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

ABSTRACT: 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.

SUBMITTER: Methou P

PROVIDER: S-EPMC7428246 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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

Methou Pierre P Michel Loïc N LN Segonzac Michel M Cambon-Bonavita Marie-Anne MA Pradillon Florence F

Royal Society open science 20200708 7

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 thei ...[more]

PMID: 32874664

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Project description: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.

Project description: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.

Project description:While most studies have focused on the timing and nature of ontogenetic niche shifts, information is scarce about the effects of community structure on trophic ontogeny of top predators. We investigated how community structure affects ontogenetic niche shifts (i.e., relationships between body length, trophic position, and individual dietary specialization) of a predatory fish, brown trout (Salmo trutta). We used stable isotope and stomach content analyses to test how functional characteristics of lake fish community compositions (competition and prey availability) modulate niche shifts in terms of (i) piscivorous behavior, (ii) trophic position, and (iii) individual dietary specialization. Northern Scandinavian freshwater fish communities were used as a study system, including nine subarctic lakes with contrasting fish community configurations: (i) trout-only systems, (ii) two-species systems (brown trout and Arctic charr [Salvelinus alpinus] coexisting), and (iii) three-species systems (brown trout, Arctic charr, and three-spined sticklebacks [Gasterosteus aculeatus] coexisting). We expected that the presence of profitable small prey (stickleback) and mixed competitor-prey fish species (charr) supports early piscivory and high individual dietary specialization among trout in multispecies communities, whereas minor ontogenetic shifts were expected in trout-only systems. From logistic regression models, the presence of a suitable prey fish species (stickleback) emerged as the principal variable determining the size at ontogenetic niche shifts. Generalized additive mixed models indicated that fish community structure shaped ontogenetic niche shifts in trout, with the strongest positive relationships between body length, trophic position, and individual dietary specialization being observed in three-species communities. Our findings revealed that the presence of a small-sized prey fish species (stickleback) rather than a mixed competitor-prey fish species (charr) was an important factor affecting the ontogenetic niche-shift processes of trout. The study demonstrates that community structure may modulate the ontogenetic diet trajectories of and individual niche specialization within a top predator.

Dataset Information

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

Publications

Integrative taxonomy revisits the ontogeny and trophic niches of <i>Rimicaris</i> vent shrimps.

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