Fuego and Kerguelen, in favor of the latter acting as a migration crossroads. Harmothoe fuligineum, widespread around the Antarctic continent, was also present but isolated at Kerguelen, possibly resulting from historical freeze-thaw cycles. The genus Polyeunoa appears to have diversified prior to colonizing the continent, leading to the co-occurrence of at least three cryptic species around the Southern and Indian Oceans. Analyses identified that nearly all populations are presently expanding following a bottleneck event, possibly caused by habitat reduction from the last glacial episodes. Findings support multiple origins for contemporary Antarctic polynoids, and some species investigated here provide information on ancestral scenarios of (re)colonization. First, it is apparent that species collected from the Antarctic continent are endemic, as the absence of closely related species in the Kerguelen and Tierra del Fuego datasets for most lineages argues in favor of Hypothesis 1 of local origin. Next, Eunoe sp. and H. fuligineum, however, support the possibility of Kerguelen and other sub-Antarctic islands acting as a crossroads for larvae of some species, in support of Hypothesis 3. Finally, the genus Polyeunoa, conversely, is found at depths greater than 150 m and may have a deep origin, in line with Hypothesis 2. These "non endemic" groups, nevertheless, have a distribution that is either north or south of the Antarctic Polar Front, indicating that there is still a barrier to dispersal, even in the deep sea.

Balanced Polymorphism at the Pgm-1 Locus of the Pompeii Worm Alvinella pompejana and Its Variant Adaptability Is Only Governed by Two QE Mutations at Linked Sites.

The polychaete Alvinella pompejana lives exclusively on the walls of deep-sea hydrothermal chimneys along the East Pacific Rise (EPR), and displays specific adaptations to withstand the high temperatures and hypoxia associated with this highly variable habitat. Previous studies have revealed the existence of a balanced polymorphism on the enzyme phosphoglucomutase associated with thermal variations, where allozymes 90 and 100 exhibit different optimal activities and thermostabilities. Exploration of the mutational landscape of phosphoglucomutase 1 revealed the maintenance of four highly divergent allelic lineages encoding the three most frequent electromorphs over the geographic range of A. pompejana. This polymorphism is only governed by two linked amino acid replacements, located in exon 3 (E155Q and E190Q). A two-niche model of selection, including 'cold' and 'hot' conditions, represents the most likely scenario for the long-term persistence of these isoforms. Using directed mutagenesis and the expression of the three recombinant variants allowed us to test the additive effect of these two mutations on the biochemical properties of this enzyme. Our results are coherent with those previously obtained from native proteins, and reveal a thermodynamic trade-off between protein thermostability and catalysis, which is likely to have maintained these functional phenotypes prior to the geographic separation of populations across the Equator about 1.2 million years ago.

Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps.

We provide the first detailed identification of Barents Sea cold seep frenulate hosts and their symbionts. Mitochondrial COI sequence analysis, in combination with detailed morphological investigations through both light and electron microscopy was used for identifying frenulate hosts, and comparing them to Oligobrachia haakonmosbiensis and Oligobrachia webbi, two morphologically similar species known from the Norwegian Sea. Specimens from sites previously assumed to host O. haakonmosbiensis were included in our molecular analysis, which allowed us to provide new insight on the debate regarding species identity of these Oligobrachia worms. Our results indicate that high Arctic seeps are inhabited by a species that though closely related to Oligobrachia haakonmosbiensis, is nonetheless distinct. We refer to this group as the Oligobrachia sp. CPL-clade, based on the colloquial names of the sites they are currently known to inhabit. Since members of the Oligobrachia sp. CPL-clade cannot be distinguished from O. haakonmosbiensis or O. webbi based on morphology, we suggest that a complex of cryptic Oligobrachia species inhabit seeps in the Norwegian Sea and the Arctic. The symbionts of the Oligobrachia sp. CPL-clade were also found to be closely related to O. haakonmosbiensis symbionts, but genetically distinct. Fluorescent in situ hybridization and transmission electron micrographs revealed extremely dense populations of bacteria within the trophosome of members of the Oligobrachia sp. CPL-clade, which is unusual for frenulates. Bacterial genes for sulfur oxidation were detected and small rod shaped bacteria (round in cross section), typical of siboglinid-associated sulfur-oxidizing bacteria, were seen on electron micrographs of trophosome bacteriocytes, suggesting that sulfide constitutes the main energy source. We hypothesize that specific, local geochemical conditions, in particular, high sulfide fluxes and concentrations could account for the unusually high symbiont densities in members of the Oligrobrachia sp. CPL-clade.

The benefit of docosahexanoic acid on the migration of vascular smooth muscle cells is partially dependent on Notch regulation of MMP-2/-9.

The Notch pathway is involved in the regulation of the migratory/proliferative phenotype acquired by vascular smooth muscle cells (VSMCs) in the pro-inflammatory context of vascular diseases. Here, we investigated whether docosahexaenoic acid (DHA), a polyunsaturated, omega-3 fatty acid, could reduce fibrinolytic/matrix-metalloproteinase (MMP) activity and whether this reduction occurs through the modulation of Notch signaling. Rat VSMCs were transdifferentiated with interleukin-1beta and then treated with DHA. Migration/proliferation was determined by performing a wound healing assay and measuring MMP-2/-9 activity, type 1 plasminogen activator inhibitor levels, and the expression of these proteins. The involvement of Notch in regulating the fibrinolytic/MMP system was evidenced using Notch pathway inhibitors and the forced expression of Notch1 and Notch3 intracellular domains. DHA significantly decreased VSMC migration/proliferation induced by interleukin-1beta as well as fibrinolytic/MMP activity. Prevention of Notch1 target gene transcription enhanced the interleukin-1beta effects on MMPs and on migration, whereas Notch3 intracellular domain overexpression reduced these effects. Finally, DHA increased Notch3 expression, Hes-1 transcription (a Notch target gene), and enhanced gamma-secretase complex activity. These results suggest that inhibition of the Notch pathway participates in the transition of VSMCs toward a migratory phenotype. These results also suggest that the beneficial inhibitory effects of DHA on fibrinolytic/MMP activity are related in part to the effects of DHA on the expression of Notch pathway components, providing new insight into the mechanisms by which omega-3 fatty acids prevent cardiovascular diseases.