Biology subjects

Methou, P.

Publications and source records attributed to Methou, P..

10 recordsLinked to original sources

bioRxiv2026

Two new gastropod holobionts from Atlantic hydrothermal vents showing different levels of endosymbiosis dependence

Chemosynthetic symbioses underpin animal life at deep-sea hydrothermal vents, encompassing substantial variabilities in symbiont identity, metabolic capacity, and host dependence. Here, we characterise symbioses in two peltospirid snails from Mid-Atlantic Ridge vents, Peltospira gargantua and P. smaragdina, using 3D anatomical reconstruction, stable isotope analyses, fluorescence in situ hybridization, transmission electron microscopy, and metagenomics. Both species hosted abundant intracellular Campylobacterota within bacteriocytes of a hypertrophied oesophageal gland. Their dominant symbionts belonged to genus Sulfurimonas, but the two hosts were associated with distinct symbiont lineages. Symbiont genomes encoded carbon fixation through the rTCA cycle, sulfide oxidation, and Group I Ni-Fe hydrogenases, indicating combined thiotrophic and hydrogenotrophic capacities. Hydrogenase copy number varied across vent fields from one to three copies. The P. gargantua symbiont from the hydrogen-enriched Hydra vent field carried two divergent copies, including one with a truncated catalytic region, potentially reflecting local adaptation to vent geochemistry. Anatomical and isotopic comparisons further revealed contrasting host dependence, with P. gargantua having a proportionally larger oesophageal gland and ventricle coupled with a reduced radula, as well as a greater nitrogen-isotope enrichment between symbiotic and non-symbiotic tissues. The smaller oesophageal gland and larger feeding apparatus of P. smaragdina point to it being mixotrophic. Previously, all known peltospirid symbioses have partnered with Gammaproteobacteria, and we expand the known diversity of peltospirid symbioses. Our findings underscore how closely related hosts can exhibit different degrees of dependence on symbiosis, and that mixotrophic symbiosis may be prevalent in small vent species previously thought to be non-symbiotic.

ecology↗

bioRxiv2026

Widespread symbiosis of ciliate epibionts colonizing gills of shrimps inhabiting vents and seeps across the Pacific Ocean

Although bacterial symbiosis is well-documented in chemosynthetic-based ecosystems, associations with microeukaryotes remain overlooked. In this study, using scanning electron microscopy and 18S rDNA barcoding, we investigate the presence, diversity, and biogeographic patterns of ciliate epibionts associated with two deep-sea caridean shrimp families: Alvinocarididae, and Thoridae. We identified a widespread lineage of ciliates colonizing the gills of different alvinocaridid species, extending their previously known distribution in freshwater and coastal habitats to deep-sea areas down to 3388 m. These ciliates form a distinct clade related to coastal Chonotrichia, but showing clear genetic divergence from the previously-described species. Geographic divergence of these ciliate populations was observed across the Pacific Ocean, with no evident structure related to their host species. These chonotrichian ciliates exhibited variation occurrence across host species, individuals, and regions, indicating a facultative association with their hosts. In contrast, the thorid shrimps harbored rare and phylogenetically diverse ciliates. More rarely, we found ciliates related to known parasitic lineages hosted by both shrimp families, with signs of immune response - black gills - in some individuals colonized by these ciliates. Our results reveal previously overlooked protist-crustacean associations in chemosynthetic ecosystems and highlight the ecological and biogeographic importance of this group in the deep ocean.

microbiology↗

bioRxiv2026

High gene flow in Atlantic vent shrimp species with multiple ridge colonizations by ecotypic lineages with contrasting symbioses

Conservation concerns regarding potential mineral extraction near deep-sea hydrothermal vents have emphasised the need for a better understanding of the contemporary connectivity of various vent-endemic species, accounting for the specifics of their life-history traits and habitat requirements. Rimicaris shrimps are a major component of vent communities in the Atlantic Ocean, both along the Mid-Atlantic Ridge (MAR) and at the Mid-Cayman Spreading Center (MCSC). Using ddRAD sequencing, we examined the genetic differentiation of three Atlantic Rimicaris species to better understand their past and present migration pathways and the possible demographic history that led to their current distribution and ecology. Rimicaris exoculata and R. chacei inhabit the MAR and exhibit widespread gene flow along the ridge with no areas of restricted connectivity. R. hybisae occurs at the MCSC and exhibits almost no genetic difference with its congeneric from the MAR, R. chacei, despite the geographic distance between them and their contrasting ecologies and morphologies. Demographic inferences support a scenario of a very recent (less than 2000 generations) separation between MCSC and MAR shrimp populations, followed by a rapid expansion in both regions, possibly triggered by symbiotic development. Analyses further suggest recent or ongoing secondary contacts involving two-way migration, which is more pronounced from the MCSC towards the MAR. All together these results suggest that R. chacei and R. hybisae represent distinct forms of the same species, which we hereby synonymise as R. chacei, highlighting their morphological plasticity in relation to symbiosis.

evolutionary biology↗

bioRxiv2025

Evolutionary convergence and trophic diversity in hot vent and cold seep shrimps showcase a continuum of symbiosis

Convergent evolution offers a powerful lens through which to examine the selective forces shaping life in extreme environments. In deep-sea hot vents and cold seeps, invertebrates have independently evolved symbioses with chemosynthetic bacteria, but repeated origins of such associations within a family remain rare. Here, we investigate the evolutionary emergence of chemosymbiosis in the shrimp family Alvinocarididae across 22 species collected globally. Electron microscopy identified a gradient of epibiotic bacterial colonization within the cephalothoracic cavity, ranging from absent to dense filamentous mats, suggesting distinct trophic strategies. Isotope and lipid trophic markers confirmed difference in reliance on chemosynthetic production among sympatric species with different bacterial colonization from a single vent. Phylogenetic analysis reveals at least two independent origins of chemosymbiosis, suggesting evolutionary convergence. Microhabitat association data further show that symbiotic phenotypes are most common in shrimps occupying the hottest, most geofluid-enriched microhabitats, though exceptions suggest contributions from additional ecological or physiological constraints. Our findings reveal many alvinocaridids as gradually evolving towards symbiosis, highlighting the importance of intermediate cases to understand the pathways to chemosymbiosis. This study contributes to a broader understanding of the predictability of evolutionary outcomes in distinct habitats such as vents, with broader implications for resilience of deep-sea ecosystems.

evolutionary biology↗

bioRxiv2024

A tale of two shrimps - Speciation and demography of two sympatric shrimp species from hydrothermal vents

Hydrothermal vents can serve as natural laboratories to study speciation processes due to their fragmented distribution often with geographic barriers between habitats. Two sympatric species of Rimicaris shrimps occur at vents on the Izu-Bonin-Mariana volcanic arc: Rimicaris loihi also occurs near Hawaii and R. cambonae is present on the Tonga Arc. These two species biogeographically co-occur and are genetically similar, raising questions about their speciation mechanism, how they maintain distinct species, and whether interbreeding occurs. Here, we use barcoding and shotgun sequencing to test their genetic isolation and investigate their speciation process. We also evaluate population demography over 10 years to assess population densities and sex ratios at vents. Our results support R. cambonae and R. loihi as two distinct species despite sympatry throughout part of their range. We also observed regional-scale genetic structure among R. loihi populations from the Izu-Bonin-Mariana volcanic arc despite their broad geographic distribution. Finally, we found concomitant variations of shrimp densities and genetic diversity following fluctuations in geological and venting activities over a decade. A combination of geological instability, ocean currents dynamics and sea-level changes might drive temporary isolation among these local populations. We suggest similar factors, with longer isolation periods, may also have promoted speciation between the two Rimicaris species whereas distinct life-history traits could strengthen and maintain reproductive barriers. Overall, our results indicate different connectivity patterns on a volcanic arc that contrast with those observed previously at vents from mid-ocean ridges or back-arc basins systems.

evolutionary biology↗

bioRxiv2023

Juvenile niches select between two distinct development trajectories and symbiosis modes in vent shrimps

Most animal species have a singular developmental pathway and adult ecology, but developmental plasticity is well-known in some like honeybees where castes display profoundly different morphology and ecology. An intriguing case is the Atlantic deep-sea hydrothermal vent shrimp Rimicaris hybisae/chacei that share dominant COI haplotypes but develops into either the symbiont-reliant hybisae with a hypertrophied head chamber (in the Mid-Cayman Spreading Centre) or the mixotrophic chacei with a narrow head chamber (on the Mid-Atlantic Ridge). Here, we use X-ray micro-computed tomography and fluorescent in situ hybridization to show that key anatomical shifts in both occur between the juvenile-subadult transition, when those developing into hybisae have fully established symbiosis but not chacei. On the Mid-Atlantic Ridge the diet of R. chacei has been hypothetically linked to competition with the obligatorily symbiotic congener R. exoculata, and we find anatomical evidences that R. exoculata is indeed better adapted for symbiosis - suggesting the chacei morph could be an adaptation to prevent competitive exclusion. Our results suggest that the two distinct development trajectories are likely selected according to the diet available to the juveniles, determined by whether energetically sufficient symbiont colonisation has occurred before reaching subadult stage.

evolutionary biology↗

bioRxiv2023

The Role of Reproductive Periodicity in Dispersal Among Hydrothermal Vents and its Implications for Regional Connectivity and Conservation

Connectivity among isolated habitat patches via planktonic larval dispersal is crucial for maintaining the regional diversity of hydrothermal vents. Despite, increasing sophistication of techniques for simulating dispersal, limited information on biological and behavioural traits of vent-associated species has unknown affects on the applicability of these methods for conservation. Here we focus on the role of periodic reproduction on dispersal among hydrothermal vents, as periodic spawning has increasingly been observed in a variety of taxa. For generalizeability, we simulate the dispersal of larvae under treatments of periodic and aperiodic release timing at various depths, with a consistant but variable planktonic larval duration. Our results show a highly variable effect of periodicity on the characteristics and distribution of dispersal, which are heavily modified by the dispersal depth and source location. The capacity for reproductive periodicity to impact the among-site dispersal warrents further investigation into its prevelance and timing among vent-associated fauna.

biophysics↗

bioRxiv2023

Symbioses of alvinocaridid shrimps from the South West Pacific: No chemosymbiotic diets but partially conserved gut microbiomes

Rimicaris exoculata shrimps from hydrothermal vent ecosystems are known to host dense epibiotic communities inside their enlarged heads and digestive systems. Conversely, other shrimps from the family, described as opportunistic feeders have received less attention. We examined the nutrition and bacterial communities colonizing "head" chambers and digestive systems of three other alvinocaridids - Rimicaris variabilis, Nautilocaris saintlaurentae and Manuscaris sp. - using a combination of electron microscopy, stable isotopes and sequencing approaches. Our observations inside "head" cavities and on mouthparts showed only a really low coverage of bacterial epibionts. In addition, no clear correlation between isotopic ratios and relative abundance of epibionts on mouthparts could be established among shrimp individuals. Altogether, these results suggest that none of these alvinocaridids rely on chemosynthetic epibionts as their main source of nutrition. Our analyses also revealed a substantial presence of several Firmicutes within the foreguts and midguts of these shrimps, which closest known lineages were systematically digestive epibionts associated with alvinocaridids, and more broadly from digestive systems of other crustaceans from marine and terrestrial ecosystems. Overall, our study opens new perspectives not only about chemosynthetic symbioses of vent shrimps, but more largely about digestive microbiomes with potential ancient and evolutionarily conserved bacterial partnerships among crustaceans.

evolutionary biology↗

bioRxiv2021

Reproductive strategies in vent shrimps shaped by feeding ecology with intriguing seasonality unlinked to surface productivity

Variations in offspring production according to feeding strategies or food supply have been recognized in many animals from various ecosystems. Despite an unusual trophic structure based on non-photosynthetic primary production, these relationships remain largely under-studied in chemosynthetic ecosystems. Here, we use Rimicaris shrimps from deep-sea hydrothermal vents as a study case to explore relations between reproduction, diets and food supply in these environments. For that, we compared reproductive outputs of three congeneric shrimps differing by their diets. They inhabit vents located under oligotrophic waters of tropical gyres with opposed latitudes, allowing us to also examine the prevalence of phylogenetic vs environmental drivers in their reproductive rhythms. For this we used both our original data and a compilation of published observations on the presence of ovigerous females covering various seasons over the past 35 years. We report distinct egg production trends between Rimicaris species relying solely on chemosymbiosis - R. exoculata and R. kairei - and those relying on mixotrophy - R. chacei - where R. chacei produces broods with higher numbers of smaller eggs. Besides, our data and historical records suggest a reproductive period with substantial proportions of brooding females mostly between January and early April for all examined species whatever the region. Intriguingly, this periodicity does not correspond to seasonal variations in surface production with presence of brooding females during either boreal winter or austral summer. These observations contrast with the long-standing paradigm in deep-sea species for which periodic reproductive patterns have always been attributed to seasonal variations of photosynthetic production sinking from surface. Our results suggest the presence of intrinsic basis for biological rhythms in the deep sea, and bring to light the importance of having year-round observations in order to understand life history of vent animals.

ecology↗

bioRxiv2021

Population structure and environmental niches of Rimicaris shrimps from the Mid Atlantic Ridge

Among the endemic and specialized fauna from hydrothermal vents, Rimicaris shrimp surely constitutes one of the most important and emblematic components of these ecosystems. In the Mid Atlantic Ridge, two species affiliated to this genus co-occur: Rimicaris exoculata and Rimicaris chacei that differ by their morphology, their trophic regime as well as by their abundance. The first forms large and dense aggregations on active vent chimney walls in close proximity to vent fluid emissions, whereas the second is recognized as much less conspicuous, living mostly in scattered groups or solitary further away from the fluids. However, the recent revision of Rimicaris juvenile stages from the Mid Atlantic Ridge shows that R. chacei abundance would be higher than expected at these early life stages. Here, we describe and compare the population structures of R. exoculata and R. chacei at the Snake Pit and TAG vent fields. We show distinct population demographics between the two co-occurring shrimps with a large post settlement collapse in R. chacei population suggesting a large juvenile mortality for this species. We also observe important spatial segregation patterns between the two species and their different life stages. Additionally, our results highlight distinct niches for the earliest juvenile stages of both R. exoculata and R. chacei, compared to all the other life stages. Finally, we discuss the potential factors - predation and competitive interactions among others - that could explain the differences we observe in the population structure of these two species.

ecology↗