Reduced Genome of the Thioautotrophic Intracellular Symbiont in a Deep-Sea Clam, Calyptogena okutanii

Kuwahara, Hiroya; Yoshida, Takao; Takaki, Yoshihiro; Shimamura, Shigeru; Nishi, Shinro; Harada, Maiko; Matsuyama, Kazuyo; Takishita, Kiyotaka; Kawato, Masaru; Uematsu, Katsuyuki; Fujiwara, Yoshihiro; Sato, Takako; Kato, Chiaki; Kitagawa, Masanari; Kato, Ikuo; Maruyama, Tadashi

doi:10.1016/j.cub.2007.04.039

Cited by 170 publications

(211 citation statements)

References 18 publications

(19 reference statements)

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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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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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“…Genome reduction is typically biased towards loss of genes that are clearly dispensable in an intracellular environment, and also loss of regulatory functions, biosynthetic pathways for metabolites provided by the host cell, DNA repair capacities and transport functions (e.g. Shigenobu et al 2000;Akman et al 2002;Gil et al 2003;Kuwahara et al 2007). The same features generally apply also for the bacterial endosymbionts of protists.…”

Section: Prokaryotic Endosymbionts In Protists (A) Photosynthetic Endmentioning

confidence: 99%

Endosymbiotic associations within protists

Nowack

Melkonian

2010

Phil. Trans. R. Soc. B

204

160

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The establishment of an endosymbiotic relationship typically seems to be driven through complementation of the host's limited metabolic capabilities by the biochemical versatility of the endosymbiont. The most significant examples of endosymbiosis are represented by the endosymbiotic acquisition of plastids and mitochondria, introducing photosynthesis and respiration to eukaryotes. However, there are numerous other endosymbioses that evolved more recently and repeatedly across the tree of life. Recent advances in genome sequencing technology have led to a better understanding of the physiological basis of many endosymbiotic associations. This review focuses on endosymbionts in protists (unicellular eukaryotes). Selected examples illustrate the incorporation of various new biochemical functions, such as photosynthesis, nitrogen fixation and recycling, and methanogenesis, into protist hosts by prokaryotic endosymbionts. Furthermore, photosynthetic eukaryotic endosymbionts display a great diversity of modes of integration into different protist hosts.In conclusion, endosymbiosis seems to represent a general evolutionary strategy of protists to acquire novel biochemical functions and is thus an important source of genetic innovation.

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“…Among the most active and abundant microorganisms in GB plumes are sulfur-oxidizing bacteria of the SUP05 group of Gammaproteobacteria (13, 16). SUP05 are dominant members of microbial communities in diverse marine environments such as hydrothermal vent plumes, symbiotic associations with hydrothermal vent clams and mussels, and oxygen minimum zones (OMZs) across the world's oceans (9,(17)(18)(19)(20)(21)(22).In the present study, we use a combination of DNA, cDNA, small subunit ribosomal RNA (SSU rRNA) amplicon sequencing, and thermodynamic/bioenergetic modeling to elucidate the genetic potential, transcriptional activity, and distribution of two uncultivated lineages of SUP05 bacteria in hydrothermal plumes and surrounding deep-sea waters. We report evidence for H 2 oxidation as an important source of electrons for microbial growth in the deep oceanic water column and suggest that the SUP05 group displays metabolic plasticity that underlies the phylogenetic diversity of these widespread bacteria.…”

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Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria

Anantharaman¹,

Breier

Sheik³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

171

206

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Hydrothermal vents are a well-known source of energy that powers chemosynthesis in the deep sea. Recent work suggests that microbial chemosynthesis is also surprisingly pervasive throughout the dark oceans, serving as a significant CO 2 sink even at sites far removed from vents. Ammonia and sulfur have been identified as potential electron donors for this chemosynthesis, but they do not fully account for measured rates of dark primary production in the pelagic water column. Here we use metagenomic and metatranscriptomic analyses to show that deep-sea populations of the SUP05 group of uncultured sulfur-oxidizing Gammaproteobacteria, which are abundant in widespread and diverse marine environments, contain and highly express genes encoding group 1 Ni, Fe hydrogenase enzymes for H 2 oxidation. Reconstruction of near-complete genomes of two cooccurring SUP05 populations in hydrothermal plumes and deep waters of the Gulf of California enabled detailed population-specific metatranscriptomic analyses, revealing dynamic patterns of gene content and transcript abundance. SUP05 transcripts for genes involved in H 2 and sulfur oxidation are most abundant in hydrothermal plumes where these electron donors are enriched. In contrast, a second hydrogenase has more abundant transcripts in background deep-sea samples. Coupled with results from a bioenergetic model that suggest that H 2 oxidation can contribute significantly to the SUP05 energy budget, these findings reveal the potential importance of H 2 as a key energy source in the deep ocean. This study also highlights the genomic plasticity of SUP05, which enables this widely distributed group to optimize its energy metabolism (electron donor and acceptor) to local geochemical conditions. Guaymas | oxygen minimum zone D eep-sea hydrothermal vent ecosystems depend on microorganisms that use reduced chemicals such as sulfur, methane, ammonium, and H 2 as electron donors for chemosynthesis (1-5). Recent work suggests that microbial chemosynthesis is also far more prevalent in the broader deep oceans than previously recognized, extending throughout the water column of the dark open ocean, where it serves as a significant source of organic carbon (6, 7). The fuels for this pelagic primary production remain unknown, but recent studies show that ammonium (3) and sulfur (8, 9) are potential electron donors in the water column. H 2 , long known as an energy source for free-living bacteria in seafloor hydrothermal systems, was also recently identified as an electron donor in hydrothermal vent animal symbioses (4). Although microbial communities at seafloor hydrothermal vent sites have attracted much attention, hydrothermal vent plumes remain poorly characterized despite their importance as habitats for free-living chemolithoautotrophs (10). These plume microorganisms mediate the hydrothermal transfer of elements from the lithosphere to the oceans (11, 12) and contribute significantly to organic carbon in the deep oceans via carbon fixation (1, 13-15).We investigated hydrothermal vent ...

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Reduced Genome of the Thioautotrophic Intracellular Symbiont in a Deep-Sea Clam, Calyptogena okutanii

Cited by 170 publications

References 18 publications

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

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

Endosymbiotic associations within protists

Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria

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