New Perspectives on the Ecology and Evolution of Siboglinid Tubeworms

Hilario, Ana Belén Ríos; Capa, María; Dahlgren, Thomas G.; Halanych, Kenneth M.; Little, Crispin T. S.; Thornhill, Daniel J.; Verna, Caroline; Glover, Adrian G.

doi:10.1371/journal.pone.0016309

Cited by 148 publications

(128 citation statements)

References 123 publications

(202 reference statements)

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“…Lack of CO 2 fixation genes supports early evidence of the heterotrophic nature of the Osedax symbionts and confirms their unusual divergence from the typical chemosynthetic lifestyle of all other related siboglinids (Naganuma et al, 2005;Thornhill et al, 2008;Hilário et al, 2011). Consistent with possible exposure to variable chemical regimes, and heterotrophy, the transport profile of the Osedax symbionts indicates flexibility in the types of compounds brought into the cell.…”

Section: Metabolic Flexibilitysupporting

confidence: 56%

“…Evidence for Osedax borings in fossilized bones suggests that the genus has historically colonized a large portion of the world's oceans (Higgs et al, 2011;Kiel et al, 2011;Higgs et al, 2012). Much is now known about the role of these worms in degrading sunken bones and the recycling of deep-sea carbon (Goffredi et al, 2005;Braby et al, 2007), their phylogenetic relationships (Vrijenhoek et al, 2009;Hilário et al, 2011), and an unusual reproductive strategy that involves dwarf males and environmental sex determination Vrijenhoek et al, 2008;Rouse et al, 2011;Miyamoto et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

Goffredi

Zhang

et al. 2013

The ISME Journal

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An unusual symbiosis, first observed at B3000 m depth in the Monterey Submarine Canyon, involves gutless marine polychaetes of the genus Osedax and intracellular endosymbionts belonging to the order Oceanospirillales. Ecologically, these worms and their microbial symbionts have a substantial role in the cycling of carbon from deep-sea whale fall carcasses. Microheterogeneity exists among the Osedax symbionts examined so far, and in the present study the genomes of the two dominant symbionts, Rs1 and Rs2, were sequenced. The genomes revealed heterotrophic versatility in carbon, phosphate and iron uptake, strategies for intracellular survival, evidence for an independent existence, and numerous potential virulence capabilities. The presence of specific permeases and peptidases (of glycine, proline and hydroxyproline), and numerous peptide transporters, suggests the use of degraded proteins, likely originating from collagenous bone matter, by the Osedax symbionts. 13 C tracer experiments confirmed the assimilation of glycine/ proline, as well as monosaccharides, by Osedax. The Rs1 and Rs2 symbionts are genomically distinct in carbon and sulfur metabolism, respiration, and cell wall composition, among others. Differences between Rs1 and Rs2 and phylogenetic analysis of chemotaxis-related genes within individuals of symbiont Rs1 revealed the influence of the relative age of the whale fall environment and support possible local niche adaptation of 'free-living' lifestages. Future genomic examinations of other horizontally-propogated intracellular symbionts will likely enhance our understanding of the contribution of intraspecific symbiont diversity to the ecological diversification of the intact association, as well as the maintenance of host diversity.

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Section: Metabolic Flexibilitysupporting

confidence: 56%

Section: Introductionmentioning

confidence: 99%

Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

Goffredi

Zhang

et al. 2013

The ISME Journal

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“…This species is also the only animal seen at the site that could 10 possibly be a seep obligate species. However, the generalist lifestyle of frenulates (Hilário et al, 2011;Southward, 2000;Southward et al, 2005) and the debate around the consideration of O. haakonmosbiensis as a separate species from the fjord frenulate Oligobrachia webbi (Meunier et al, 2010), means that it is possible that, despite the cold seep setting, the entire pingo community consists solely of background benthic species, regardless of whether community members are chemosynthesis based or conventionally heterotrophic. Nonetheless, the animals at the study site appear to take advantage of, 15…”

Section: Community Characteristicsmentioning

confidence: 99%

“…All frenulates have obligate, nutritional symbiotic associations with bacterial endosymbionts (Fisher, 1990;Hilário et al, 2011;Southward, 1982;Southward et al, 2005) and molecular data and electron micrographs suggest that thiotrophy is the dominant metabolic mode for symbionts of O. haakonmosbiensis (Lösekann et al, 2008;Pimenov et al, 30 2000). Thus we expected sediment sulfide concentrations at GHP5 to be lower than those at the other pingos, and too low to sustain the frenulate worms and their symbionts.…”

Section: Factors Controlling the Distribution Of Chemosynthesis Basedmentioning

confidence: 99%

Geophysical and geochemical controls on the megafaunal community of a high Arctic cold seep

Sen¹,

Åström²,

Hong³

et al. 2018

Preprint

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Cold seep communities around gas hydrate mounds (pingos) in the Western Barents Sea (76°N, 16°E, ~400 m depth) were investigated with high resolution, geographically referenced images acquired with an ROV and towed camera. Four pingos associated with seabed methane release hosted diverse biological communities of mainly non-seep (background) species including commercially important fish and crustaceans, as well as a species new to this area (the snow crab Chionoecetes 15 opilio). We attribute the presence of most benthic community members to habitat heterogeneity and the occurrence of hard substrates (methane derived authigenic carbonates), particularly the most abundant phyla (Cnidaria and Porifera), though food availability and exposure to a diverse microbial community is also important for certain taxa. Only one chemosynthesis based species was confirmed, the siboglinid frenulate polychaete, Oligobrachia haakonmosbiensis. Overall, the pingo communities formed two distinct clusters, distinguished by the presence or absence of frenulates. Methane gas advection through sediments 20 was absent below the single pingo that lacked frenulates, while seismic profiles indicated gas saturated sediment below the other frenulate colonized pingos. The absence of frenulates could not be explained by sediment sulfide concentrations, despite these worms likely containing sulfide oxidizing symbionts. We propose that high levels of seafloor methane seepage linked to sub-surface gas reservoirs support an abundant and active sediment methanotrophic community that maintains high sulfide fluxes and serves as a carbon source for frenulate worms. The pingo currently lacking a sub-surface gas source and lower 25 methane concentrations has lower sulfide flux rates and limited amounts of carbon insufficient to support frenulates. Two previously undocumented behaviors were visible through the images: grazing activity of snow crabs on bacterial mats, and seafloor crawling of Nothria conchylega onuphid polychaetes.Biogeosciences Discuss., https://doi

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“…Lonsdale, 1977;Van Dover, 2000) and whale falls (Smith and Baco, 2003) are characterized by distinct biota, largely different from that of the surrounding marine environments (Levin, 2005). The large concentrations of reduced compounds available at these sites, chiefly sulphides and to a lesser extent methane, sustain mass accumulations of chemosymbiotic fauna, such as solemyid, lucinid, thyasirid and vesicomyid clams, and bathymodiolin mussels (Métiver & Cosel, 1993;Sibuet and Olu, 1998;Fujikura et al, 1999;Glover et al, 2004;Taylor and Glover, 2010;Krylova et al, 2011), large abyssochrysoid gastropods (Kojima et al, 2001;Sasaki et al, 2010) and siboglinid tubeworms (Hilário et al, 2011). Additionally, exposed hard substrates provide attachment opportunities for hard-substrate dwellers, such as serpulid polychaetes, and sea anemones (e.g.…”

Section: Introductionmentioning

confidence: 99%

Late Jurassic–Early Cretaceous hydrocarbon seep boulders from Novaya Zemlya and their faunas

Hryniewicz

Hagström

Hammer

et al. 2015

Palaeogeography, Palaeoclimatology, Palaeoecology

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The paper describes Late Jurassic-Early Cretaceous seep carbonate boulders from the Russian Arctic island of Novaya Zemlya, collected in 1875 by A.E. Nordenskiöld during his expedition to Siberia. The carbonates are significantly depleted in heavy carbon isotopes Other seep faunas with similar taxonomic structure are suggestive of rather shallow water settings, but in case of Novaya Zemlya seep faunas such structure might result also from high northern latitude.

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New Perspectives on the Ecology and Evolution of Siboglinid Tubeworms

Cited by 148 publications

References 123 publications

Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

Geophysical and geochemical controls on the megafaunal community of a high Arctic cold seep

Late Jurassic–Early Cretaceous hydrocarbon seep boulders from Novaya Zemlya and their faunas

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