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Neuroanatomy of a hydrothermal vent shrimp provides insights into the evolution of crustacean integrative brain centers.

ABSTRACT: Alvinocaridid shrimps are emblematic representatives of the deep hydrothermal vent fauna at the Mid-Atlantic Ridge. They are adapted to a mostly aphotic habitat with extreme physicochemical conditions in the vicinity of the hydrothermal fluid emissions. Here, we investigated the brain architecture of the vent shrimp Rimicaris exoculata to understand possible adaptations of its nervous system to the hydrothermal sensory landscape. Its brain is modified from the crustacean brain ground pattern by featuring relatively small visual and olfactory neuropils that contrast with well-developed higher integrative centers, the hemiellipsoid bodies. We propose that these structures in vent shrimps may fulfill functions in addition to higher order sensory processing and suggest a role in place memory. Our study promotes vent shrimps as fascinating models to gain insights into sensory adaptations to peculiar environmental conditions, and the evolutionary transformation of specific brain areas in Crustacea.

SUBMITTER: Machon J

PROVIDER: S-EPMC6684273 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Neuroanatomy of a hydrothermal vent shrimp provides insights into the evolution of crustacean integrative brain centers.

Machon Julia J Krieger Jakob J Meth Rebecca R Zbinden Magali M Ravaux Juliette J Montagné Nicolas N Chertemps Thomas T Harzsch Steffen S

eLife 20190806

Alvinocaridid shrimps are emblematic representatives of the deep hydrothermal vent fauna at the Mid-Atlantic Ridge. They are adapted to a mostly aphotic habitat with extreme physicochemical conditions in the vicinity of the hydrothermal fluid emissions. Here, we investigated the brain architecture of the vent shrimp <i>Rimicaris exoculata</i> to understand possible adaptations of its nervous system to the hydrothermal sensory landscape. Its brain is modified from the crustacean brain ground patt ...[more]

PMID: 31383255

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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:Symbioses between metazoans and microbes involved in sulfur cycling are integral to the ability of animals to thrive within deep-sea hydrothermal vent environments; the development of such interactions is regarded as a key adaptation in enabling animals to successfully colonize vents. Microbes often colonize the surfaces of vent animals and, remarkably, these associations can also be observed intricately preserved by pyrite in the fossil record of vent environments, stretching back to the lower Paleozoic (Ordovician-early Silurian). In non-vent environments, sulfur isotopes are often employed to investigate the metabolic strategies of both modern and fossil organisms, as certain metabolic pathways of microbes, notably sulfate reduction, can produce large sulfur isotope fractionations. However, the sulfur isotopes of vent fossils, both ancient and recently mineralized, have seldom been explored, and it is not known if the pyrite-preserved vent organisms might also preserve potential signatures of their metabolisms. Here, we use high-resolution secondary ion mass spectrometry (SIMS) to investigate the sulfur isotopes of pyrites from recently mineralized and Ordovician-early Silurian tubeworm fossils with associated microbial fossils. Our results demonstrate that pyrites containing microbial fossils consistently have significantly more negative δ34 S values compared with nearby non-fossiliferous pyrites, and thus represent the first indication that the presence of microbial sulfur-cycling communities active at the time of pyrite formation influenced the sulfur isotope signatures of pyrite at hydrothermal vents. The observed depletions in δ34 S are generally small in magnitude and are perhaps best explained by sulfur isotope fractionation through a combination of sulfur-cycling processes carried out by vent microbes. These results highlight the potential for using sulfur isotopes to explore biological functional relationships within fossil vent communities, and to enhance understanding of how microbial and animal life has co-evolved to colonize vents throughout geological time.

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Neuroanatomy of a hydrothermal vent shrimp provides insights into the evolution of crustacean integrative brain centers.

Publications

Neuroanatomy of a hydrothermal vent shrimp provides insights into the evolution of crustacean integrative brain centers.

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