Geochemical study of the bathyal seep communities at the Hatsushima site, Sagami Bay, Central Japan.

Sakai, Hitoshi; Gamo, Toshitaka; Endow, K.; Ishibashi, Jun Ichiro; Ishizuka, T.; Yanagisawa, Fumitaka; Kusakabe, Minoru; Akagi, Tetsuya; Igarashi, George; Ohta, Suguru

doi:10.2343/geochemj.21.227

Cited by 29 publications

(23 citation statements)

References 20 publications

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“…One possible explanation for this result is that this clam species may bear a methanotrophic symbiont, which may assimilate carbon via non-RuBisCO pathways. The occurrence of RuBisCO in the current tubeworm rather than in the clam may be correlated with the geochemical characters of this methane seep, where it has abundant methane in ambient water and sediment but has available hydrogen sulfide only in sediment (59). The seep-dwelling tubeworm Lamellibrachia sp.…”

Section: Resultsmentioning

confidence: 99%

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Phylogenetic Diversity of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Large-Subunit Genes from Deep-Sea Microorganisms

Elsaied

Naganuma

2001

Appl Environ Microbiol

126

132

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The phylogenetic diversity of the ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO, E.C. 4.1.1.39) large-subunit genes of deep-sea microorganisms was analyzed. Bulk genomic DNA was isolated from seven samples, including samples from the Mid-Atlantic Ridge and various deep-sea habitats around Japan. The kinds of samples were hydrothermal vent water and chimney fragment; reducing sediments from a bathyal seep, a hadal seep, and a presumed seep; and symbiont-bearing tissues of the vent mussel, Bathymodiolus sp., and the seep vestimentiferan tubeworm, Lamellibrachia sp. The RuBisCO genes that encode both form I and form II large subunits (cbbL and cbbM) were amplified by PCR from the seven deep-sea sample DNA populations, cloned, and sequenced. From each sample, 50 cbbL clones and 50 cbbM clones, if amplified, were recovered and sequenced to group them into operational taxonomic units (OTUs). A total of 29 OTUs were recorded from the 300 total cbbL clones, and a total of 24 OTUs were recorded from the 250 total cbbM clones. All the current OTUs have the characteristic RuBisCO amino acid motif sequences that exist in other RuBisCOs. The recorded OTUs were related to different RuBisCO groups of proteobacteria, cyanobacteria, and eukarya. The diversity of the RuBisCO genes may be correlated with certain characteristics of the microbial habitats. The RuBisCO sequences from the symbiont-bearing tissues showed a phylogenetic relationship with those from the ambient bacteria. Also, the RuBisCO sequences of known species of thiobacilli and those from widely distributed marine habitats were closely related to each other. This suggests that the Thiobacillus-related RuBisCO may be distributed globally and contribute to the primary production in the deep sea.Phylogenetic information on deep-sea microorganisms that has been accumulated relates mainly to the 16S ribosomal DNA (rDNA) sequences (9,33,53). In understanding the microbial contribution to deep-sea primary production, the 16S rDNA-based phylogeny will be better complemented by knowledge of the genes encoding the enzymes relevant to carbon fixation. The genes encoding ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) represent such an enzyme that is involved in autotrophy. RuBisCO is the most abundant enzyme on the globe and has attracted much phylogenetic attention (5). RuBisCO catalyzes the assimilation of carbon dioxide to organic carbon via the Calvin-Benson cycle. The enzyme consists of large and small subunits (42). The site responsible for carbon fixation is in the large subunit (42). More than 20% of the amino acid residues in the large subunit are conserved among the higher plants (32). Generally, RuBisCO has two forms. Form I consists of large and small subunits (L n S n , typically L 8 S 8 ), and form II contains only large subunits (L n ) with 25 to 30% amino acid sequence identity with those of form I (32). The large subunits of form I and form II are coded by genes designated cbbL and cbbM, respectively (37). Some organisms have two genes en...

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Section: Resultsmentioning

confidence: 99%

“…High abundance of H 2 S over other reducing inorganic materials in the deep sea (29,31,59,74) and dual possession of RuBisCO forms I and II (11,36,64) facilitate this global distribution of thiobacilli and make free-living and symbiotic thiobacilli the major primary producers in the deep-sea habitats (29,30).…”

Section: Resultsmentioning

confidence: 99%

Phylogenetic Diversity of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Large-Subunit Genes from Deep-Sea Microorganisms

Elsaied

Naganuma

2001

Appl Environ Microbiol

126

132

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“…These bacteria have been found to be sulfur oxidizers and have been postulated to be important to the nutrit~on of host clams (Felbeck et al 1981, Sakai et al 1987. Because of their role in clam life, it is important to know the mode of establishment of the symbiosis in each new generation.…”

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confidence: 99%

Occurrence of bacteria in the primary oocytes of vesicomyid clam Calyptogena soyoae

Endow¹,

Ohta²

1990

Mar. Ecol. Prog. Ser.

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been introduced into eggs in cryptic forms. AmongThese bacteria resembled gill endosymbionts in the following 3 polnts: dimensions and general outllne, occurrence of elecdeep-sea tZlftia pachyptila was tron-transparent vacuoles in the periplasm, and occurrence of establish syn~biosis by talung up bacteria from freeelectron-dense materials in the periplasm. Eggs which harbored bacteria were all in the vitellogenic stage. This finding suggests some restricted time schedule of the entry of bacteria into oocytes. It is hypothesized that these bacteria represent transmission stage of gill symbionts, and continuum of the symbiosis is maintained by maternal inheritance through egg infection.

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“…The occurrence of multiple bacterial morphotypes within the trophosome may reflect the complexity of the geochemical processes seen in tubeworm habitats. Some seep habitats, such as the area of sample collection for this study, have abundant methane in the water and sediment, but hydrogen sulfide is only present in the sediment (Sakai et al, 1987). The seep-dwelling tubeworms are known to incorporate hydrogen sulfide from the sediment via their posterior end, which is buried in the sediment (Julian et al, 1999).…”

Section: Ish Using the 16s Rdna And Rubisco Probesmentioning

confidence: 99%

Molecular characterization and endosymbiotic localization of the gene encoding D-ribulose 1,5-bisphosphate carboxylase–oxygenase (RuBisCO) form II in the deep-sea vestimentiferan trophosome The DDBJ accession numbers for the sequences reported in this paper are AB042416 [ST-Sym(16S)-1], AB032829 [ST-Sym(II)-1] and AB040509 [ST-Sym(II)-2].

2002

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To better understand the contribution of micro-organisms to the primary production in the deep-sea gutless tubeworm Lamellibrachia sp., the 16S-rDNAbased phylogenetic data would be complemented by knowledge of the genes that encode the enzymes relevant to chemoautotrophic carbon fixation, such as D-ribulose 1,5-bisphosphate carboxylase-oxygenase (RuBisCO ; EC 4.1.1.39). To phylogenetically characterize the autotrophic endosymbiosis within the trophosome of the tubeworm Lamellibrachia sp., bulk trophosomal DNA was extracted and analysed based on the 16S-rRNA-and RuBisCO-encoding genes. The 16S-rRNA-and RuBisCO-encoding genes were amplified by PCR, cloned and sequenced. For the 16S rDNA, a total of 50 clones were randomly selected and analysed directly by sequencing. Only one operational taxonomic unit resulted from the 16S rDNA sequence analysis. This may indicate the occurrence of one endosymbiotic bacterial species within the trophosome of the Lamellibrachia sp. used in this study. Phylogenetic analysis of the 16S rDNA showed that the Lamellibrachia sp. endosymbiont was closely related to the genus Rhodobacter, a member of the α-Proteobacteria. For the RuBisCO genes, only the form II gene (cbbM) was amplified by PCR. A total of 50 cbbM clones were sequenced, and these were grouped into two operational RuBisCO units (ORUs) based on their deduced amino acid sequences. The cbbM ORUs showed high amino acid identities with those recorded from the ambient sediment bacteria. To confirm the results of sequence analysis, the localization of the symbiontspecific 16S rRNA and cbbM sequences in the Lamellibrachia sp. trophosome was visualized by in situ hybridization (ISH), using specific probes. Two types of cells, coccoid and filamentous, were observed at the peripheries of the trophosome lobules. Both the symbiont-specific 16S rDNA and cbbM probes hybridized at the same sites coincident with the location of the coccoid cells, whereas the filamentous cells showed no cbbM-specific signals. The RuBisCO form I gene (cbbL) was neither amplified by PCR nor detected by ISH. This is the first demonstration of chemoautotrophic symbiosis in the deep-sea gutless tubeworm, based on sequence data and in situ localization of both the 16S-rRNA-and RuBisCO-encoding genes.

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Geochemical study of the bathyal seep communities at the Hatsushima site, Sagami Bay, Central Japan.

Cited by 29 publications

References 20 publications

Phylogenetic Diversity of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Large-Subunit Genes from Deep-Sea Microorganisms

Phylogenetic Diversity of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Large-Subunit Genes from Deep-Sea Microorganisms

Occurrence of bacteria in the primary oocytes of vesicomyid clam Calyptogena soyoae

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