Metabolic diversity in epibiotic microflora associated with the Pompeii wormsAlvinella pompejana andA. caudata (Polychaetae: Annelida) from deep-sea hydrothermal vents

Prieur, Daniël; Chamroux, S.; Durand, Pascale; Erauso, Gaël; Fera, Ph.; Jeanthon, Christian; Borgne, L. Le; Mével, Geneviève; Vincent, P

doi:10.1007/bf01344313

Cited by 32 publications

(24 citation statements)

References 25 publications

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“…It is important to note that the guts of the lower level consumers (the prey items) are likely to contain ingested free-living bacteria, and their external body surfaces probably host free-living chemoautotrophic bacteria colonists. For example, alvinellids have been shown to possess a dense and diverse assemblage of external bacteria (Prieur et al, 1990), and dense bacterial growth has been observed on the shells of some gastropods such as Depressigyra globulus (C.R.F. and I.A.U.…”

Section: Predatorsmentioning

confidence: 99%

Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web

Bergquist¹,

Eckner

Urcuyo³

et al. 2007

Mar. Ecol. Prog. Ser.

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To investigate food web structure in diffuse flow vent environments, an entire macrofaunal community associated with a single aggregation of the tubeworm Ridgeia piscesae was collected from a vent field on the Juan de Fuca Ridge in the NE Pacific. All members of the community were identified and enumerated, and the biomass and stable carbon (δ 13 C) and nitrogen (δ 15 N) isotope ratios were determined for almost all taxa. Symbiont-bearing invertebrates (primarily R. piscesae) accounted for a vast majority of the biomass of the community, and 3 presumably grazing bacterivorous gastropods dominated the biomass of the consumer fauna. Biomass and abundance of individuals declined from the bacterivore to the scavenger/detritivore to the predator feeding guild. Several species (a folliculinid ciliate, Idas washingtonia, Provanna variabilis) possessed unique stable isotope signatures, suggesting the possibility of symbiotic relationships with autotrophic bacteria. Stable isotope values varied widely between and occasionally within species in the lowest consumer levels suggesting a great diversity of food source 13 C and 15 N composition. Based on the distinct isotopic values of 3 bacterivores, 3 potential pools of isotopically-distinct microbial production were identified. The 4 highest-biomass predatory species (all polynoids) possessed δ 13 C and δ 15 N values consistent with a diet that included the tubeworm R. piscesae, a species comprising 83% of the total biomass in the collection, and the gastropod Depressigyra globulus, a species comprising 10% of the total biomass in the collection. A potential specialist predator (Clypeosectus curvus) on folliculinid ciliates was also identified. Overall the study suggested a dominant pattern of energy transfer from microbial producers to symbiont-bearing siboglinid tubeworms, various bacterivores (gastropods, polychaetes and pycnogonids), and detritivorous polychaetes to predaceous polynoids.

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Section: Predatorsmentioning

confidence: 99%

Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web

Bergquist¹,

Eckner

Urcuyo³

et al. 2007

Mar. Ecol. Prog. Ser.

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“…Despite the great interest of scientists in studying thermophilic or hyperthermophilic micro-organisms, it is generally admitted that mesophiles, as well as moderate thermophiles, may represent the most abundant microbes in hydrothermal vents (Campbell et al, 2001;Jeanthon, 2000). This is exemplified by the isolation of (i) metabolically diverse non-filamentous mesophilic bacteria from the dorsal integument of Alvinella pompejana (Prieur & Jeanthon, 1987;Prieur et al, 1990;Raguénès et al, 1996), (ii) several mesophilic sulfur-oxidizing bacteria (Durand et al, 1993;Jannasch et al, 1985;Ruby & Jannasch, 1982;Wirsen et al, 1998) and (iii) moderate thermophiles belonging to the e-Proteobacteria (Campbell et al, 2001). Sulfate reduction activity was evident in sediments from Guaymas Basin (Elsgaard et al, 1994;Jørgensen et al, 1992) and successful isolation was achieved from various samples collected at different marine hydrothermal environments, thus suggesting the probable ecological significance of SRB in the biogeochemistry of such environments.…”

Section: Strain Am13mentioning

confidence: 99%

Desulfovibrio hydrothermalis sp. nov., a novel sulfate-reducing bacterium isolated from hydrothermal vents

Alazard

Dukan

Urios

et al. 2003

International Journal of Systematic and Evolutionary Microbiology

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T ) differed from D. zosterae not only phylogenetically, but also genomically (DNA-DNA reassociation value between the two bacteria was 23?8 %) and phenotypically. This isolate is therefore proposed as the type strain of a novel species of the genus Desulfovibrio, Desulfovibrio hydrothermalis sp. nov.Deep-sea hydrothermal vents are among the most productive ecosystems on Earth, where unusual animal and microbial communities are able to survive the harsh combinations of toxic chemicals, high pressures, high temperatures and total darkness. This high biomass productivity is based largely on the activity of ectoand endosymbiotic associations of chemolithotrophic micro-organisms and vent fauna (Jeanthon, 2000;Polz & Cavanaugh, 1995). Microbial hydrothermal vent communities also include free-living bacteria associated with the discharged vent fluids, free-living microbial mats and micro-organisms within the deep-sea hydrothermal vent plume (Karl, 1995). Although increasing attention has been paid to the thermophilic and hyperthermophilic microorganisms that inhabit deep-sea hydrothermal vents, because of their high biotechnological potential, mesophilic and psychrophilic micro-organisms are known to be significant components of the microbial community along the physico-chemical gradient of the vent ecosystem (Jeanthon, 2000). The occurrence of mesophilic sulfatereducing bacteria (SRB) was made evident by (i) significant sulfate-reduction activities in vent sediments (Elsgaard et al., 1994;Jørgensen et al., 1992) and (ii) their isolation from various samples collected at different hydrothermal sites (Elsgaard et al., 1995). However, none of them has yet been characterized.Here, we report the isolation from deep-sea hydrothermal chimneys of SRB that are phylogenetically similar to Desulfovibrio profundus (Bale et al., 1997) and the characterization of a novel mesophilic, barophilic species (strain AM13 T ) of the genus Desulfovibrio, Desulfovibrio hydrothermalis sp. nov.Strains BL5, H9, H1 and AM13T were isolated from a deep-sea hydrothermal chimney sample stored in sea water at 4˚C until processing. The GenBank accession number for the 16S rDNA sequence of strain AM13T is AF458778.

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“…Various types of bacteria have been cultured, including heavy metal-resistant strains and both heterotrophic and chemolithautotrophic members of the epsilon Proteobacteria (11,31,37,42,43). None of these isolates are the dominant episymbionts, and they represent Ͻ1% of the community (11; B. Campbell and S. Cary, unpublished data).…”

mentioning

confidence: 99%

Evidence of Chemolithoautotrophy in the Bacterial Community Associated withAlvinella pompejana, a Hydrothermal Vent Polychaete

Campbell

Stein

Cary

2003

Appl Environ Microbiol

118

124

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The deep-sea polychaete Alvinella pompejana colonizes tubes on the sides of black smoker chimneys along the East Pacific Rise. A diverse, yet phylogenetically constrained episymbiotic community is obligately associated with its dorsal surface. The morphologically and phylogenetically distinct dominant episymbionts have not yet been cultured, and there are no clearly defined roles for these bacteria in this symbiosis. A large insert fosmid library was screened for the presence of the two dominant phylotypes. Two fosmids, 35.2 and 38 kb, containing phylotype-specific 16S ribosmal DNA sequences were fully sequenced. Each fosmid had a gene encoding ATP citrate lyase, a key enzyme in the reverse tricarboxylic acid (rTCA) cycle, a CO 2 fixation pathway. A selection of episymbiont communities from various geographic locations and vent sites were screened for the presence, diversity, and expression (via reverse transcription-PCR) of the ATP citrate lyase gene. Our results indicate that the ATP citrate lyase gene is not only a consistent presence in these episymbiont communities but is also expressed. Phylogenetically distinct forms of ATP citrate lyase were also found associated with and expressed by bacteria extracted from the tubes of A. pompejana. Utilizing PCR with degenerate primers based on a second key enzyme in the rTCA cycle, 2-oxoglutarate:acceptor oxidoreductase, we also demonstrated the persistent presence and expression of this gene in the episymbiont community. Our results suggest that members of both the episymbiont and the surrounding free-living communities display a chemolithoautotrophic form of growth and therefore contribute fixed carbon to other organisms in the vent community.The tube-dwelling polychete Alvinella pompejana inhabits high-temperature hydrothermal vent chimneys from 21°N to 32°S along the East Pacific Rise (EPR) (17,18,21). A morphologically and phylogenetically diverse episymbiotic bacterial community forms a dense layer on the dorsal surface of A. pompejana (12,18,28). This association is specific and obligate, and the dominant epibionts are filamentous and associated with the dorsal epidermal expansions (hair-like projections) of A. pompejana (12,18). The role of these episymbiotic bacteria in the association has been difficult to decipher. The symbionts have previously been hypothesized to be involved in both the nutrition of the host and in the detoxification of sulfide and heavy metals (1,19,43). The ␦ 13 C ratios of the A. pompejana worms and fatty acid profiles of the symbiont community indicate potential chemolithoautotrophy within the community (17,19,53). However, the dominant bacterial filaments associated with the polysaccharide structures on A. pompejana appear not to assimilate CO 2 in any appreciable amount via the Calvin-Benson cycle according to ribulose 1,5-bisphosphate carboxylase-oxygenase, 14 C labeling, and bicarbonate uptake assays (17,19).Molecular characterizations of the A. pompejana symbiont population indicate that the majority of the symbionts group withi...

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Metabolic diversity in epibiotic microflora associated with the Pompeii wormsAlvinella pompejana andA. caudata (Polychaetae: Annelida) from deep-sea hydrothermal vents

Cited by 32 publications

References 25 publications

Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web

Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web

Desulfovibrio hydrothermalis sp. nov., a novel sulfate-reducing bacterium isolated from hydrothermal vents

Evidence of Chemolithoautotrophy in the Bacterial Community Associated withAlvinella pompejana, a Hydrothermal Vent Polychaete

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