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Detection and Characterisation of Mutations Responsible for Allele-Specific Protein Thermostabilities at the Mn-Superoxide Dismutase Gene in the Deep-Sea Hydrothermal Vent Polychaete Alvinella pompejana

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Abstract

Alvinella pompejana (Polychaeta, Alvinellidae) is one of the most thermotolerant marine eukaryotes known to date. It inhabits chimney walls of deep-sea hydrothermal vents along the East Pacific Rise (EPR) and is exposed to various challenging conditions (e.g. high temperature, hypoxia and the presence of sulphides, heavy metals and radiations), which increase the production of dangerous reactive oxygen species (ROS). Two different allelic forms of a manganese-superoxide dismutase involved in ROS detoxification, ApMnSOD1 and ApMnSOD2, and differing only by two substitutions (M110L and A138G) were identified in an A. pompejana cDNA library. RFLP screening of 60 individuals from different localities along the EPR showed that ApMnSOD2 was rare (2 %) and only found in the heterozygous state. Dynamic light scattering measurements and residual enzymatic activity experiments showed that the most frequent form (ApMnSOD1) was the most resistant to temperature. Their half-lives were similarly long at 65 °C (>110 min) but exhibited a twofold difference at 80 °C (20.8 vs 9.8 min). Those properties are likely to be explained by the occurrence of an additional sulphur-containing hydrogen bond involving the M110 residue and the effect of the A138 residue on the backbone entropy. Our results confirm the thermophily of A. pompejana and suggest that this locus is a good model to study how the extreme thermal heterogeneity of the vent conditions may help to maintain old rare variants in those populations.

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Abbreviations

AAT:

Aspartate-amino transferase

CuZnSOD:

Cu,Zn-superoxide dismutase

EPR:

East Pacific Rise

GPI:

Glucose-6-phosphate isomerase

LSE:

Local structural entropy

MDH:

Malate dehydrogenase

MnSOD:

Mn-superoxide dismutase

PGM:

Phosphoglucomutase

ROS:

Reactive oxygen species

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Acknowledgments

We are grateful to the chief scientists and the crews of the Nautile submersible and the N/O L’Atalante involved in the PHARE2002 and BIOSPEEDO2004 oceanographic expeditions for their help and their efforts during the sampling missions. We would like to thank Mirjam Czjzek and Etienne Rebuffet for their help with the DLS experiments and Eric Fontanillas for his bioinformatic expertise in the assembly and annotation of the alvinellid polychaete transcriptomes, as well as the two anonymous reviewers for their comments which helped to improve the manuscript. We are also grateful to Susan Johnston for proofreading the English version of this manuscript. This study was funded by the PRIRE AMETHYST (Région Bretagne) programme, by a GIS Europôle Mer grant and by the ANR grant ‘Alvinella’ (05BLAN0407).

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Authors and Affiliations

  1. UPMC Université Pierre-et-Marie Curie, UMR 7144, Laboratoire Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, 29680, Roscoff, France

    Matthieu Bruneaux, Jean Mary, Marie Verheye, Didier Jollivet & Arnaud Tanguy

  2. CNRS, UMR 7144, Station Biologique de Roscoff, 29682, Roscoff, France

    Matthieu Bruneaux, Jean Mary, Marie Verheye, Didier Jollivet & Arnaud Tanguy

  3. IGBMC Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS UMR 7104—INSERM U 964, UDS, Laboratoire de Bioinformatique et Génomique Intégratives, 67400, Illkirch, France

    Odile Lecompte & Olivier Poch

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  3. Marie Verheye
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  4. Odile Lecompte
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  7. Arnaud Tanguy
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Correspondence to Arnaud Tanguy.

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Bruneaux, M., Mary, J., Verheye, M. et al. Detection and Characterisation of Mutations Responsible for Allele-Specific Protein Thermostabilities at the Mn-Superoxide Dismutase Gene in the Deep-Sea Hydrothermal Vent Polychaete Alvinella pompejana . J Mol Evol 76, 295–310 (2013). https://doi.org/10.1007/s00239-013-9559-y

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  • DOI: https://doi.org/10.1007/s00239-013-9559-y

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