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Neuroanatomy of the vestimentiferan tubeworm Lamellibrachia satsuma provides insights into the evolution of the polychaete nervous system.

ABSTRACT: Vestimentiferan tubeworms are marine invertebrates that inhabit chemosynthetic environments, and although recent molecular phylogenetic analyses have suggested that vestimentiferan tubeworms are derived from polychaete annelids, they show some morphological features that are different from other polychaetes. For example, vestimentiferans lack a digestive tract and have less body segments and comparative neuroanatomy can provide essential insight into the vestimentiferan body plan and its evolution. In the present study, we investigated the adult nervous system in the vestimentiferan Lamellibrachia satsuma using antibodies against synapsin, serotonin, FMRMamide and acetylated ?-tubulin. We also examined the expressions of neural marker genes, elav and synaptotagmin to reveal the distribution of neuronal cell bodies. Brain anatomy shows simple organization in Lamellibrachia compared to other polychaetes. This simplification is probably due to the loss of the digestive tract, passing through the body between the brain and the subesophageal ganglion. In contrast, the ventral nerve cord shows a repeated organizational structure as in the other polychaetes, despite the absence of the multiple segmentation of the trunk. These results suggest that the brain anatomy is variable depending on the function and the condition of surrounding tissues, and that the formation of the rope ladder-like nervous system of the ventral nerve cord is independent from segmentation in polychaetes.

SUBMITTER: Miyamoto N

PROVIDER: S-EPMC3553155 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Neuroanatomy of the vestimentiferan tubeworm Lamellibrachia satsuma provides insights into the evolution of the polychaete nervous system.

Miyamoto Norio N Shinozaki Ayuta A Fujiwara Yoshihiro Y

PloS one 20130123 1

Vestimentiferan tubeworms are marine invertebrates that inhabit chemosynthetic environments, and although recent molecular phylogenetic analyses have suggested that vestimentiferan tubeworms are derived from polychaete annelids, they show some morphological features that are different from other polychaetes. For example, vestimentiferans lack a digestive tract and have less body segments and comparative neuroanatomy can provide essential insight into the vestimentiferan body plan and its evoluti ...[more]

PMID: 23372830

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Project description:UnlabelledThe symbiotic relationship between vestimentiferan tubeworms and their intracellular chemosynthetic bacteria is one of the more noteworthy examples of adaptation to deep-sea hydrothermal vent environments. The tubeworm symbionts have never been cultured in the laboratory. Nucleotide sequences from the small subunit rRNA gene suggest that the intracellular symbionts of the eastern Pacific vent tubeworms Oasisia alvinae, Riftia pachyptila, Tevnia jerichonana, and Ridgeia piscesae belong to the same phylotype of gammaproteobacteria, "Candidatus Endoriftia persephone." Comparisons of symbiont genomes between the East Pacific Rise tubeworms R. pachyptila and T. jerichonana confirmed that these two hosts share the same symbionts. Two Ridgeia symbiont genomes were assembled from trophosome metagenomes from worms collected from the Juan de Fuca Ridge (one and five individuals, respectively). We compared these assemblies to those of the sequenced Riftia and Tevnia symbionts. Pangenome composition, genome-wide comparisons of the nucleotide sequences, and pairwise comparisons of 2,313 orthologous genes indicated that "Ca Endoriftia persephone" symbionts are structured on large geographical scales but also on smaller scales and possibly through host specificity.ImportanceRemarkably, the intracellular symbionts of four to six species of eastern Pacific vent tubeworms all belong to the same phylotype of gammaproteobacteria, "Candidatus Endoriftia persephone." Understanding the structure, dynamism, and interconnectivity of "Ca Endoriftia persephone" populations is important to advancing our knowledge of the ecology and evolution of their host worms, which are often keystone species in vent communities. In this paper, we present the first genomes for symbionts associated with the species R. piscesae, from the Juan de Fuca Ridge. We then combine these genomes with published symbiont genomes from the East Pacific Rise tubeworms R. pachyptila and T. jerichonana to develop a portrait of the "Ca Endoriftia persephone" pangenome and an initial outline of symbiont population structure in the different host species. Our study is the first to apply genome-wide comparisons of "Ca Endoriftia persephone" assemblies in the context of population genetics and molecular evolution.

Project description:BACKGROUND:The microbial endosymbionts of two species of vestimentiferan tubeworms (Escarpia sp. and Lamellibrachia sp.2) collected from an area of low-temperature hydrothermal diffuse vent flow at the Mid-Cayman Rise (MCR) in the Caribbean Sea were characterized using microscopy, phylogenetic analyses, and a metagenomic approach. RESULTS:Bacteria, with a typical Gram negative cell envelope contained within membrane-bound vacuoles, were observed within the trophosome of both tubeworm species. Phylogenetic analysis of the 16S rRNA gene and ITS region suggested MCR individuals harbored highly similar endosymbionts that were >?98% identical, with the exception of two symbionts that showed a 60 bp insertion within the ITS region. All sequences from MCR endosymbionts formed a separate well-supported clade that diverged from those of symbionts of seep and vent vestimentiferans from the Pacific, Gulf of Mexico, and Mediterranean Sea. The metagenomes of the symbionts of two specimens of each tubeworm species were sequenced, and two distinct Gammaproteobacteria metagenome-assembled genomes (MAGs) of more than 4 Mbp assembled. An Average Nucleotide Identity (ANI) of 86.5% between these MAGs, together with distinct 16S rRNA gene and ITS sequences, indicate the presence of multiple endosymbiont phylotypes at the MCR, with one MAG shared between one Escarpia and two Lamellibrachia individuals, indicating these endosymbionts are not specific to either host species. Genes for sulfur and hydrogen oxidation, nitrate reduction (assimilatory and dissimilatory), glycolysis and the Krebs cycle, peptide, sugar, and lipid transporters, and both rTCA and CBB carbon fixation cycles were detected in the MAGs, highlighting key and shared functions with symbiont metagenomes of the vestimentiferans Riftia, Tevnia, and Ridgeia from the Pacific. The potential for a second hydrogen oxidation pathway (via a bidirectional hydrogenase), formate dehydrogenase, a catalase, and several additional peptide transporters were found exclusively in the MCR endosymbiont MAGs. CONCLUSIONS:The present study adds new evidence that tubeworm endosymbionts can potentially switch from autotrophic to heterotrophic metabolism, or may be mixotrophic, presumably while free-living, and also suggests their versatile metabolic potential may enable both the host and symbionts to exploit a wide range of environmental conditions. Together, the marked gene content and sequence dissimilarity at the rRNA operon and whole genome level between vent and seep symbionts suggest these newly described endosymbionts from the MCR belong to a novel tubeworm endosymbiont genera, introduced as Candidatus Vondammii.

Project description:BACKGROUND:Symbiotic relationships between microbes and their hosts are widespread and diverse, often providing protection or nutrients, and may be either obligate or facultative. However, the genetic mechanisms allowing organisms to maintain host-symbiont associations at the molecular level are still mostly unknown, and in the case of bacterial-animal associations, most genetic studies have focused on adaptations and mechanisms of the bacterial partner. The gutless tubeworms (Siboglinidae, Annelida) are obligate hosts of chemoautotrophic endosymbionts (except for Osedax which houses heterotrophic Oceanospirillales), which rely on the sulfide-oxidizing symbionts for nutrition and growth. Whereas several siboglinid endosymbiont genomes have been characterized, genomes of hosts and their adaptations to this symbiosis remain unexplored. RESULTS:Here, we present and characterize adaptations of the cold seep-dwelling tubeworm Lamellibrachia luymesi, one of the longest-lived solitary invertebrates. We sequenced the worm's ~?688-Mb haploid genome with an overall completeness of ~?95% and discovered that L. luymesi lacks many genes essential in amino acid biosynthesis, obligating them to products provided by symbionts. Interestingly, the host is known to carry hydrogen sulfide to thiotrophic endosymbionts using hemoglobin. We also found an expansion of hemoglobin B1 genes, many of which possess a free cysteine residue which is hypothesized to function in sulfide binding. Contrary to previous analyses, the sulfide binding mediated by zinc ions is not conserved across tubeworms. Thus, the sulfide-binding mechanisms in sibgolinids need to be further explored, and B1 globins might play a more important role than previously thought. Our comparative analyses also suggest the Toll-like receptor pathway may be essential for tolerance/sensitivity to symbionts and pathogens. Several genes related to the worm's unique life history which are known to play important roles in apoptosis, cell proliferation, and aging were also identified. Last, molecular clock analyses based on phylogenomic data suggest modern siboglinid diversity originated in 267 mya (±?70 my) support previous hypotheses indicating a Late Mesozoic or Cenozoic origins of approximately 50-126 mya for vestimentiferans. CONCLUSIONS:Here, we elucidate several specific adaptations along various molecular pathways that link phenome to genome to improve understanding of holobiont evolution. Our findings of adaptation in genomic mechanisms to reducing environments likely extend to other chemosynthetic symbiotic systems.

Dataset Information

Neuroanatomy of the vestimentiferan tubeworm Lamellibrachia satsuma provides insights into the evolution of the polychaete nervous system.

Publications

Neuroanatomy of the vestimentiferan tubeworm Lamellibrachia satsuma provides insights into the evolution of the polychaete nervous system.

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