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Assessing a species thermal tolerance through a multiparameter approach: the case study of the deep-sea hydrothermal vent shrimp Rimicaris exoculata

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Cell Stress and Chaperones Aims and scope

Abstract

Assessing species thermal tolerance requires identification of their thermal strategies and evaluation of their ability to cope with temperature fluctuations. The mobilization of the molecular heat stress response (HSR), which is a proxy for the thermal tolerance, would be part of the strategy of species colonizing highly variable thermal environments. We here investigate multiple parameters of the HSR in the deep-sea vent shrimp Rimicaris exoculata that colonizes such environments. The set points of the HSR induction, compared to those of the coastal species Palaemonetes varians, clearly reflect a high thermotolerance in this species, while the HSR is proved to be rarely mobilized in the R. exoculata natural populations. Finally, the compilation of multiple parameters such as the upper thermal limit and several thresholds of the HSR, as well as thermal behavior observations, allows us to provide a more accurate picture of the combination and complementarity of strategies that can account for the overall thermal tolerance of the species.

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References

  • Airriess CN, Childress JJ (1994) Homeoviscous properties implicated by the interactive effects of pressure and temperature on the hydrothermal vent crab Bythograea thermydron. Biol Bull 187(2):208–214

    Article  CAS  PubMed  Google Scholar 

  • Angilletta MJ (2009) Thermal acclimation. In: Thermal adaptation. Oxford University Press Inc, New York, pp 126–156

    Chapter  Google Scholar 

  • Auguste MC, Mestre N, Rocha T, Cardoso C, Cueff-Gauchard V, Le Bloa S, Cambon-Bonavita MA, Shillito B, Zbinden M, Ravaux J, Bebianno M (2016) Development of an ecotoxicological protocol for the deep-sea fauna using the hydrothermal vent shrimp Rimicaris exoculata. Aquat Toxicol 175:277–285

    Article  CAS  PubMed  Google Scholar 

  • Barua D, Heckathorn SA (2004) Acclimation of the temperature set-points of the heat-shock response. J Therm Biol 29:185–193

    Article  Google Scholar 

  • Bates AE, Lee RW, Tunnicliffe V, Lamare MD (2010) Deep-sea hydrothermal vent animals seek cool fluids in a highly variable thermal environment. Nat Commun 1:14–16. https://doi.org/10.1038/ncomms1014

    Article  CAS  PubMed  Google Scholar 

  • Chown SL, Jumbam KR, Sørensen JG, Terblanche JS (2009) Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Funct Ecol 23:133–140

    Article  Google Scholar 

  • Copley JTP, Tyler PA, Murton BJ, Van Dover CL (1997) Spatial and interannual variation in the faunal distribution at Broken Spur vent field (29°N, Mid-Atlanic Ridge). Mar Biol 129:723–733

    Article  Google Scholar 

  • Cottin D, Shillito B, Chertemps T, Thatje S, Léger N, Ravaux J (2010a) Comparison of heat-shock responses between the hot vent shrimp Rimicaris exoculata and the related coastal shrimp Palaemonetes varians. J Exp Mar Biol Ecol 393:9–16

    Article  Google Scholar 

  • Cottin D, Shillito B, Tanguy A, Léger N, Ravaux J (2010b) Identification of differentially expressed genes in the hydrothermal vent shrimp Rimicaris exoculata exposed to heat stress. Mar Genomics 3:71–78

    Article  PubMed  Google Scholar 

  • Desbruyères D, Biscoito M, Caprais JC, Colaço A, Comtet T, Crassous P, Fouquet Y, Khripounoff A, Le Bris N, Olu K, Riso R, Sarradin PM, Segonzac M, Vangriesheim A (2001) Variations in the deep-sea hydrothermal vent communities on the Mid-Atlantic Ridge near the Azores plateau. Deep-Sea Res 48:1325–1346

    Article  Google Scholar 

  • Gebruk AV, Southward EC, Kennedy H, Southward AJ (2000) Food source, behaviour and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge. J Mar Biol Ass UK 80:485–499

    Article  CAS  Google Scholar 

  • Geret F, Riso R, Sarradin PM, Caprais JC, Cosson R (2002) Metal bioaccumulation and storage forms in the shrimp, Rimicaris exoculata, from the rainbow hydrothermal field (Mid-Atlantic Ridge); preliminary approach to the fluid-organism relationship. Cah Biol Mar 43:43–52

    Google Scholar 

  • Girguis PR, Lee RW (2006) Thermal preference and tolerance of Alvinellids. Science 312:231

    Article  PubMed  Google Scholar 

  • Jones JC, Oldroy BP (2007) Nest thermoregulation in social insects. Adv In Insect Phys 33:153–191. https://doi.org/10.1016/S0065-2806(06)33003-2

    Article  Google Scholar 

  • Lee RW (2003) Thermal tolerances of deep-sea hydrothermal vent animals from the Northeast Pacific. Biol Bull 205:98–101

    Article  PubMed  Google Scholar 

  • McMullin ER, Bergquist DC, Fisher CR (2000) Metazoans in extreme environments: adaptations of hydrothermal vent and hydrocarbon seep fauna. Gravit Space Biol Bull 13(2):13–23

    CAS  PubMed  Google Scholar 

  • Morris J, Thatje S, Hauton C (2013) The use of stress-70 proteins in physiology: a re-appraisal. Mol Ecol 22:1494–1502

    Article  CAS  PubMed  Google Scholar 

  • Polz MF, Robinson JJ, Cavanaugh CM, Van Dover CL (1998) Trophic ecology of massive shrimp aggregations at a Mid-Atlantic hydorthermal vent site. Limnol Oceanogr 43(7):1631–1638

    Article  CAS  Google Scholar 

  • Ponsard J, Cambon-Bonavita MA, Zbinden M, Lepoint G, Joassin A, Corbari L, Shillito B, Durand L, Cueff-Gauchard V, Compère P (2013) Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host shrimp Rimicaris exoculata. ISME J 7(1):96–109

    Article  CAS  PubMed  Google Scholar 

  • Ravaux J, Gaill F, Le Bris N, Sarradin PM, Jollivet D, Shillito B (2003) Heat shock response and temperature resistance in the deep-sea vent shrimp Rimicaris exoculata. J Exp Biol 206:2345–2354

    Article  PubMed  Google Scholar 

  • Ravaux J, Toullec JY, Léger N, Lopez P, Gaill F, Shillito B (2007) First hsp70 from two hydrothermal vent shrimps, Mirocaris fortunata and Rimicaris exoculata : characterization and sequence analysis. Gene 386:162–172

    Article  CAS  PubMed  Google Scholar 

  • Ravaux J, Cottin D, Chertemps T, Hamel G, Shillito B (2009) Hydrothermal vent shrimps display low expression of heat-inducible hsp70 gene in nature. Mar Ecol Prog Ser 396:153–156

    Article  CAS  Google Scholar 

  • Ravaux J, Léger N, Rabet N, Morini M, Zbinden M, Thatje S, Shillito B (2012) Adaptation to thermally variable environments: capacity for acclimation of thermal limit and heat shock response in the shrimp Palaemonetes varians. J Comp Physiol B 182(7):899–907

    Article  CAS  PubMed  Google Scholar 

  • Ravaux J, Hamel G, Zbinden M, Tasiemski AA, Boutet I, Léger N, Tanguy A, Jollivet D, Shillito B (2013) Thermal limit for metazoan life in question: in vivo heat tolerance of the Pompeii worm. PLoS One 8(5):e64074. https://doi.org/10.1371/journal.pone.0064074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ravaux J, Léger N, Rabet N, Fourgous C, Voland G, Zbinden M, Shillito B (2016) Plasticity and acquisition of the thermal tolerance (upper thermal limit and heat shock response) in the intertidal species Palaemon elegans. J Exp Mar Biol Ecol 484:39–45

    Article  Google Scholar 

  • Ritz DA, Hobday AJ, Montgomery JC, Ward AJW (2011) Social aggregation in the pelagic zone with special reference to fish and invertebrates. Adv Mar Biol 60:161–227

    Article  PubMed  Google Scholar 

  • Schmidt C, Le Bris N, Gaill F (2008) Interactions of deep-sea vent invertebrates with their environment: the case of Rimicaris exoculata. J Shell Res 27(1):9–90

    Article  Google Scholar 

  • Segonzac M, De Saint Laurent M, Casanova B (1993) L’énigme du comportement trophique des crevettes Alvinocarididea des sites hydrothermaux de la dorsale médio-atlantique. Cah Bio Mar 34:535–571

    Google Scholar 

  • Shillito B, Le Bris N, Hourdez S, Ravaux J, Cottin D, Caprais JC, Jollivet D, Gaill F (2006) Temperature resistance studies on the deep-sea vent shrimp Mirocaris fortunata. J Exp Biol 209:945–955

    Article  PubMed  Google Scholar 

  • Shillito B, Hamel G, Duchi C, Cottin D, Sarrazin J, Sarradin PM, Ravaux J, Gaill F (2008) Live capture of megafauna from 2300 m depth, using a newly- designed pressurised recovery device. Deep-Sea Res I Oceanogr Res Pap 55:881–889

    Article  Google Scholar 

  • Shillito B, Gaill F, Ravaux J (2014) The IPOCAMP pressure incubator for deep-sea fauna. J Mar Sci Technol (Taiwan) 22 (1): 97–102. 10.6119/ JMST-013-0718-3

  • Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers. J Exp Biol 213:912–920

    Article  CAS  PubMed  Google Scholar 

  • Tomanek L (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species’ biogeographical distribution ranges and metabolic costs. J Exp Biol 213:971–979

    Article  CAS  PubMed  Google Scholar 

  • Tunnicliffe V, McArthur AG, McHugh D (1998) A biogeographical perspective of the deep-sea hydrothermal vent fauna. Adv Mar Biol 34:353–442

    Article  Google Scholar 

  • Van Dover CL, Fry B, Grassle JF, Humphris S, Rona PA (1988) Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the mid-Atlantic ridge. Mar Biol 98:209–216

    Article  Google Scholar 

  • Van Dover CL, Lutz RA (2004) Experimental ecology at deep-sea hydrothermal vents: a perspective. J Exp Mar Biol Ecol 300:273–307

    Article  Google Scholar 

  • Vinagre C, Leal I, Mendonça V, Flores AAV (2015) Effect of warming rate on the critical thermal maxima of crabs, shrimp and fish. J Therm Biol 47:19–25

    Article  PubMed  Google Scholar 

  • Zbinden M, Le Bris N, Gaill F, Compère P (2004) Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes. Mar Ecol Prog Ser 284:237–251

    Article  Google Scholar 

Download references

Acknowledgements

We thank the captain and crew of the RV Pourquoi Pas ? and ROV Victor 6000 groups (IFREMER), and M.A. Cambon-Bonnavita (chief scientist of the BICOSE 2014 cruise), M. Zbinden, and K. Szafranski for their assistance on board, as well as M. Léger for her help. The qPCR analyses were performed at the Real Time PCR service (IFR 83 Biologie Intégrative, Université Pierre et Marie Curie).

Funding

This study was funded by the EXOCET/D European Community project (FP6-GOCE-CT-2003-505342), by CNRS and ANR grants (BALIST ANR-08-BLAN-0252), and by the Université Pierre et Marie Curie (BQR UPMC 2008). The work also benefited from the support of the MIDAS European Community project (European Union Seventh Framework Programme FP7/2007–2013) under the grant agreement no. 603418.

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Authors and Affiliations

  1. BOREA Biologie des Organismes et Ecosystèmes Aquatiques, UMR 7208 MNHN CNRS SU UA UCN IRD 207, Equipe Adaptation aux Milieux Extrêmes, Sorbonne Université, Bât. A, 4e étage, 7 Quai St Bernard, 75005, Paris, France

    Juliette Ravaux, Nelly Léger & Bruce Shillito

  2. IMPMC Institut de Minéralogie, de Physique des Matériaux et Cosmochimie, UMR CNRS SU 7590, Sorbonne Université, Paris Cedex 05, France

    Gérard Hamel

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  1. Juliette Ravaux
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  2. Nelly Léger
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  3. Gérard Hamel
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  4. Bruce Shillito
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Correspondence to Juliette Ravaux.

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Ravaux, J., Léger, N., Hamel, G. et al. Assessing a species thermal tolerance through a multiparameter approach: the case study of the deep-sea hydrothermal vent shrimp Rimicaris exoculata. Cell Stress and Chaperones 24, 647–659 (2019). https://doi.org/10.1007/s12192-019-01003-0

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