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Most animal species have a singular developmental pathway and adult ecology, but developmental plasticity is well-known in some such as honeybees where castes display profoundly different morphology and ecology. An intriguing case is the Atlantic deep-sea hydrothermal vent shrimp pair Rimicaris hybisae and R. chacei that share dominant COI haplotypes and could represent very recently diverging lineages or even morphs of the same species. Rimicaris hybisae is symbiont-reliant with a hypertrophied head chamber (in the Mid-Cayman Spreading Centre), while R. chacei is mixotrophic with a narrow head chamber (on the Mid-Atlantic Ridge). Here, we use X-ray micro-computed tomography and fluorescence in situ hybridization to show that key anatomical shifts in both occur during the juvenile-subadult transition, when R. hybisae has fully established symbiosis but not R. 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 evidence that R. exoculata is indeed better adapted for symbiosis. We speculate the possibility that the distinct development trajectories in R. hybisae and R. chacei may be determined by symbiont colonization at a "critical period" before subadulthood, though further genetic studies are warranted to test this hypothesis along with the true relationship between R. hybisae and R. chacei.
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Decápodos , Respiraderos Hidrotermales , Animales , Abejas/genética , Simbiosis , Hibridación Fluorescente in Situ , Microtomografía por Rayos X , Decápodos/genética , Decápodos/anatomía & histologíaRESUMEN
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 colonising '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 and Deferribacterota lineages within the foreguts and midguts of these shrimps, which closest known lineages were systematically digestive symbionts associated with alvinocaridids, and more broadly for Firmicutes 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.
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Decápodos , Microbioma Gastrointestinal , Respiraderos Hidrotermales , Microbiota , Humanos , Animales , Filogenia , Decápodos/microbiología , Dieta , Respiraderos Hidrotermales/microbiologíaRESUMEN
BACKGROUND: In deep-sea hydrothermal vent areas, deprived of light, most animals rely on chemosynthetic symbionts for their nutrition. These symbionts may be located on their cuticle, inside modified organs, or in specialized cells. Nonetheless, many of these animals have an open and functional digestive tract. The vent shrimp Rimicaris exoculata is fueled mainly by its gill chamber symbionts, but also has a complete digestive system with symbionts. These are found in the shrimp foregut and midgut, but their roles remain unknown. We used genome-resolved metagenomics on separate foregut and midgut samples, taken from specimens living at three contrasted sites along the Mid-Atlantic Ridge (TAG, Rainbow, and Snake Pit) to reveal their genetic potential. RESULTS: We reconstructed and studied 20 Metagenome-Assembled Genomes (MAGs), including novel lineages of Hepatoplasmataceae and Deferribacteres, abundant in the shrimp foregut and midgut, respectively. Although the former showed streamlined reduced genomes capable of using mostly broken-down complex molecules, Deferribacteres showed the ability to degrade complex polymers, synthesize vitamins, and encode numerous flagellar and chemotaxis genes for host-symbiont sensing. Both symbionts harbor a diverse set of immune system genes favoring holobiont defense. In addition, Deferribacteres were observed to particularly colonize the bacteria-free ectoperitrophic space, in direct contact with the host, elongating but not dividing despite possessing the complete genetic machinery necessary for this. CONCLUSION: Overall, these data suggest that these digestive symbionts have key communication and defense roles, which contribute to the overall fitness of the Rimicaris holobiont. Video Abstract.
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Decápodos , Respiraderos Hidrotermales , Animales , Simbiosis , Decápodos/genética , Branquias , Sistema InmunológicoRESUMEN
The herbicide glyphosate has been widely used in the past 40 years, under the assumption that side effects were minimal. In recent years, its impact on microbial compositions and potential indirect effects on plant, animal and human health have been strongly suspected. Glyphosate and co-formulates have been detected in various water sources, but our understanding of their potential effects on aquatic animals is still in its infancy compared with mammals. In this study, we investigated the effect of chronic exposure to an environmentally relevant concentration of glyphosate on bacterial communities of rainbow trout (Oncorhynchus mykiss). Gills, gut contents and gut epithelia were then analyzed by metabarcoding targeting the 16S rRNA gene. Our results revealed that rainbow trout has its own bacterial communities that differ from their surrounding habitats and possess microbiomes specific to these three compartments. The glyphosate-based herbicide treatment significantly affected the gill microbiome, with a decrease in diversity. Glyphosate treatments disrupted microbial taxonomic composition and some bacteria seem to be sensitive to this environmental pollutant. Lastly, co-occurrence networks showed that microbial interactions in gills tended to decrease with chemical exposure. These results demonstrate that glyphosate could affect microbiota associated with aquaculture fish.
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Microbioma Gastrointestinal , Herbicidas , Microbiota , Oncorhynchus mykiss , Animales , Bacterias/genética , Branquias/microbiología , Glicina/análogos & derivados , Herbicidas/toxicidad , Humanos , Mamíferos/genética , Oncorhynchus mykiss/microbiología , ARN Ribosómico 16S/genética , GlifosatoRESUMEN
Remote deep-ocean sediment (DOS) ecosystems are among the least explored biomes on Earth. Genomic assessments of their biodiversity have failed to separate indigenous benthic organisms from sinking plankton. Here, we compare global-scale eukaryotic DNA metabarcoding datasets (18S-V9) from abyssal and lower bathyal surficial sediments and euphotic and aphotic ocean pelagic layers to distinguish plankton from benthic diversity in sediment material. Based on 1685 samples collected throughout the world ocean, we show that DOS diversity is at least threefold that in pelagic realms, with nearly two-thirds represented by abundant yet unknown eukaryotes. These benthic communities are spatially structured by ocean basins and particulate organic carbon (POC) flux from the upper ocean. Plankton DNA reaching the DOS originates from abundant species, with maximal deposition at high latitudes. Its seafloor DNA signature predicts variations in POC export from the surface and reveals previously overlooked taxa that may drive the biological carbon pump.
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Hyperthermophilic archaea of the genus Archaeoglobus are the subject of many fundamental and biotechnological researches. Despite their significance, the class Archaeoglobi is currently represented by only eight species obtained as axenic cultures and taxonomically characterized. Here, we report the isolation and characterization of a new species of Archaeoglobus from a deep-sea hydrothermal vent (Mid-Atlantic Ridge, TAG) for which the name Archaeoglobus neptunius sp. nov. is proposed. The type strain is SE56T (=DSM 110954T = VKM B-3474T). The cells of the novel isolate are motile irregular cocci growing at 50-85°C, pH 5.5-7.5, and NaCl concentrations of 1.5-4.5% (w/v). Strain SE56T grows lithoautotrophically with H2 as an electron donor, sulfite or thiosulfate as an electron acceptor, and CO2/HCO3 - as a carbon source. It is also capable of chemoorganotrophic growth by reduction of sulfate, sulfite, or thiosulfate. The genome of the new isolate consists of a 2,115,826 bp chromosome with an overall G + C content of 46.0 mol%. The whole-genome annotation confirms the key metabolic features of the novel isolate demonstrated experimentally. Genome contains a complete set of genes involved in CO2 fixation via reductive acetyl-CoA pathway, gluconeogenesis, hydrogen and fatty acids oxidation, sulfate reduction, and flagellar motility. The phylogenomic reconstruction based on 122 conserved single-copy archaeal proteins supported by average nucleotide identity (ANI), average amino acid identity (AAI), and alignment fraction (AF) values, indicates a polyphyletic origin of the species currently included into the genus Archaeoglobus, warranting its reclassification.
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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. Video Abstract.
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Decápodos , Respiraderos Hidrotermales , Animales , Filogenia , Proteobacteria , ARN Ribosómico 16S/genética , SimbiosisRESUMEN
Despite representing one of the largest biomes on earth, biodiversity of the deep seafloor is still poorly known. Environmental DNA metabarcoding offers prospects for fast inventories and surveys, yet requires standardized sampling approaches and careful choice of environmental substrate. Here, we aimed to optimize the genetic assessment of prokaryote (16S), protistan (18S V4), and metazoan (18S V1-V2, COI) communities, by evaluating sampling strategies for sediment and aboveground water, deployed simultaneously at one deep-sea site. For sediment, while size-class sorting through sieving had no significant effect on total detected alpha diversity and resolved similar taxonomic compositions at the phylum level for all markers studied, it effectively increased the detection of meiofauna phyla. For water, large volumes obtained from an in situ pump (~ 6000 L) detected significantly more metazoan diversity than 7.5 L collected in sampling boxes. However, the pump being limited by larger mesh sizes (> 20 µm), only captured a fraction of microbial diversity, while sampling boxes allowed access to the pico- and nanoplankton. More importantly, communities characterized by aboveground water samples significantly differed from those characterized by sediment, whatever volume used, and both sample types only shared between 3 and 8% of molecular units. Together, these results underline that sediment sieving may be recommended when targeting metazoans, and aboveground water does not represent an alternative to sediment sampling for inventories of benthic diversity.
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Biodiversidad , Biomarcadores/análisis , ADN Ambiental/análisis , Monitoreo del Ambiente/métodos , Sedimentos Geológicos/análisis , Animales , Mar MediterráneoRESUMEN
Shallow-water hydrothermal vents are widespread, especially in the Mediterranean Sea, owing to the active volcanism of the area. Apart free microbial communities' investigations, few biological studies have been leaded yet. Investigations of microbial communities associated with Nematoda, an ecologically important group in sediments, can help to improve our overall understanding of these ecosystems. We used a multidisciplinary-approach, based on microscopic observations (scanning electron microscopy: SEM and Fluorescence In Situ Hybridization: FISH) coupled with a molecular diversity analysis using metabarcoding, based on the 16S rRNA gene (V3-V4 region), to characterize the bacterial community of a free-living marine nematode and its environment, the shallow hydrothermal vent near Naples (Italy). Observations of living bacteria in the intestine (FISH), molecular and phylogenetic analyses showed that this species of nematode harbors its own bacterial community, distinct from the surrounding sediment and water. Metabarcoding results revealed the specific microbiomes of the sediment from three sites of this hydrothermal area to be composed mainly of sulfur oxidizing and reducing related bacteria.
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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.
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The symbiotic shrimp Rimicaris exoculata dominates the macrofauna inhabiting the active smokers of the deep-sea mid Atlantic ridge vent fields. We investigated the nature of the host mechanisms controlling the vital and highly specialized ectosymbiotic community confined into its cephalothoracic cavity. R. exoculata belongs to the Pleocyemata, crustacean brooding eggs, usually producing Type I crustins. Unexpectedly, a novel anti-Gram-positive type II crustin was molecularly identified in R. exoculata. Re-crustin is mainly produced by the appendages and the inner surfaces of the cephalothoracic cavity, embedding target epibionts. Symbiosis acquisition and regulating mechanisms are still poorly understood. Yet, symbiotic communities were identified at different steps of the life cycle such as brooding stage, juvenile recruitment and molt cycle, all of which may be crucial for symbiotic acquisition and control. Here, we show a spatio-temporal correlation between the production of Re-crustin and the main ectosymbiosis-related life-cycle events. Overall, our results highlight (i) a novel and unusual AMP sequence from an extremophile organism and (ii) the potential role of AMPs in the establishment of vital ectosymbiosis along the life cycle of deep-sea invertebrates.
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Anostraca/fisiología , Péptidos Catiónicos Antimicrobianos/metabolismo , Péptidos Catiónicos Antimicrobianos/farmacocinética , Proteínas de Artrópodos/metabolismo , Bacterias Grampositivas/fisiología , Infecciones por Bacterias Grampositivas/inmunología , Proteínas Citotóxicas Formadoras de Poros/metabolismo , Animales , Péptidos Catiónicos Antimicrobianos/genética , Ecosistema , Interacciones Huésped-Patógeno , Estadios del Ciclo de Vida , Océanos y Mares , Proteínas Citotóxicas Formadoras de Poros/genética , SimbiosisRESUMEN
The chemosymbiotic gastropod Alviniconcha (Provannidae), first described in 1988, is one of the most emblematic hydrothermal-vent taxa described from the Central Indian Ridge and the Southwest (SW) Pacific. Symbiotic bacteria found in the gill of Alviniconcha are thought to be their principal source of nutrition. In the SW Pacific, species distributions for A. kojimai, A. boucheti - and to a lesser extent A. strummeri - overlap. While Alviniconcha species do not appear to truly co-exist in these highly energetic but spatially limited habitats, certain species regularly co-occur within a single vent field and in rare instances, the same edifice. Past research suggests that SW-Pacific Alviniconcha species might aggregate around fluids with distinct geothermal profiles. These small-scale distribution patterns have been attributed to differences in their symbiont assemblages or host physiologies. However, little is known about the anatomy of most Alviniconcha species, beyond that detailed for the type species Alviniconcha hessleri, whose geographic range does not overlap with other congeners. In fact, species within this genus are currently described as cryptic, despite the absence of any comparative morphological studies to assess this. To test whether the genus is genuinely cryptic and identify any functional differences in host anatomy that might also mediate habitat partitioning in SW Pacific species, the current study examined the morphoanatomy of A. kojimai, A. boucheti and A. strummeri from the Fatu Kapa vent field, an area of hydrothermal activity recently discovered north of the Lau Basin near the Wallis and Futuna Islands and the only known example where all three species occur within adjacent vent fields. A combination of detailed dissections, histology and X-ray computed tomography demonstrate that A. kojimai, A. strummeri and A. boucheti are readily identifiable based on shell morphology and ornamentation alone, and therefore not truly cryptic. These traits provide a rapid and reliable means for species identification. However, aside from some subtle differences in radular morphology, these species of Alviniconcha exhibit conserved anatomical features, providing no evidence that functional host anatomy is implicated in habitat partitioning. This provides support for the current belief that host-species distributions are probably governed by symbiont-mediated physiological factors.
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The deep-sea hydrothermal vent shrimp Rimicaris exoculata largely depends on a dense epibiotic chemoautotrophic bacterial community within its enlarged cephalothoracic chamber. However, our understanding of shrimp-bacterium interactions is limited. In this report, we focused on the deltaproteobacterial epibiont of R. exoculata from the relatively unexplored South Mid-Atlantic Ridge. A nearly complete genome of a Deltaproteobacteria epibiont was binned from the assembled metagenome. Whole-genome phylogenetic analysis reveals that it is affiliated with the genus Desulfobulbus, representing a potential novel species for which the name "Candidatus Desulfobulbus rimicarensis" is proposed. Genomic and transcriptomic analyses reveal that this bacterium utilizes the Wood-Ljungdahl pathway for carbon assimilation and harvests energy via sulfur disproportionation, which is significantly different from other shrimp epibionts. Additionally, this epibiont has putative nitrogen fixation activity, but it is extremely active in directly taking up ammonia and urea from the host or vent environments. Moreover, the epibiont could be distinguished from its free-living relatives by various features, such as the lack of chemotaxis and motility traits, a dramatic reduction in biosynthesis genes for capsular and extracellular polysaccharides, enrichment of genes required for carbon fixation and sulfur metabolism, and resistance to environmental toxins. Our study highlights the unique role and symbiotic adaptation of Deltaproteobacteria in deep-sea hydrothermal vent shrimps.IMPORTANCE The shrimp Rimicaris exoculata represents the dominant faunal biomass at many deep-sea hydrothermal vent ecosystems along the Mid-Atlantic Ridge. This organism harbors dense bacterial epibiont communities in its enlarged cephalothoracic chamber that play an important nutritional role. Deltaproteobacteria are ubiquitous in epibiotic communities of R. exoculata, and their functional roles as epibionts are based solely on the presence of functional genes. Here, we describe "Candidatus Desulfobulbus rimicarensis," an uncultivated deltaproteobacterial epibiont. Compared to campylobacterial and gammaproteobacterial epibionts of R. exoculata, this bacterium possessed unique metabolic pathways, such as the Wood-Ljungdahl pathway, as well as sulfur disproportionation and nitrogen fixation pathways. Furthermore, this epibiont can be distinguished from closely related free-living Desulfobulbus strains by its reduced genetic content and potential loss of functions, suggesting unique adaptations to the shrimp host. This study is a genomic and transcriptomic analysis of a deltaproteobacterial epibiont and largely expands the understanding of its metabolism and adaptation to the R. exoculata host.
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Adaptación Biológica , Decápodos/microbiología , Deltaproteobacteria/aislamiento & purificación , Genoma Bacteriano , Respiraderos Hidrotermales/microbiología , Simbiosis , Animales , Océano Atlántico , Deltaproteobacteria/clasificación , Deltaproteobacteria/genética , Deltaproteobacteria/fisiología , Rasgos de la Historia de Vida , FilogeniaRESUMEN
Rimicaris exoculata is one of the most well-known and emblematic species of endemic vent fauna. Like many other species from these ecosystems, Rimicaris shrimps host important communities of chemosynthetic bacteria living in symbiosis with their host inside the cephalothorax and gut. For many of these symbiotic partners, the mode of transmission remains to be elucidated and the starting point of the symbiotic relationship is not yet defined, but could begin with the egg. In this study, we explored the proliferation of microbial communities on R. exoculata broods through embryonic development using a combination of NGS sequencing and microscopy approaches. Variations in abundance and diversity of egg microbial communities were analyzed in broods at different developmental stages and collected from mothers at two distinct vent fields on the Mid-Atlantic Ridge (TAG and Snake Pit). We also assessed the specificity of the egg microbiome by comparing communities developing on egg surfaces with those developing on the cuticle of pleopods, which are thought to be exposed to similar environmental conditions because the brood is held under the female's abdomen. In terms of abundance, bacterial colonization clearly increases with both egg developmental stage and the position of the egg within the brood: those closest to the exterior having a higher bacterial coverage. Bacterial biomass increase also accompanies an increase of mineral precipitations and thus clearly relates to the degree of exposure to vent fluids. In terms of diversity, most bacterial lineages were found in all samples and were also those found in the cephalothorax of adults. However, significant variation occurs in the relative abundance of these lineages, most of this variation being explained by body surface (egg vs. pleopod), vent field, and developmental stage. The occurrence of symbiont-related lineages of Epsilonbacteraeota, Gammaproteobacteria, Zetaproteobacteria, and Mollicutes provide a basis for discussion on both the acquisition of symbionts and the potential roles of these bacterial communities during egg development.
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Rimicaris chacei Williams and Rona 1986, formerly named as Chorocaris chacei, is a caridean shrimp living in deep-sea hydrothermal ecosystems. This shrimp is endemic to the Mid Atlantic Ridge (MAR) and lives at the periphery of aggregates of its well-known congeneric R. exoculata Williams and Rona 1986. Contrasting with the very dense and mobile clusters formed by R. exoculata, R. chacei lives in small groups of several individuals that are not very mobile. Although devoid of the characteristic hypertrophied cephalothorax of R. exoculata, which harbors the ectosymbionts, a microbial community has also been reported in the cephalothorax of R. chacei. Previous data on morphology, behavior and isotopic values indicate a diet based on a combination of feeding on its epibiotic bacteria and scavenging or occasional predation. In this study, our objective was to describe, for the first time, the distribution, morphology and phylogeny of the microbial communities associated with R. chacei. This species is significantly less studied than R. exoculata, but nevertheless represents the only other known example of symbiosis in crustaceans of MAR hydrothermal vent sites. Microbial communities have been observed at the same locations as in R. exoculata (mouthparts, branchiostegites and digestive tract). However, in R. chacei, the surfaces occupied by the bacteria are smaller. The main lineages are affiliated to Epsilon and Gammaproteobacteria in the cephalothorax and to Deferribacteres, Mollicutes, Epsilon and Gammaproteobacteria in the digestive tract. Comparison with the well-described bacterial communities of R. exoculata and hypotheses about the role of these communities in R. chacei are discussed.
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Decápodos/microbiología , Microbioma Gastrointestinal , Branquias/microbiología , Respiraderos Hidrotermales/microbiología , Microbiota , Simbiosis , Animales , Bacterias/citología , Bacterias/crecimiento & desarrollo , Bacterias/ultraestructura , Secuencia de Bases , Biodiversidad , Colorantes Fluorescentes/metabolismo , Gammaproteobacteria/genética , Tracto Gastrointestinal/ultraestructura , Filogenia , ARN Ribosómico 16S/genéticaRESUMEN
Deep-sea hydrothermal vent meiofauna have been the focus of recent research and the discovery of an abundant well-adapted free-living marine nematode on the Mid-Atlantic Ridge offers new perspectives on adaptations to the vent environment. Indeed, knowledge concerning biological interactions of microbes and meiofauna in marine extreme environments is scarce, especially for nematodes. In this study, we used microscopic observations [fluorescence in situ hybridization (FISH) and scanning electron microscopy (SEM)] and metabarcoding of 16S rRNA to characterize the bacterial community of the nematode species Oncholaimus dyvae, an overlooked but ecologically important vent organism. Detection of bacteria in the buccal cavity and on the cuticle (SEM) and epibionts in its intestine (FISH) suggests that O. dyvae harbors its own bacterial community. Molecular results and phylogenetic analysis show that bacteria associated with this species are related to symbiotic lineages typical of hydrothermal vent fauna, such as sulfur-oxidizing bacteria related to Epsilonproteobacteria and Gammaproteobacteria. This multi-approach study suggests a potential symbiotic role of bacteria with its nematode host and opens new research perspectives on vent meiofauna.
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Prokaryotic communities forming symbiotic relationships with the vent shrimp, Rimicaris exoculata, are well studied components of hydrothermal ecosystems at the Mid-Atlantic Ridge (MAR). Despite the tight link between host and symbiont, the observed lack of spatial genetic structure seen in R. exoculata contrasts with the geographic differentiation detected in specific bacterial ectosymbionts. The geographic clustering of bacterial lineages within a seemingly panmictic host suggests either the presence of finer scale restriction to gene flow not yet detected in the host, horizontal transmission (environmental selection) of its endosymbionts as a consequence of unique vent geochemistry, or vertically transmitted endosymbionts that exhibit genetic differentiation. To identify which hypothesis best fits, we tested whether bacterial assemblages exhibit differentiation across sites or host populations by performing a 16S rRNA metabarcoding survey on R. exoculata digestive prokaryote samples (n = 31) taken from three geochemically distinct vents across MAR: Rainbow, Trans-Atlantic Geotraverse (TAG) and Logatchev. Analysis of communities across two organs (digestive tract, stomach), three molt colors (white, red, black) and three life stages (eggs, juveniles, adults) also provided insights into symbiont transmission mode. Examining both whole communities and operational taxonomic units (OTUs) confirmed the presence of three main epibionts: Epsilonproteobacteria, Mollicutes and Deferribacteres. With these findings, we identified a clear pattern of geographic segregation by vent in OTUs assigned to Epsilonproteobacteria. Additionally, we detected evidence for differentiation among all communities associated to vents and life stages. Overall, results suggest a combination of environmental selection and vertical inheritance of some of the symbiotic lineages.
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Crustáceos/microbiología , Tracto Gastrointestinal/microbiología , Geografía , AnimalesRESUMEN
Rimicaris exoculata is a caridean shrimp that dominates the fauna at several hydrothermal vent sites of the Mid-Atlantic Ridge. It has two distinct and stable microbial communities. One of these epibiontic bacterial communities is located in the shrimp gut and has a distribution and role that are poorly understood. The second colonizes its enlarged gill chamber and is involved in host nutrition. It is eliminated after each molt, and has colonization processes reminiscent of those of a biofilm. The presence and expression of genes usually involved in quorum sensing (QS) were then studied. At four sites, Rainbow, TAG, Snake Pit and Logatchev, two lux genes were identified in the R. exoculata epibiontic community at different shrimp molt stages and life stages. RT-PCR experiments highlighted lux gene expression activity at TAG, Snake Pit and Rainbow vent sites. Their potential QS activity and their possible roles in epibiont colonization processes are discussed. Moreover, phylogenetic analysis has shown the presence of three clades for luxS (Epsilonproteobacteria) and four clades for luxR (Gammaproteobacteria) genes, each clade being restricted to a single site. These genes are more divergent than the 16S rRNA one. They could therefore be used as biogeographical genetic markers.
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ADN Bacteriano/genética , Decápodos/microbiología , Genes Bacterianos/genética , Marcadores Genéticos/genética , Respiraderos Hidrotermales/microbiología , Percepción de Quorum/genética , Animales , Epsilonproteobacteria/genética , Gammaproteobacteria/genética , Branquias/microbiología , Filogenia , ARN Ribosómico 16S/genética , Análisis de Secuencia de ADN/métodosRESUMEN
Alvinocaridid shrimps are endemic species inhabiting hydrothermal vents and/or cold seeps. Although indirect evidences (genetic and lipid markers) suggest that their larval stages disperse widely and support large scale connectivity, larval life and mechanisms underlying dispersal are unknown in alvinocaridids. Here we provide for the first time detailed descriptions of the first larval stage (zoea I) of four alvinocaridid species: Rimicaris exoculata and Mirocaris fortunata from the Mid-Atlantic Ridge, Alvinocaris muricola from the Congo Basin and Nautilocaris saintlaurentae from the Western Pacific. The larvae were obtained from onboard hatching of brooding females (either at atmospheric pressure or at habitat pressure in hyperbaric chambers) and from the water column near adult habitats, sampled with plankton pumps or sediment traps. Major characteristics of the alvinocaridid larvae include undeveloped mandible and almost complete absence of setation in the inner margin of the mouth parts and maxillipeds. Although the larvae are very similar between the four species studied, some morphological features could be used for species identification. In addition, undeveloped mouthparts and the large amount of lipid reserves strongly support the occurrence of primary lecithotrophy in the early stage of alvinocaridids. Although lecithotrophy in decapod crustaceans is usually associated with abbreviated larval development, as a mechanism of larval retention, morphological and physiological evidences suggest the occurrence of an extended and lecithotrophic larval stage in the Alvinocarididae. These traits permit the colonization of widely dispersed and fragmented environments of hydrothermal vents and cold seeps. Distribution of larval traits along the phylogenetic reconstruction of the Alvinocarididae and related families suggest that lecithotrophy/planktotrophy and extended/abbreviated development have evolved independently along related families in all potential combinations. However, the Alvinocarididae is the only taxa with a combination of lecithotrophy and extended larval development.