The
            <i>Calyptogena magnifica</i>
            Chemoautotrophic Symbiont Genome

Newton, Irene L. G.; Woyke, Tanja; Auchtung, Thomas A.; Dilly, Geoffrey F.; Dutton, Rachel J.; Fisher, Meredith C.; Fontanez, Kristina M.; Lau, Evan; Stewart, Frank J.; Richardson, Paul M.; Barry, Kerrie; Saunders, Elizabeth; Detter, John C.; Wu, Dongying; Eisen, Jonathan A.; Cavanaugh, Colleen M.

doi:10.1126/science.1138438

Cited by 193 publications

(239 citation statements)

References 22 publications

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“…SUP05 is abundant in oxic/anoxic interfacial environments such as deep-sea hydrothermal plumes (Sunamura et al, 2004;Dick and Tebo, 2010;German et al, 2010), oxygen minimum zones (Stevens and Ulloa, 2008;Lavik et al, 2009;Walsh et al, 2009;Canfield et al, 2010) and symbioses with deep-sea bivalves (Newton et al, 2007). Our data set supports previous genomic studies that showed that members of this group are chemolithoautotrophic, obtaining energy by coupling sulfur oxidation to reduction of nitrate and/or oxygen (Newton et al, 2007;Walsh et al, 2009). The increased abundance of SUP05 sox gene transcripts in the Guaymas Basin plume-among the most plume-enriched genes in the metatranscriptome-provides evidence that SUP05 responds to reduced sulfur compounds commonly found within the plume environment (Figure 2).…”

Section: Discussionmentioning

confidence: 99%

The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs

et al. 2012

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Microorganisms mediate geochemical processes in deep-sea hydrothermal vent plumes, which are a conduit for transfer of elements and energy from the subsurface to the oceans. Despite this important microbial influence on marine geochemistry, the ecology and activity of microbial communities in hydrothermal plumes is largely unexplored. Here, we use a coordinated metagenomic and metatranscriptomic approach to compare microbial communities in Guaymas Basin hydrothermal plumes to background waters above the plume and in the adjacent Carmen Basin. Despite marked increases in plume total RNA concentrations (3-4 times) and microbially mediated manganese oxidation rates (15-125 times), plume and background metatranscriptomes were dominated by the same groups of methanotrophs and chemolithoautotrophs. Abundant community members of Guaymas Basin seafloor environments (hydrothermal sediments and chimneys) were not prevalent in the plume metatranscriptome. De novo metagenomic assembly was used to reconstruct genomes of abundant populations, including Marine Group I archaea, Methylococcaceae, SAR324 Deltaproteobacteria and SUP05 Gammaproteobacteria. Mapping transcripts to these genomes revealed abundant expression of genes involved in the chemolithotrophic oxidation of ammonia (amo), methane (pmo) and sulfur (sox). Whereas amo and pmo gene transcripts were abundant in both plume and background, transcripts of sox genes for sulfur oxidation from SUP05 groups displayed a 10-20-fold increase in plumes. We conclude that the biogeochemistry of Guaymas Basin hydrothermal plumes is mediated by microorganisms that are derived from seawater rather than from seafloor hydrothermal environments such as chimneys or sediments, and that hydrothermal inputs serve as important electron donors for primary production in the deep Gulf of California.

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Section: Discussionmentioning

confidence: 99%

The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs

et al. 2012

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“…Peptide sequence from SUP05-derived Dsr proteins were used as query in similarity searches against the NCBI nr-protein database. The only sequences that were 100% identical to the peptides were from the SUP05-related sulfur-oxidizing symbionts of deep-sea clams and mussels (Kuwahara et al, 2007;Newton et al, 2007) and Dsr sequences recovered from an oxygen minimum zone . Five of the six peptides from SUP05-related SoxA and SoxB were also specific to SUP05 proteins.…”

Section: Metabolism Of the Sup05 Cladementioning

confidence: 99%

Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton

et al. 2014

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In this study, we used comparative metaproteomics to investigate the metabolic activity of microbial plankton inhabiting a seasonally hypoxic basin in the Northwest Atlantic Ocean (Bedford Basin). From winter to spring, we observed a seasonal increase in high-affinity membrane transport proteins involved in scavenging of organic substrates; Rhodobacterales transporters were strongly associated with the spring phytoplankton bloom, whereas SAR11 transporters were abundant in the underlying waters. A diverse array of transporters for organic compounds were similar to the SAR324 clade, revealing an active heterotrophic lifestyle in coastal waters. Proteins involved in methanol oxidation (from the OM43 clade) and carbon monoxide (from a wide variety of bacteria) were identified throughout Bedford Basin. Metabolic niche partitioning between the SUP05 and ARCTIC96BD-19 clades, which together comprise the Gamma-proteobacterial sulfur oxidizers group was apparent. ARCTIC96BD-19 proteins involved in the transport of organic compounds indicated that in productive coastal waters this lineage tends toward a heterotrophic metabolism. In contrast, the identification of sulfur oxidation proteins from SUP05 indicated the use of reduced sulfur as an energy source in hypoxic bottom water. We identified an abundance of Marine Group I Thaumarchaeota proteins in the hypoxic deep layer, including proteins for nitrification and carbon fixation. No transporters for organic compounds were detected among the thaumarchaeal proteins, suggesting a reliance on autotrophic carbon assimilation. In summary, our analyses revealed the spatiotemporal structure of numerous metabolic activities in the coastal ocean that are central to carbon, nitrogen and sulfur cycling in the sea.

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“…The Osedax symbionts possess many genes devoted to the specific degradation of branched-chain amino acids, which also results in the generation of propionyl-CoA, rather than acetyl-CoA (Muñ oz-Elías et al, 2006), thus increasing the necessity for the methylcitrate cycle. The observation of genes for these two TCA shunts in both Osedax symbionts, as well as in the marine bivalve symbiont, Ruthia magnifica (Newton et al, 2007), suggests that they, too, may be important for intracellular life. Again, however, a more thorough comparison between heterotrophic symbionts and pathogens is critical to our understanding of the relative importance of these pathways for symbiosis.…”

Section: Genomic Implications For Intracellular Lifementioning

confidence: 99%

“…New details have emerged regarding the range of adaptations used by endosymbionts, parallels with pathogens, provisioning from symbiont to host and many ecological aspects, including transmission between host generations and the duality of negotiating between host-associated and free-living lifestages. Recent advances in molecular biology and genomics have enabled this insight for chemosynthetic symbionts, in particular, hosted by the marine oligochaete Olavius algarvensis (Woyke et al, 2006), vesicomyid clam species (Kuwahara et al, 2007;Newton et al, 2007), the siboglinid tubeworm Riftia pachyptila (Robidart et al, 2008) and the heterotrophic symbionts of wood-boring bivalves (Yang et al, 2009). …”

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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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 Calyptogena magnifica Chemoautotrophic Symbiont Genome

Cited by 193 publications

References 22 publications

The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs

The metatranscriptome of a deep-sea hydrothermal plume is dominated by water column methanotrophs and lithotrophs

Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton

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

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