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Organic solutes in the deepest phylogenetic branches of the Bacteria: identification of α(1–6)glucosyl-α(1–2)glucosylglycerate in Persephonella marina

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Abstract

The accumulation of organic solutes was investigated in the thermophilic bacteria Persephonella marina and Marinitoga piezophila, two representatives of the deepest lineages in the domain Bacteria. These organisms grow optimally at around 70 °C in medium containing 3 % NaCl. A new disaccharide, accumulating in Persephonella marina, was identified as α(1–6)glucosyl-α(1–2)glucosylglycerate (GGG), by nuclear magnetic resonance. This identification was validated by comparison with the spectra of the compound obtained by chemical synthesis. Besides GGG, the solute pool of Persephonella marina comprised β-glutamate, di-myo-inositol-1,3′-phosphate and 2-O-α-glucosylglycerate. In contrast, amino acids such as α-glutamate, proline and alanine were the dominant components of the solute pool of Marinitoga piezophila and sugar derivatives were absent. The ability of GGG to protect protein structure against heat denaturation was assessed using model proteins. A genomic search for the biosynthetic pathways of known ionic solutes in Aquificales and Thermotogales shows the inability of this analysis to predict the nature of compatible solutes and underlines the need for efficient cultivation techniques.

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Acknowledgments

This work was supported by the European Commission, 6th Framework Programme contract COOP-CT-2003-508644, PRODEP and POCI, Portugal (PTDC/BIO/70806/2006) (POCI/V.5/A0004/2005). Technical assistance by Ana I Mingote is acknowledged. The NMR spectrometers are part of The National NMR Network (REDE/1517/RMN/2005), supported by “Programa Operacional Ciência e Inovação (POCTI) 2010” and Fundação para a Ciência e a Tecnologia (FCT). M.V.R. and L.G.G. received fellowships from FCT (SFRH/BPD/80219/2011 and SFRH/BPD/26905/2006). Data for the amino acid analysis was obtained by the Analytical Laboratory, Analytical Services Unit, Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa.

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Authors and Affiliations

  1. Biology Division, Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Av. da República, Estação Agronómica Nacional, 2780-157, Oeiras, Portugal

    Pedro Lamosa, Marta V. Rodrigues, Luís G. Gonçalves & Helena Santos

  2. Chemistry Division, Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Av. da República, Estação Agronómica Nacional, 2780-157, Oeiras, Portugal

    Rita Ventura & Christopher Maycock

  3. Health Protection Agency, Porton Down, Salisbury, Wiltshire, SP4 0JG, UK

    Jean Carr & Neil D. Raven

Authors
  1. Pedro Lamosa
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  2. Marta V. Rodrigues
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  3. Luís G. Gonçalves
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  5. Rita Ventura
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  7. Neil D. Raven
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  8. Helena Santos
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Corresponding author

Correspondence to Helena Santos.

Additional information

Communicated by H. Atomi.

P. Lamosa and M. V. Rodrigues contributed equally to this study.

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Lamosa, P., Rodrigues, M.V., Gonçalves, L.G. et al. Organic solutes in the deepest phylogenetic branches of the Bacteria: identification of α(1–6)glucosyl-α(1–2)glucosylglycerate in Persephonella marina . Extremophiles 17, 137–146 (2013). https://doi.org/10.1007/s00792-012-0500-x

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