Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California

Whale-falls represent localized areas of extreme organic enrichment in an otherwise oligotrophic deep-sea environment. Anaerobic remineralization within these habitats is typically portrayed as sulfidogenic; however, we demonstrate that these systems are also favorable for diverse methaneproducing archaeal assemblages, representing up to 40% of total cell counts. Chemical analyses revealed elevated methane and depleted sulfate concentrations in sediments under the whale-fall, as compared to surrounding sediments. Carbon was enriched (up to 3.5%) in whale-fall sediments, as well as the surrounding sea floor to at least 10 m, forming a 'bulls eye' of elevated carbon. The diversity of sedimentary archaea associated with the 2893 m whale-fall in Monterey Canyon (California) varied both spatially and temporally. 16S rRNA diversity, determined by both sequencing and terminal restriction fragment length polymorphism analysis, as well as quantitative PCR of the methyl-coenzyme M reductase gene, revealed that methanogens, including members of the Methanomicrobiales and Methanosarcinales, were the dominant archaea (up to 98%) in sediments immediately beneath the whale-fall. Temporal changes in this archaeal community included the early establishment of methylotrophic methanogens followed by development of methanogens thought to be hydrogenotrophic, as well as members related to the newly described methanotrophic lineage, ANME-3. In comparison, archaeal assemblages in 'reference' sediments collected 10 m from the whale-fall primarily consisted of Crenarchaeota affiliated with marine group I and marine benthic group B. Overall, these results indicate that whale-falls can favor the establishment of metabolically and phylogenetically diverse methanogen assemblages, resulting in an active near-seafloor methane cycle in the deep sea.

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“…The whale-fall was originally discovered in February 2002 (Goffredi et al, 2004;36.781N/122.081W, 2893 m depth; Figure 1a (Braby et al, 2007).…”

Section: Methodsmentioning

confidence: 99%

Temporal evolution of methane cycling and phylogenetic diversity of archaea in sediments from a deep-sea whale-fall in Monterey Canyon, California

et al. 2008

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“…These spatially heterogeneous and enriched habitats persist for varying timespans of 5 to 50 years, depending on a number of conditions (for example, depth and oxygen concentrations; Smith and Baco, 2003;Goffredi et al, 2004;Braby et al, 2007;Lundsten et al, 2010). Many organisms, both animals and free-living microbes, tend to be stratified in space and time around the decomposing carcasses (Smith et al, 2002;Goffredi et al, 2004;Braby et al, 2007;Goffredi et al, 2008;Vrijenhoek et al, 2009;Goffredi and Orphan, 2010;Lundsten et al, 2010).…”

Section: Genomic Implications For Intracellular Lifementioning

confidence: 99%

“…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%

“…Now, 17 morphologically diverse species are known worldwide from depths ranging from 25 to 3000 meters Rouse et al, 2004;Glover et al, 2005;Fujikura et al, 2006;Braby et al, 2007;Vrijenhoek et al, 2009;Salathé and Vrijenhoek, 2012). 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).…”

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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“…The enigmatic polychaete genus Osedax is now thought to consist of at least 11 known species recorded from the depths of 30-2900 m in both the Atlantic and Pacific oceans (Dahlgren et al 2006;Braby et al 2007;Jones et al 2008;Rouse et al 2008). Osedax presents a biogeographic paradox.…”

mentioning

confidence: 99%

On the role of bone-eating worms in the degradation of marine vertebrate remains

et al. 2008

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Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California

Cited by 156 publications

References 19 publications

Temporal evolution of methane cycling and phylogenetic diversity of archaea in sediments from a deep-sea whale-fall in Monterey Canyon, California

Temporal evolution of methane cycling and phylogenetic diversity of archaea in sediments from a deep-sea whale-fall in Monterey Canyon, California

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

On the role of bone-eating worms in the degradation of marine vertebrate remains

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