Biology and ecology of the “Pompeii worm” (Alvinella pompejana Desbruyères and Laubier), a normal dweller of an extreme deep-sea environment: A synthesis of current knowledge and recent developments

Desbruyères, Daniel; Chevaldonné, Pierre; Alayse, Anne-Marie; Jollivet, Didier; Lallier, F.; Jouin-Toulmond, C.; Zal, Franck; Sarradin, Pierre‐Marie; Cosson, Richard P.; Caprais, Jean‐Claude; Arndt, C.; O’Brien, John; Guézennec, Jean; Hourdez, Stéphane; Riso, Ricardo; Gaill, Françoise; Laubier, Lucien; Toulmond, André

doi:10.1016/s0967-0645(97)00083-0

Cited by 153 publications

(148 citation statements)

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“…Higher temperatures experienced by some species, e.g. the "Pompeii worm" (105°C at hydrothermal deep sea vents, Desbruyeres et al 1998), a desert ant (53.6°C, Wehner et al 1992) are only tolerated during short-term exposure (see Dahlhoff and Somero 1991 for the "Pompeii worm"). The heat tolerance limits of metazoa are much lower than the thermal limits of bacteria, some of which can thrive in continuously boiling waters.…”

Section: Thermal Tolerance and The Complexity Of Physiological Functionmentioning

confidence: 99%

Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals

Pörtner

2001

Naturwissenschaften

957

232

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Recent years have shown a rise in mean global temperatures and a shift in the geographical distribution of ectothermic animals. For a cause and effect analysis the present paper discusses those physiological processes limiting thermal tolerance. The lower heat tolerance in metazoa compared with unicellular eukaryotes and bacteria suggests that a complex systemic rather than molecular process is limiting in metazoa. Whole-animal aerobic scope appears as the first process limited at low and high temperatures, linked to the progressively insufficient capacity of circulation and ventilation. Oxygen levels in body fluids may decrease, reflecting excessive oxygen demand at high temperatures or insufficient aerobic capacity of mitochondria at low temperatures. Aerobic scope falls at temperatures beyond the thermal optimum and vanishes at low or high critical temperatures when transition to an anaerobic mitochondrial metabolism occurs. The adjustment of mitochondrial densities on top of parallel molecular or membrane adjustments appears crucial for maintaining aerobic scope and for shifting thermal tolerance. In conclusion, the capacity of oxygen delivery matches full aerobic scope only within the thermal optimum. At temperatures outside this range, only time-limited survival is supported by residual aerobic scope, then anaerobic metabolism and finally molecular protection by heat shock proteins and antioxidative defence. In a cause and effect hierarchy, the progressive increase in oxygen limitation at extreme temperatures may even enhance oxidative and denaturation stress. As a corollary, capacity limitations at a complex level of organisation, the oxygen delivery system, define thermal tolerance limits before molecular functions become disturbed.

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Section: Thermal Tolerance and The Complexity Of Physiological Functionmentioning

confidence: 99%

Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals

Pörtner

2001

Naturwissenschaften

957

232

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“…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).…”

mentioning

confidence: 98%

“…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).…”

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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“…Sex was determined externally by the morphology of the genital pore (Pradillon & Gaill 2003), or by the presence, in males, of 1 pair of thick buccal tentacles, which are lacking in females (Desbruyères et al 1998).…”

Section: Methodsmentioning

confidence: 99%

Colonisation of newly-opened habitat by a pioneer species, Alvinella pompejana (Polychaeta: Alvinellidae), at East Pacific Rise vent sites

Pradillon¹,

Zbinden²,

Mullineaux³

et al. 2005

Mar. Ecol. Prog. Ser.

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Animal communities on the walls of deep-sea hydrothermal chimneys are distributed in mosaics of patches that may evolve as local environmental conditions change and biological interactions develop. Alvinella pompejana Desbruyères et Laubier, 1980 is one of the first metazoan colonisers of new surfaces created by mineral precipitation, and therefore may be particularly important in community establishment in active parts of smokers. Here our goal was to investigate the colonisation mechanisms of A. pompejana in new patches and determine whether these mechanisms may influence population structure and reproductive patterns in this species. We deployed a series of TRAC (Titanium Ring for Alvinellid Colonisation) devices at East Pacific Rise (EPR) vent sites to compare the size and stage (i.e. reproductive maturity) distribution of A. pompejana individuals between recently colonised patches (TRACs) and established patches (grabbed by submersible). TRACs deployed for short time periods (11 d to 1 mo) were generally colonised by smaller individuals than those found in background populations or in TRACs deployed for longer time periods (>1 mo). Colonists into new patches were a mix of juveniles and individuals that were sexually mature but non-reproductive (i.e. not producing gametes), whereas background population and older patches harboured a mixture of individuals at different stages including reproductive females. Although some individuals may have recruited on TRACs as larvae, the major colonisation process involved was probably immigration of post-larval stages. In long-term TRAC, reproductive females were not reproductively synchronised. In this dynamic environment, reproduction would be triggered by the disturbance/migration processes, explaining the heterogeneity observed in reproductive patterns.

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Biology and ecology of the “Pompeii worm” (Alvinella pompejana Desbruyères and Laubier), a normal dweller of an extreme deep-sea environment: A synthesis of current knowledge and recent developments

Cited by 153 publications

References 0 publications

Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals

Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals

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

Colonisation of newly-opened habitat by a pioneer species, Alvinella pompejana (Polychaeta: Alvinellidae), at East Pacific Rise vent sites

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