Do Hydrothermal Shrimp Smell Vents?

Deep-sea species endemic to hydrothermal vents face the critical challenge of detecting active sites in a vast environment devoid of sunlight. This certainly requires specific sensory abilities, among which olfaction could be a relevant sensory modality, since chemical compounds in hydrothermal fluids or food odors could potentially serve as orientation cues. The temperature of the vent fluid might also be used for locating vent sites. The objective of this study is to observe the following key behaviors of olfaction in hydrothermal shrimp, which could provide an insight into their olfactory capacities: (1) grooming behavior; (2) attraction to environmental cues (food odors and fluid markers). We designed experiments at both deep-sea and atmospheric pressure to assess the behavior of the vent shrimp Rimicaris exoculata and Mirocaris fortunata, as well as of the coastal species Palaemon elegans and Palaemon serratus for comparison. Here, we show that hydrothermal shrimp groom their sensory appendages similarly to other crustaceans, but this does not clean the dense bacterial biofilm that covers the olfactory structures. These shrimp have previously been shown to possess functional sensory structures, and to detect the environmental olfactory signals tested, but we do not observe significant attraction behavior here. Only temperature, as a signature of vent fluids, clearly attracts vent shrimp and thus is confirmed to be a relevant signal for orientation in their environment.

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 component 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 show 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 widely 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.

Population structure and reproduction of the alvinocaridid shrimp Rimicaris exoculata on the Mid-Atlantic Ridge: variations between habitats and vent fields

Rimicaris exoculata is a dominant species of deep Mid-Atlantic Ridge (MAR) vent fields and inhabits areas close to vent emissions at depths below 2000 m. Its high abundance and strong genetic connectivity along the MAR point at a remarkable ability to produce dispersing larval stages. However, the reproduction of this species long remained enigmatic because brooding females were rarely observed. Here, we describe the population structure and reproduction of R. exoculata at the Snake Pit and TAG vent fields (3600m depth) for the months of January-February. We observed major differences in population structure between habitats within a single vent field: females widely dominate the large swarms near active venting while inactive peripheries are inhabited by large males. Low temperature diffusion zones are mainly colonized by small juveniles of R. chacei instead of R. exoculata. Size structure of populations from dense active areas is polymodal at both fields, suggesting discontinuous recruitment. Male and female sizes did not vary across habitats and vent fields, with sexually mature female being slightly larger than males. In contrast to previous studies, hundreds of ovigerous females were observed at both vent fields, suggesting seasonal reproduction. Proportion of ovigerous females among sexually mature females were similar between vent fields (36.7 %). However, reproductive output was lower at TAG, where ovigerous females had smaller size-specific fecundity and egg size, and more aborted broods. Broods were colonized by the dirivultid copepod Stygiopontius pectinatus at both vent fields, apparently without deleterious effect on egg development. In the light of the observed variability in R. exoculata population structure, we propose a hypothetical scenario depicting its mating system and brooding behavior, and discuss more generally intraspecific interactions during its benthic life stages.

Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria

Background Free-living and symbiotic chemosynthetic microbial communities support primary production and higher trophic levels in deep-sea hydrothermal vents. The shrimp Rimicaris exoculata, which dominates animal communities along the Mid-Atlantic Ridge, houses a complex bacterial community in its enlarged cephalothorax. The dominant bacteria present are from the taxonomic groups Campylobacteria, Desulfobulbia (formerly Deltaproteobacteria), Alphaproteobacteria, Gammaproteobacteria, and some recently discovered iron oxyhydroxide-coated Zetaproteobacteria. This epibiotic consortium uses iron, sulfide, methane, and hydrogen as energy sources. Here, we generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic communities to reconstruct and investigate symbiotic genomes. We collected specimens from three geochemically contrasted vent fields, TAG, Rainbow, and Snake Pit, to unravel the specificity, variability, and adaptation of Rimicaris–microbe associations. Results Our data enabled us to reconstruct 49 metagenome-assembled genomes (MAGs) from the TAG and Rainbow vent fields, including 16 with more than 90% completion and less than 5% contamination based on single copy core genes. These MAGs belonged to the dominant Campylobacteria, Desulfobulbia, Thiotrichaceae, and some novel candidate phyla radiation (CPR) lineages. In addition, most importantly, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (average nucleotide identity ANI < 77% with the closest relative Ghiorsea bivora isolated from TAG, and 88% with each other), suggesting potential novel species. Genes for Calvin-Benson Bassham (CBB) carbon fixation, iron, and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts co-existing in a single shrimp at both the basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further examination of the seeming functional redundancy among these epibionts revealed important differences. Conclusion These data highlight microniche partitioning in the Rimicaris holobiont and support recent studies showing that functional diversity enables multiple symbiont strains to coexist in animals colonizing hydrothermal vents.

Niche Partitioning in the Rimicaris Exoculata Holobiont: The Case of the First Symbiotic Zetaproteobacteria

Background Mutualistic symbioses between invertebrate animals and chemosynthetic bacteria are the basis of life in hydrothermal vent ecosystems. The shrimp Rimicaris exoculata , which dominates animal communities along the Mid-Atlantic Ridge, houses a complex bacterial community in its enlarged cephalothorax, including the dominant Campylobacteria , Desulfobulbia (formerly Deltaproteobacteria ), Alpha proteobacteria , Gammaproteobacteria and some recently discovered iron oxyhydroxide-coated Zetaproteobacteria . This epibiotic consortium uses iron, sulfide, methane, and hydrogen as energy sources. Here, we generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic communities to reconstruct and investigate symbiotic genomes. We collected specimens in three geochemically contrasted vent fields, TAG, Rainbow, and Snake Pit, to unravel the specificity, variability, and adaptation of Rimicaris –microbe associations. Results Our data enabled us to reconstruct 49 metagenome-assembled genomes (MAGs) from the TAG and Rainbow vent fields, including 16 with more than 90% completion and less than 5% contamination based on single copy core genes. These MAGs belonged to the dominant Campylobacteria , Desulfobulbia , Thiotrichaceae as well as some novel candidate phyla radiation (CPR) lineages. In addition, most importantly, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (average nucleotide identity ANI < 77% with the closest relative Ghiorsea bivora isolated from TAG, and 88% with each other), suggesting potential novel species. Genes for Calvin-Benson Bassham (CBB) carbon fixation, iron, and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts co-existing in a single shrimp at both the basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further examination of the seeming functional redundancy among these epibionts revealed important differences. Conclusion These data highlight microniche partitioning in the Rimicaris holobiont and support recent studies showing that functional diversity enables multiple symbiont strains to coexist in animals colonizing hydrothermal vents.

Rimicaris exoculata: biology and ecology of a shrimp from deep-sea hydrothermal vents associated with ectosymbiotic bacteria

Rimicaris exoculata, the ‘blind shrimp,’ is the most abundant species living on active hydrothermal edifices at deep-sea vents of the Mid-Atlantic Ridge. Its unusually enlarged branchial chamber houses a dense ectosymbiotic community of chemoautotrophic bacteria. Long debated, shrimp nutrition has been proven to be a kind of osmotrophy, whereby small organic molecules produced by the symbionts pass through the integument of the shrimp directly into the circulatory system, rather than through the digestive system. The broad phylogenetic and metabolic diversity of this epibiotic community suggests a highly flexible and adjustable microbial consortium, adapted to the chemically contrasting environments inhabited by the shrimp. To cope with the highly fluctuating oxygen and temperature conditions of its habitat, R. exoculata possesses hemocyanin with a strong oxygen affinity, and has developed both molecular and behavioral responses to heat stresses. If R. exoculata is able to detect very dim light or chemical compounds emitted by vents, the relatively small visual and olfactory areas in the brain, along with the disproportionately enlarged higher centers, argue for a significant involvement of navigational skills using learning and place memory to orient itself within its aphotic environment. This shrimp undergoes unconventional larval development, with a primary lecithotrophic stage followed by an extended planktotrophic period, allowing a huge potential for dispersion. In light of mining licenses posing a threat for deep-sea environments, this species is a model still to be studied to better understand life in extreme deep-sea ecosystems at the global scale of an ocean.

Integrative taxonomy revisits the ontogeny and trophic niches of Rimicaris vent shrimps

Among hydrothermal vent species, Rimicaris exoculata is one of the most emblematic, hosting abundant and diverse ectosymbioses that provide most of its nutrition. Rimicaris exoculata co-occurs in dense aggregates with the much less abundant Rimicaris chacei in many Mid-Atlantic Ridge vent fields. This second shrimp also houses ectosymbiotic microorganisms but has a mixotrophic diet. Recent observations have suggested potential misidentifications between these species at their juvenile stages, which could have led to misinterpretations of their early-life ecology. Here, we confirm erroneous identification of the earliest stages and propose a new set of morphological characters unambiguously identifying juveniles of each species. On the basis of this reassessment, combined use of C, N and S stable isotope ratios reveals distinct ontogenic trophic niche shifts in both species, from photosynthesis-based nutrition before settlement, towards a chemosynthetic diet afterwards. Furthermore, isotopic compositions in the earliest juvenile stages suggest differences in larval histories. Each species thus exhibits specific early-life strategies that would, without our re-examination, have been interpreted as ontogenetic variations. Overall, our results provide a good illustration of the identification issues persisting in deep-sea ecosystems and the importance of integrative taxonomy in providing an accurate view of fundamental aspects of the biology and ecology of species inhabiting these environments.

Niche Partitioning in the Rimicaris Exoculata Holobiont: The Case of the First Symbiotic Zetaproteobacteria

BackgroundMutualistic symbioses between invertebrate animals and chemosynthetic bacteria are at the basis of Life in hydrothermal vent ecosystems. The shrimp Rimicaris exoculata, which dominates animal fauna along the Mid Atlantic Ridge, houses in its cephalothorax a complex bacterial community including Campylobacteria, Gamma- Delta- and some recently discovered iron oxyhydroxides-coated Zetaproteobacteria. This epibiotic consortium uses iron, sulfide, methane and hydrogen as energy sources. Here, we used a DNA extraction procedure adapted to recalcitrant embedded bacteria and generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic community. We aimed reconstructing symbiotic genomes from specimen collected in three geochemically contrasted vent fields, TAG, Rainbow and Snake Pit to unravel the specificity, variability and adaptation of host-microbes associations.ResultsUsing these data we were able to reconstruct 49 high quality metagenome-assembled genomes (MAGs) from TAG and Rainbow vents fields. Most critically, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (ANI < 77% from the closest relative Ghiorsea bivora isolated from TAG and <88% between each other), suggesting potential novel species. Genes for CBB carbon fixation, iron and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and quorum sensing as well as multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts that co-exist in a single shrimp at both basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further insights into the seemingly functional redundancy between those epibionts revealed important differences. ConclusionThese data highlight microniche partitioning in the Rimicaris holobiont and confirm recent works that show functional diversity enables multiple symbiont strains to coexist in animals from hydrothermal vents.