Revision of the alvinocaridid shrimp genus Rimicaris Williams & Rona, 1986 (Decapoda: Caridea) with description of a new species from the Mariana Arc hydrothermal vents.

A new species of alvinocaridid shrimp is reported, from the Northwest Eifuku hydrothermal vent field at 16191667 m depth on the Mariana Arc. A comprehensive phylogenetic reconstruction of Alvinocarididae based on the mitochondrial cytochrome c oxidase subunit I (COI) gene including this new species reveals the paraphyly of the genus Rimicaris Williams & Rona, 1986 with four other generaAlvinocaridinides, Manuscaris, Opaepele, and Shinkaicarisnested within it. We re-examine material of these four problematic genera, and synonymise them under Rimicaris whose diagnosis has been amended, in order to maintain a monophyletic Rimicaris. Our new species, Rimicaris cambonae sp. nov. is genetically close to Rimicaris loihi (Williams & Dobbs, 1995) comb. nov. (previously Opaepele loihi) with which it co-occurs, but can be morphologically distinguished by the less elevated dorsal surface of the rostrum, this being devoid of a median carina, a stronger pterygostomial tooth on the carapace, and a blunt rather than acuminate proximolateral process on the antennular stylocerite. Species previously assigned to the above listed, synonymized genera are also discussed, with new material examined for three key species: R. loihi, R. acuminata, and R. leurokolos. Further, Alvinocaridinides formosa Komai & Chan, 2010 and Manuscaris liui Wang & Sha, 2016 are synonymized under Rimicaris leurokolos (Kikuchi & Hashimoto, 2000) comb. nov. and R. acuminata (Komai & Tsuchida, 2015) comb. nov., respectively. Revised diagnoses are presented for R. loihi, R. acuminata, and R. leurokolos. After the present revision revision, Rimicaris now consists of 15 species.

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 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.

Symbioses of alvinocaridid shrimps from the South West Pacific: No chemosymbiotic diets but 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 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.

Reproduction in deep-sea vent shrimps is influenced by diet, with rhythms apparently unlinked to surface production.

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 as a study case to explore relationships 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 one relying on mixotrophy, R. chacei. Besides, our data suggest a reproductive periodicity that does not correspond to seasonal variations in surface production, with substantial proportions of brooding females during the same months of the year, despite those months corresponding to either boreal winter or austral summer depending on the hemisphere. 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 the surface. Our results suggest the presence of an intrinsic basis for biological rhythms in the deep sea, and bring to light the importance of having year-round observations in order to understand the life history of vent animals.

Symbiont Community Composition in Rimicaris kairei Shrimps from Indian Ocean Vents with Notes on Mineralogy.

Hydrothermal vent ecosystems are home to a wide array of symbioses between animals and chemosynthetic microbes, among which shrimps in the genus Rimicaris is one of the most iconic. So far, studies of Rimicaris symbioses have been restricted to Atlantic species, including Rimicaris exoculata, which is totally reliant on the symbionts for nutrition, and the mixotrophic species Rimicaris chacei. Here, we expand this by investigating and characterizing the symbiosis of the Indian Ocean species Rimicaris kairei using specimens from two vent fields, Kairei and Edmond. We also aimed to evaluate the differences in mineralogy and microbial communities between two cephalothorax color morphs, black and brown, through a combination of 16S metabarcoding, scanning electron microscopy, fluorescent in situ hybridization, energy-dispersive X-ray spectroscopy, and synchrotron near-edge X-ray absorption structure analyses. Overall, our results highlight that R. kairei exhibits similar symbiont lineages to those of its Atlantic congeners, although with a few differences, such as the lack of Zetaproteobacteria. We found distinct mineralization processes behind the two color morphs that were linked to differences in the vent fluid composition, but the symbiotic community composition was surprisingly similar. In R. exoculata, such mineralogical differences have been shown to stem from disparity in the microbial communities, but our results indicate that in R. kairei this is instead due to the shift of dominant metabolisms by the same symbiotic partners. We suggest that a combination of local environmental factors and biogeographic barriers likely contribute to the differences between Atlantic and Indian Ocean Rimicaris symbioses. IMPORTANCE Hydrothermal vent shrimps in the genus Rimicaris are among the most charismatic deep-sea animals of Atlantic and Indian Oceans, often occurring on towering black smokers in dense aggregates of thousands of individuals. Although this dominance is only possible because of symbiosis, no study on the symbiosis of Indian Ocean Rimicaris species has been conducted. Here, we characterize the Rimicaris kairei symbiosis by combining molecular, microscopic, and elemental analyses, making comparisons with those of the Atlantic species possible for the first time. Although most symbiotic partners remained consistent across the two oceans, some differences were recognized in symbiont lineages, as well as in the mechanisms behind the formation of two color morphs with distinct mineralogies. Our results shed new light on relationships among mineralogy, environmental factors, and microbial communities that are useful for understanding other deep-sea symbioses in the future.

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.

Antimicrobial Peptides and Ectosymbiotic Relationships: Involvement of a Novel Type IIa Crustin in the Life Cycle of a Deep-Sea Vent Shrimp.

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.

Is It First the Egg or the Shrimp? - Diversity and Variation in Microbial Communities Colonizing Broods of the Vent Shrimp Rimicaris exoculata During Embryonic Development.

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.