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Greg W Rouse - One of the best experts on this subject based on the ideXlab platform.
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an inordinate fondness for osedax Siboglinidae annelida fourteen new species of bone worms from california
Zootaxa, 2018Co-Authors: Greg W Rouse, Shana K Goffredi, Shannon B Johnson, Robert C. VrijenhoekAbstract:We incorporate DNA sequences from a comprehensive sampling of taxa to provide an updated phylogeny of Osedax and discuss the remarkable diversity of this clade of siboglinids. We formally describe 14 new species of Osedax from Monterey Bay, California, USA, raising the total number of properly named Osedax species to 25. These new species had formerly been recognized by informal names in various publications, and on GenBank. The descriptions document the occurrence of dwarf males in five of the new species. The distribution for the 19 species of Osedax known to occur in Monterey Bay across depths from 385 to 2898 meters and various bone substrates is documented. The exploitation of extant bird and marine turtle bones by Osedax is reported for the first time .
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the reproductive system of osedax annelida Siboglinidae ovary structure sperm ultrastructure and fertilization mode
Invertebrate Biology, 2013Co-Authors: Sigrid Katz, Greg W RouseAbstract:Osedax is a genus of siboglinid annelids in which the females live on dead vertebrate bones on the seafloor. These females have a posterior end that lies within the bone and contains the ovarian tissue, as well as the “roots” involved with bone degradation and nutrition. The males are microscopic and live as “harems” in the lumen of the gelatinous tube that surrounds the female trunk, well away from the ovary. Females are known to spawn fertilized primary oocytes, suggesting internal fertilization. However, little is known about sperm transfer, sperm storage, or the location of fertilization, and the morphology of the female reproductive system has not been described and compared with the reproductive systems of other siboglinids. A 3D-reconstruction of the ovisac of Osedax showed ovarian tissue with multiple lobes and mature oocytes stored in a “uterus” before being released through the single oviduct. The oviduct emerges as a gonopore on the trunk and travels along the trunk to finally open to the seawater as a thin cylindrical tube among the crown of palps. Light and transmission electron microscopy of mature Osedax sperm revealed elongate heads consisting of a nucleus with helical grooves occupied by mitochondria. In contrast to other Siboglinidae, Osedax sperm are not packaged into spermatophores or spermatozeugmata, and Osedax females lack a discrete region for sperm storage. Transmission electron microscopy and fluorescence microscopy allowed detection of sperm associated with ovarian tissue of the female ovisac of four different Osedax species. This provides the first evidence for the site of internal fertilization in Osedax. A heart body was found in the circulatory system, as seen in other siboglinids and some other annelids. The possible presence of nephridia in the anterior ovisac region was also documented. These morphological features provide new insights for comparing the regionalization of Osedax females in relation to other siboglinids.
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a remarkable diversity of bone eating worms osedax Siboglinidae annelida
BMC Biology, 2009Co-Authors: Robert C. Vrijenhoek, Shannon B Johnson, Greg W RouseAbstract:Bone-eating Osedax worms have proved to be surprisingly diverse and widespread. Including the initial description of this genus in 2004, five species that live at depths between 25 and 3,000 m in the eastern and western Pacific and in the north Atlantic have been named to date. Here, we provide molecular and morphological evidence for 12 additional evolutionary lineages from Monterey Bay, California. To assess their phylogenetic relationships and possible status as new undescribed species, we examined DNA sequences from two mitochondrial (COI and 16S rRNA) and three nuclear genes (H3, 18S and 28S rRNA). Phylogenetic analyses identified 17 distinct evolutionary lineages. Levels of sequence divergence among the undescribed lineages were similar to those found among the named species. The 17 lineages clustered into five well-supported clades that also differed for a number of key morphological traits. Attempts to determine the evolutionary age of Osedax depended on prior assumptions about nucleotide substitution rates. According to one scenario involving a molecular clock calibrated for shallow marine invertebrates, Osedax split from its siboglinid relatives about 45 million years ago when archeocete cetaceans first appeared and then diversified during the late Oligocene and early Miocene when toothed and baleen whales appeared. Alternatively, the use of a slower clock calibrated for deep-sea annelids suggested that Osedax split from its siboglinid relatives during the Cretaceous and began to diversify during the Early Paleocene, at least 20 million years before the origin of large marine mammals. To help resolve uncertainties about the evolutionary age of Osedax, we suggest that the fossilized bones from Cretaceous marine reptiles and late Oligocene cetaceans be examined for possible trace fossils left by Osedax roots. Regardless of the outcome, the present molecular evidence for strong phylogenetic concordance across five separate genes suggests that the undescribed Osedax lineages comprise evolutionarily significant units that have been separate from one another for many millions of years. These data coupled with ongoing morphological analyses provide a solid foundation for their future descriptions as new species.
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spawning and development in osedax boneworms Siboglinidae annelida
Marine Biology, 2009Co-Authors: Greg W Rouse, Nerida G Wilson, Shana K Goffredi, Shannon B Johnson, Tracey I Smart, Chad L Widmer, Craig M Young, Robert C. VrijenhoekAbstract:We report observations on spawning and early development in bone-eating worms of the genus Osedax. Individual females of Osedax rubiplumus were observed at 1820 m depth freely spawning hundreds of oocytes, and females of an undescribed species, Osedax “orange collar”, were observed spawning in laboratory aquaria. Cytological and molecular analysis of the spawned oocytes of two Osedax species revealed no evidence for the bacterial endosymbionts that the female worms require for their nutrition, suggesting that the bacteria must be acquired later from the environment, as they are in other siboglinids. Individual O. “orange collar” females released an average of 335 (±130) eggs per day, but the number of oocytes spawned per day varied greatly, suggesting that not all the females spawned daily. Fertilization rates of the spawned oocytes varied from 0 to 100%, though most females showed nearly 100% fertilization rates. Oocytes spawned in the laboratory at 4–6°C were negatively buoyant. If fertilized, these oocytes extruded polar bodies and then after at least four hours cleaved unequally. Subsequent cleavages occurred in a spiral pattern at roughly 2-h intervals, resulting in free-swimming trochophore larvae after 24 h. These lecithotrophic trochophores swam for 9–16 days before settling with several hooked chaetae, similar to those of dwarf Osedax males. The larval life span of the Osedax species studied in the laboratory appears to be shorter than in closely related Vestimentifera. Osedax rubiplumus, on the other hand, has much larger oocytes and so may have greater dispersal potential than these other Osedax species. The high fecundity and apparently continuous reproduction of Osedax boneworms permits the opportunistic exploitation of sunken vertebrate bones.
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Progress in systematics: from Siboglinidae to Pogonophora and Vestimentifera and back to Siboglinidae.
Comptes rendus biologies, 2008Co-Authors: Fredrik Pleijel, Thomas G Dahlgren, Greg W RouseAbstract:We review the taxonomic history of pogonophores (frenulates and vestimentiferans), from the species in first described 1914 to the recently described bone-eating worm Osedax. Previous systematists have referred both groups to the rank of phylum, and the animals have been treated as deuterostomes with a dorsal nerve cord. Further knowledge on their embryology, the discovery of the previously overlooked posterior, segmented part provided with chaetae, and access to molecular data, have completely changed earlier views on their affinities. They are now referred to as a single family of polychaete annelids, Siboglinidae.
Monika Bright - One of the best experts on this subject based on the ideXlab platform.
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Supporting Material, Supporting Figures S1-S4, Supporting Tables S1-S6 from Polyclonal symbiont populations in hydrothermal vent tubeworms and the environment
2019Co-Authors: Julia Polzin, Philip Arevalo, Thomas Nussbaumer, Martin F. Polz, Monika BrightAbstract:Horizontally transmitted symbioses usually house multiple and variable symbiont genotypes that are acquired from a much more diverse environmental pool via partner choice mechanisms. However, in the deep-sea hydrothermal vent tubeworm Riftia pachyptila (Vestimentifera, Siboglinidae), it has been suggested that the Candidatus Endoriftia persephone symbiont is monoclonal. Here, we show with high-coverage metagenomics that adult R. pachyptila house a polyclonal symbiont population consisting of one dominant and several low-frequency variants. This dominance of one genotype is confirmed by multilocus sequencing of amplified housekeeping genes in a broad range of host individuals where three out of four loci (atpA, uvrD and recA) revealed no genomic differences, while one locus (gyrB) was more diverse in adults than in juveniles. We also analysed a metagenome of free-living Endoriftia and found that the free-living population showed greater sequence variability than the host-associated population. Most juveniles and adults shared a specific dominant genotype, while other genotypes can dominate in few individuals. We suggest that although generally permissive, partner choice is selective enough to restrict uptake of some genotypes present in the environment
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Supporting Material, Supporting Figures S1-S4, Supporting Tables S1-S6 from Polyclonal symbiont populations in hydrothermal vent tubeworms and the environment
2019Co-Authors: Julia Polzin, Philip Arevalo, Thomas Nussbaumer, Martin F. Polz, Monika BrightAbstract:Horizontally transmitted symbioses usually house multiple and variable symbiont genotypes that are acquired from a much more diverse environmental pool via partner choice mechanisms. However, in the deep-sea hydrothermal vent tubeworm Riftia pachyptila (Vestimentifera, Siboglinidae), it has been suggested that the Candidatus Endoriftia persephone symbiont is monoclonal. Here, we show with high-coverage metagenomics that adult R. pachyptila house a polyclonal symbiont population consisting of one dominant and several low-frequency variants. This dominance of one genotype is confirmed by multilocus gene sequencing of amplified housekeeping genes in a broad range of host individuals where three out of four loci (atpA, uvrD and recA) revealed no genomic differences, while one locus (gyrB) was more diverse in adults than in juveniles. We also analysed a metagenome of free-living Endoriftia and found that the free-living population showed greater sequence variability than the host-associated population. Most juveniles and adults shared a specific dominant genotype, while other genotypes can dominate in few individuals. We suggest that although generally permissive, partner choice is selective enough to restrict uptake of some genotypes present in the environment
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endosymbionts escape dead hydrothermal vent tubeworms to enrich the free living population
Proceedings of the National Academy of Sciences of the United States of America, 2015Co-Authors: Julia Klose, Sabine Gollner, Martin F. Polz, Michael Wagner, Mario P Schimak, Monika BrightAbstract:Theory predicts that horizontal acquisition of symbionts by plants and animals must be coupled to release and limited dispersal of symbionts for intergenerational persistence of mutualisms. For deep-sea hydrothermal vent tubeworms (Vestimentifera, Siboglinidae), it has been demonstrated that a few symbiotic bacteria infect aposymbiotic host larvae and grow in a newly formed organ, the trophosome. However, whether viable symbionts can be released to augment environmental populations has been doubtful, because (i) the adult worms lack obvious openings and (ii) the vast majority of symbionts has been regarded as terminally differentiated. Here we show experimentally that symbionts rapidly escape their hosts upon death and recruit to surfaces where they proliferate. Estimating symbiont release from our experiments taken together with well-known tubeworm density ranges, we suggest a few million to 1.5 billion symbionts seeding the environment upon death of a tubeworm clump. In situ observations show that such clumps have rapid turnover, suggesting that release of large numbers of symbionts may ensure effective dispersal to new sites followed by active larval colonization. Moreover, release of symbionts might enable adaptations that evolve within host individuals to spread within host populations and possibly to new environments.
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The metatrochophore of a deep-sea hydrothermal vent vestimentiferan (Polychaeta: Siboglinidae)
Organisms Diversity & Evolution, 2013Co-Authors: Monika Bright, Irmgard Eichinger, Luitfried Von Salvini-plawenAbstract:Vestimentiferans (Siboglinidae, Polychaeta) live as juveniles and adults in an obligate mutualistic association with thiotrophic bacteria. Since their development is aposymbiotic, metatrochophores of vestimentiferans from the East Pacific Rise colonizing deep-sea hydrothermal vents are infected with the specific symbiont, develop the trophosome, and reduce their digestive system. To gain insight into the anatomy and ultrastructure and to compare this stage with metatrochophores from other siboglinids, we serial sectioned and reconstructed three specimens using light and transmission electron microscopy. The metatrochophore was composed of a prostomium, a small peristomium, two chaetigers (or two chaetigers and one additional segment without chaetae), and a minute pygidium. A digestive system and an intraepidermal nervous system were developed. Larval organs such as the prototroch, the neurotroch, and an apical organ were present, along with juvenile/adult organs such as tentacles, uncini, pyriform glands, and the anlage of the nephridial organ. We propose that in vestimentiferans, the vestimentum is the head arising from the prostomium, peristomium, and the anterior part of the first chaetiger. In frenulates, in contrast, the head is composed on the one hand of the cephalic lobe arising from the prostomium and on the other of the forepart developing from the peristomium and the anterior part of the first chaetiger. In frenulates the muscular septum between the forepart and trunk develops later than the first two chaetigers. Since this septum has no counterpart in vestimentiferans, the forepart-trunk border of frenulates is not considered homologous with the vestimentum-trunk border in vestimentiferans. The obturacular region in vestimentiferans does not appear to be a body region but rather the head appendages arising from the first chaetiger. In contrast, the tentacles in frenulates are prostomial head appendages. In both taxa, the trunk is the posterior part of the first chaetiger, and the opisthosoma is the following chaetigers and the pygidium. Comparisons with other polychaetes suggest that two larval segments are autapomorphic for the monophyletic Siboglinidae.
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simultaneous 16s and 18s rrna fluorescence in situ hybridization fish on lr white sections demonstrated in vestimentifera Siboglinidae tubeworms
Acta Histochemica, 2012Co-Authors: Mario P Schimak, Elena R Toenshoff, Monika BrightAbstract:Traditional morphological identification of invertebrate marine species is limited in early life history stages for many taxa. In this study, we demonstrate, by example of Vestimentiferan tubeworms (Siboglinidae, Polychaeta), that the simultaneous fluorescence in situ hybridization (FISH) of both eukaryotic host and bacterial symbiont cells is possible on a single semi-thin (1 μm) section. This allows the identification of host specimens to species level as well as offering visualization of bacteria distributed within the host tissue. Previously published 18S rRNA host-specific oligonucleotide probes for Riftia pachyptila, Tevnia jerichonana and a newly designed Oasisia alvinae probe, as well as a 16S rRNA probe targeting symbionts found in all host species, were applied. A number of standard fixation and hybridization parameters were tested and optimized for the best possible signal intensity and cellular resolution. Ethanol conserved samples embedded in LR White low viscosity resin yielded the best results with regard to both signal intensity and resolution. We show that extended storage times of specimens does not affect the quality of signals attained by FISH and use our protocol to identify morphologically unidentifiable tubeworm individuals from a small data set, conforming to previous findings in succession studies of the Siboglinidae family.
Charles R. Fisher - One of the best experts on this subject based on the ideXlab platform.
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depth dependent gene flow in gulf of mexico cold seep lamellibrachia tubeworms annelida Siboglinidae
Hydrobiologia, 2014Co-Authors: Dominique A Cowart, Kenneth M. Halanych, Stephen W Schaeffer, Charles R. FisherAbstract:Lamellibrachia vestimentiferan tubeworms form aggregations at hydrocarbon cold seeps in the deep Gulf of Mexico (GoM), creating structures that provide living space for other fauna. In the GoM, three Lamellibrachia taxa vary in morphology and depth ranges: Lamellibrachia luymesi (300–950 m), Lamellibrachia sp. 1 (950–2,604 m), and Lamellibrachia sp. 2 (1,175–3,304 m). While Lamellibrachia sp. 2 is consistently identified as a separate species, L. luymesi and sp. 1 cannot be discriminated using barcoding markers cytochrome oxidase subunit 1 (COI) and large ribosomal subunit rDNA (16S). To determine if limited gene flow was a factor in the formation of these taxa, we employed more quickly evolving markers, including mitochondrial cytochrome B (CYTB), hemoglobin subunit B2 intron (HbB2i), and six polymorphic microsatellites; microsatellites were amplified across 45 L. luymesi and sp. 1 individuals. Additionally, we used microsatellites to ask whether populations of Lamellibrachia sp. 1 and sp. 2 show evidence of significant structure. Despite a lack of resolution seen with CYTB and HbB2i, L. luymesi and sp. 1 form genetically differentiated clusters at the cross-amplified microsatellites. Furthermore, we find no evidence for population structure for either Lamellibrachia sp. 1 or sp. 2 across the GoM.
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restriction to large scale gene flow vs regional panmixia among cold seep escarpia spp polychaeta Siboglinidae
Molecular Ecology, 2013Co-Authors: Dominique A Cowart, Charles R. Fisher, Chunya Huang, Sophie Arnaudhaond, Susan L Carney, Stephen W SchaefferAbstract:The history of colonization and dispersal in fauna distributed among deep-sea chemosynthetic ecosystems remains enigmatic and poorly understood because of an inability to mark and track individuals. A combination of molecular, morphological and environmental data improves understanding of spatial and temporal scales at which panmixia, disruption of gene flow or even speciation may occur. Vestimentiferan tubeworms of the genus Escarpia are important components of deep -sea cold seep ecosystems, as they provide long-term habitat for many other taxa. Three species of Escarpia, Escarpia spicata [Gulf of California (GoC)], Escarpia laminata [Gulf of Mexico (GoM)] and Escarpia southwardae (West African Cold Seeps), have been described based on morphology, but are not discriminated through the use of mitochondrial markers (cytochrome oxidase subunit 1; large ribosomal subunit rDNA, 16S; cytochrome b). Here, we also sequenced the exon-primed intron-crossing Haemoglobin subunit B2 intron and genotyped 28 microsatellites to (i) determine the level of genetic differentiation, if any, among the three geographically separated entities and (ii) identify possible population structure at the regional scale within the GoM and West Africa. Results at the global scale support the occurrence of three genetically distinct groups. At the regional scale among eight sampling sites of E. laminata (n = 129) and among three sampling sites of E. southwardae (n = 80), no population structure was detected. These findings suggest that despite the patchiness and isolation of seep habitats, connectivity is high on regional scales.
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species boundaries of gulf of mexico vestimentiferans polychaeta Siboglinidae inferred from mitochondrial genes
Deep-sea Research Part Ii-topical Studies in Oceanography, 2010Co-Authors: Maria Pia Miglietta, Stéphane Hourdez, Dominique A Cowart, Stephen W Schaeffer, Charles R. FisherAbstract:At least six morphospecies of vestimentiferan tubeworms are associated with cold seeps in the Gulf of Mexico (GOM). The physiology and ecology of the two best-studied species from depths above 1000 m in the upper Louisiana slope (Lamellibrachia luymesi and Seepiophila jonesi) are relatively well understood. The biology of one rare species from the upper slope (escarpiid sp. nov.) and three morphospecies found at greater depths in the GOM (Lamellibrachia sp. 1, L sp. 2, and Escarpia laminata) are not as well understood. Here we address species distributions and boundaries of cold-seep tubeworms using phylogenetic hypotheses based on two mitochondrial genes. Fragments of the mitochondrial large ribosomal subunit rDNA (16S) and cytochrome oxidase subunit I (COI) genes were sequenced for 167 vestimentiferans collected from the GOM and analyzed in the context of other seep vestimentiferans for which sequence data were available. The analysis supported five monophyletic clades of vestimentiferans in the GOM. Intra-clade variation in both genes was very low, and there was no apparent correlation between the within-clade diversity and collection depth or location. Two of the morphospecies of Lamellibrachia from different depths in the GOM could not be distinguished by either mitochondrial gene. Similarly, E. laminata could not be distinguished from other described species of Escarpia from either the west coast of Africa or the eastern Pacific using COI. We suggest that the mitochondrial COI and 16S genes have little utility as barcoding markers for seep vestimentiferan tubeworms.
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horizontal endosymbiont transmission in hydrothermal vent tubeworms
Nature, 2006Co-Authors: Andrea D Nussbaumer, Charles R. Fisher, Monika BrightAbstract:Transmission of obligate bacterial symbionts between generations is vital for the survival of the host. Although the larvae of certain hydrothermal vent tubeworms (Vestimentifera, Siboglinidae) are symbiont-free and possess a transient digestive system, these structures are lost during development, resulting in adult animals that are nutritionally dependent on their bacterial symbionts. Thus, each generation of tubeworms must be newly colonized with its specific symbiont. Here we present a model for tubeworm symbiont acquisition and the development of the symbiont-housing organ, the trophosome. Our data indicate that the bacterial symbionts colonize the developing tube of the settled larvae and enter the host through the skin, a process that continues through the early juvenile stages during which the trophosome is established from mesodermal tissue. In later juvenile stages we observed massive apoptosis of host epidermis, muscles and undifferentiated mesodermal tissue, which was coincident with the cessation of the colonization process. Characterizing the symbiont transmission process in this finely tuned mutualistic symbiosis provides another model of symbiont acquisition and additional insights into underlying mechanisms common to both pathogenic infections and beneficial host-symbiont interactions.
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The color of the trophosome: elemental sulfur distribution in the endosymbionts of Riftia pachyptila (Vestimentifera; Siboglinidae)
Marine Biology, 2004Co-Authors: B. Pflugfelder, Charles R. Fisher, Monika BrightAbstract:Riftia pachyptila Jones, 1981, lives in association with a chemoautotrophic, sulfide-oxidizing γ-Proteobacterium that occurs in a specialized organ, the trophosome. Ultrastructurally different bacterial subpopulations occur in different regions of the trophosome lobules (central rods, median small cocci, peripheral large cocci) and contain vesicles, which have been proposed to be sites of elemental sulfur storage. Differently colored trophosomes have been suggested to reflect different amounts of elemental sulfur in the tissue. In this study, the presence of elemental sulfur (S0) was confirmed in the vesicles of the symbionts of R. pachyptila by electron energy loss spectrography (EELS). The proportion of (two-dimensional) area occupied by sulfur vesicles in the cells was found to be strongly correlated with trophosome color, both in individuals with uniformly colored trophosomes and individuals that exhibited a gradual color change along the length of their trophosomes. Elemental sulfur content was highly variable between individuals from a single collection, suggesting a high degree of microhabitat heterogeneity within vestimentiferan aggregations.
Robert C. Vrijenhoek - One of the best experts on this subject based on the ideXlab platform.
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an inordinate fondness for osedax Siboglinidae annelida fourteen new species of bone worms from california
Zootaxa, 2018Co-Authors: Greg W Rouse, Shana K Goffredi, Shannon B Johnson, Robert C. VrijenhoekAbstract:We incorporate DNA sequences from a comprehensive sampling of taxa to provide an updated phylogeny of Osedax and discuss the remarkable diversity of this clade of siboglinids. We formally describe 14 new species of Osedax from Monterey Bay, California, USA, raising the total number of properly named Osedax species to 25. These new species had formerly been recognized by informal names in various publications, and on GenBank. The descriptions document the occurrence of dwarf males in five of the new species. The distribution for the 19 species of Osedax known to occur in Monterey Bay across depths from 385 to 2898 meters and various bone substrates is documented. The exploitation of extant bird and marine turtle bones by Osedax is reported for the first time .
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the morphological diversity of osedax worm borings annelida Siboglinidae
Journal of the Marine Biological Association of the United Kingdom, 2014Co-Authors: Nicholas D Higgs, Thomas G Dahlgren, Robert C. Vrijenhoek, Adrian G Glover, Yoshihiro Fujiwara, Shannon B Johnson, Craig R Smith, Florence Pradillon, Crispin Ts LittleAbstract:Marine worms in the genus Osedax, have specialized ‘root’ tissues used to bore into the bones of decomposing vertebrate skeletons and obtain nutrition. We investigated the borings of nine Osedax species, using micro computed tomography to quantitatively describe the morphology of the borings and provide three-dimensional reconstructions of the space occupied by Osedax root tissues inside the bone. Each Osedax species displayed a consistent boring morphology in any given bone, but these differed between bones. In bones where multiple species coexisted there was limited evidence for spatial niche partitioning by Osedax root tissues inside the bones investigated here. The new morphological data may be applied to Osedax traces in fossil bones, showing that borings can be used to indicate minimum species richness in these bones.
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Complete mitochondrial genome of the hydrothermal vent tubeworm, Ridgeia piscesae (Polychaeta, Siboglinidae)
Mitochondrial DNA. Part A DNA mapping sequencing and analysis, 2014Co-Authors: Jumin Jun, Yong-jin Won, Robert C. VrijenhoekAbstract:The complete mitochondrial genome of Ridgeia piscesae (Polychaeta, Siboglinidae), one of the dominant taxa in deep-sea hydrothermal vents, is reported here for the first time. The R. piscesae mitogenome is 15,002 bp in total length and includes 13 protein-coding gene sequences, small and large rRNA sequences and 22 tRNA sequences. All genes are encoded on the heavy strand. The mitochondrial genomes of R. piscesae and other six polychaete species have a conserved gene order.
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temporal variation and lack of host specificity among bacterial endosymbionts of osedax bone worms polychaeta Siboglinidae
BMC Evolutionary Biology, 2012Co-Authors: Rahel M Salathe, Robert C. VrijenhoekAbstract:Osedax worms use a proliferative root system to extract nutrients from the bones of sunken vertebrate carcasses. The roots contain bacterial endosymbionts that contribute to the nutrition of these mouthless and gutless worms. The worms acquire these essential endosymbionts locally from the environment in which their larvae settle. Here we report on the temporal dynamics of endosymbiont diversity hosted by nine Osedax species sampled during a three-year investigation of an experimental whale fall at 1820-m depth in the Monterey Bay, California. The host species were identified by their unique mitochondrial COI haplotypes. The endosymbionts were identified by ribotyping with PCR primers specifically designed to target Oceanospirillales. Thirty-two endosymbiont ribotypes associated with these worms clustered into two distinct bacterial ribospecies that together comprise a monophyletic group, mostly restricted to deep waters (>1000 m). Statistical analyses confirmed significant changes in the relative abundances of host species and the two dominant endosymbiont ribospecies during the three-year sampling period. Bone type (whale vs. cow) also had a significant effect on host species, but not on the two dominant symbiont ribospecies. No statistically significant association existed between the host species and endosymbiont ribospecies. Standard PCR and direct sequencing proved to be an efficient method for ribotyping the numerically dominant endosymbiont strains infecting a large sample of host individuals; however, this method did not adequately represent the frequency of mixed infections, which appears to be the rule rather than an exception for Osedax individuals. Through cloning and the use of experimental dilution series, we determined that minority ribotypes constituting less than 30% of a mixture would not likely be detected, leading to underestimates of the frequency of multiple infections in host individuals.
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high diversity of frenulates polychaeta Siboglinidae in the gulf of cadiz mud volcanoes a dna taxonomy analysis
Deep Sea Research Part I: Oceanographic Research Papers, 2010Co-Authors: Ana Hilário, Shannon B Johnson, Marina R. Cunha, Robert C. VrijenhoekAbstract:Abstract Frenulates are the most poorly known members of the family Siboglinidae (Polychaeta: Canalipalpata). These thread-like worms occur in reducing marine sediments worldwide, but they are often overlooked in benthic samples or too poorly preserved for adequate taxonomic evaluations. We report on a remarkable diversity of frenulates that were recently sampled from 13 mud volcanoes (350–3902 m deep) in the Gulf of Cadiz, off southern Iberia. Sampled with benthic coring devices, the bodies of these long tubiculous worms were often broken or incomplete, making them difficult to identify morphologically. Consequently, we employed DNA taxonomic methods to assess their diversity. Mitochondrial cytochrome-c-oxidase subunit 1 (COI) sequences distinguished 15 evolutionary lineages inhabiting the Gulf of Cadiz. Only four of the lineages could be assigned to currently recognized Atlantic species; the remaining 11 may be new to science. This remarkable diversity of frenulates in a small geographical region is unprecedented and is hypothesized to result from environmental heterogeneity associated with the bathymetric and geochemical settings of these mud volcanoes.
Kenneth M. Halanych - One of the best experts on this subject based on the ideXlab platform.
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The mitochondrial genome of the bone-eating worm Osedaxrubiplumus(Annelida, Siboglinidae)
Mitochondrial DNA. Part B Resources, 2020Co-Authors: Yadong Zhou, Kenneth M. Halanych, Hong Cheng, Chunsheng WangAbstract:Osedaxrubiplumus(Annelida, Siboglinidae)uses heterotrophic bacteria to feed onvertebrate carcasses and is currently found in the Pacific, Antarctic and Indian Ocean.Here, we report its nearly compl...
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phylogenomics of tubeworms Siboglinidae annelida and comparative performance of different reconstruction methods
Zoologica Scripta, 2017Co-Authors: Daniel J. Thornhill, Kevin M Kocot, Nathan V Whelan, Scott R Santos, Damien S Waits, Kenneth M. HalanychAbstract:Deep-sea tubeworms (Annelida, Siboglinidae) represent dominant species in deep-sea chemosynthetic communities (e.g. hydrothermal vents and cold methane seeps) and occur in muddy sediments and organic falls. Siboglinids lack a functional digestive tract as adults, and they rely on endosymbiotic bacteria for energy, making them of evolutionary and physiological interest. Despite their importance, inferred evolutionary history of this group has been inconsistent among studies based on different molecular markers. In particular, placement of bone-eating Osedax worms has been unclear in part because of their distinctive biology, including harbouring heterotrophic bacteria as endosymbionts, displaying extreme sexual dimorphism and exhibiting a distinct body plan. Here, we reconstructed siboglinid evolutionary history using 12 newly sequenced transcriptomes. We parsed data into three data sets that accommodated varying levels of missing data, and we evaluate effects of missing data on phylogenomic inference. Additionally, several multispecies-coalescent approaches and Bayesian concordance analysis (BCA) were employed to allow for a comparison of results to a supermatrix approach. Every analysis conducted herein strongly supported Osedax being most closely related to the Vestimentifera and Sclerolinum clade, rather than Frenulata, as previously reported. Importantly, unlike previous studies, the alternative hypothesis that frenulates and Osedax are sister groups to one another was explicitly rejected by an approximately unbiased (AU) test. Furthermore, although different methods showed largely congruent results, we found that a supermatrix method using data partitioning with site-homogenous models potentially outperformed a supermatrix method using the CAT-GTR model and multispecies-coalescent approaches when the amount of missing data varies in a data set and when taxa susceptible to LBA are included in the analyses.
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mitogenomics reveals phylogeny and repeated motifs in control regions of the deep sea family Siboglinidae annelida
Molecular Phylogenetics and Evolution, 2015Co-Authors: Daniel J. Thornhill, Christoffer Schander, Kevin M Kocot, Scott R Santos, Kenneth M. HalanychAbstract:Deep-sea tubeworms in the annelid family Siboglinidae have drawn considerable interest regarding their ecology and evolutionary biology. As adults, they lack a digestive tract and rely on endosymbionts for nutrition. Moreover, they are important members of chemosynthetic environments including hydrothermal vents, cold seeps, muddy sediments, and whale bones. Evolution and diversification of siboglinids has been associated with host-symbiont relationships and reducing habitats. Despite their importance, the taxonomy and phylogenetics of this clade are debated due to conflicting results. In this study, 10 complete and 2 partial mitochondrial genomes and one transcriptome were sequenced and analyzed to address siboglinid evolution. Notably, repeated nucleotide motifs were found in control regions of these mt genomes, which may explain previous challenges of sequencing siboglinid mt genomes. Phylogenetic analyses of amino acid and nucleotide datasets were conducted in order to infer evolutionary history. Both analyses generally had strong nodal support and suggest Osedax is most closely related to the Vestimentifera + Sclerolinum clade, rather than Frenulata, as recently reported. These results imply Osedax, the only siboglinid lineage with heterotrophic endosymbionts, evolved from a lineage utilizing chemoautotrophic symbionts.
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depth dependent gene flow in gulf of mexico cold seep lamellibrachia tubeworms annelida Siboglinidae
Hydrobiologia, 2014Co-Authors: Dominique A Cowart, Kenneth M. Halanych, Stephen W Schaeffer, Charles R. FisherAbstract:Lamellibrachia vestimentiferan tubeworms form aggregations at hydrocarbon cold seeps in the deep Gulf of Mexico (GoM), creating structures that provide living space for other fauna. In the GoM, three Lamellibrachia taxa vary in morphology and depth ranges: Lamellibrachia luymesi (300–950 m), Lamellibrachia sp. 1 (950–2,604 m), and Lamellibrachia sp. 2 (1,175–3,304 m). While Lamellibrachia sp. 2 is consistently identified as a separate species, L. luymesi and sp. 1 cannot be discriminated using barcoding markers cytochrome oxidase subunit 1 (COI) and large ribosomal subunit rDNA (16S). To determine if limited gene flow was a factor in the formation of these taxa, we employed more quickly evolving markers, including mitochondrial cytochrome B (CYTB), hemoglobin subunit B2 intron (HbB2i), and six polymorphic microsatellites; microsatellites were amplified across 45 L. luymesi and sp. 1 individuals. Additionally, we used microsatellites to ask whether populations of Lamellibrachia sp. 1 and sp. 2 show evidence of significant structure. Despite a lack of resolution seen with CYTB and HbB2i, L. luymesi and sp. 1 form genetically differentiated clusters at the cross-amplified microsatellites. Furthermore, we find no evidence for population structure for either Lamellibrachia sp. 1 or sp. 2 across the GoM.
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Integrative and Comparative Biology Advance Access published June 30, 2006 A review of molecular markers used for Annelid phylogenetics
2014Co-Authors: Kenneth M. Halanych, Alexis M. JanosikAbstract:Synopsis Annelida, one of the most successful animal phyla, exhibits an amazing variety of morphological forms. Disparity between some of the forms is so great that until molecular tools were used, some annelid lineages (for example, echiurids and pogonophorans) were not commonly recognized as belonging to the group. Although it is easy to assign annelids to a given family, understanding the deeper relationships within the group has been difficult. The main working hypothesis for annelid phylogeny is based on morphological cladistic analysis. However, the recent work using molecular tools has caused a revision of our view of annelid evolutionary history. For example, Scolecida and Palpata appear not to be natural groups, and the phylogenetic positions of some aberrant taxa (for example, Siboglinidae, Poeobius, Pisione) have been determined. Herein, we discuss some of the main molecular markers that have been used to elucidate annelid phylogeny and the contribution that such work is making to our understanding. A table highlighting the molecular literature and the genes used is included. Annelida is one of the most successful major animal lineages. Segmented worms, with over 16,500 recognized species (Brusca and Brusca 2003), are one of the dominant fauna in most marine habitats and have successfully radiated into fresh water and terrestrial environments. Despite their success and ecologica