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Mannosylglycerate: structural analysis of biosynthesis and evolutionary history

  • Special Issue: Review
  • 10th International Congress on Extremophiles
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Abstract

Halophilic and halotolerant microorganisms adapted to thrive in hot environments accumulate compatible solutes that usually have a negative charge either associated with a carboxylic group or a phosphodiester unit. Mannosylglycerate (MG) has been detected in several members of (hyper)thermophilic bacteria and archaea, in which it responds primarily to osmotic stress. The outstanding ability of MG to stabilize protein structure in vitro as well as in vivo has been convincingly demonstrated. These findings led to an increasingly supported link between MG and microbial adaptation to high temperature. However, the accumulation of MG in many red algae has been known for a long time, and the peculiar distribution of MG in such distant lineages was intriguing. Knowledge on the biosynthetic machinery together with the rapid expansion of genome databases allowed for structural and phylogenetic analyses and provided insight into the distribution of MG. The two pathways for MG synthesis have distinct evolutionary histories and physiological roles: in red algae MG is synthesised exclusively via the single-step pathway and most probably is unrelated with stress protection. In contrast, the two-step pathway is strongly associated with osmoadaptation in (hyper)thermophilic prokaryotes. The phylogenetic analysis of the two-step pathway also reveals a second cluster composed of fungi and mesophilic bacteria, but MG has not been demonstrated in members of this cluster; we propose that the synthase is part of a more complex pathway directed at the synthesis of yet unknown molecules containing the mannosyl-glyceryl unit.

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Abbreviations

MGS:

Mannosylglycerate synthase

MPGS:

Mannosyl-3-phosphoglycerate synthase

MPGP:

Mannosyl-3-phosphoglycerate phosphatase

MPG:

Mannosyl-3-phosphoglycerate

MGH:

Mannosylglycerate hydrolase

GTs:

Glycosyltransferases

PhoMPGS:

Pyrococcus horikoshii OT3 MPGS

TthMPGS:

Thermus thermophilus HB27 MPGS

RmaMGS:

Rhodothermus marinus MGS

r.m.s.d.:

Root mean square deviation

SSM:

Secondary structure matching

RmMGS∆15 :

Rhodothermus marinus MGS 15 residues truncated at the C-terminus

RxyMPGS/GPGS:

Rubrobacter xylanophilus MPGS/GPGS

3-PGA:

3-d-phosphoglycerate

M2+ :

Generic divalent co-catalytic metal ion

NDP:

Nucleoside diphosphate

HGT:

Horizontal gene transfer

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Acknowledgments

This work was funded by the Fundação para a Ciência e a Tecnologia (FCT): Projects PTDC/BIA-MIC/71146/2006, PTDC/BBB-BEP/2532/2012 and PEst-OE/EQB/LA0004/2011. C.D.J. and L.G. acknowledge FCT for the award of post-doc grants (SFRH/BPD/43410/2008 and SFRH/BPD/26905/2006, respectively). The NMR spectrometers are part of The National NMR Facility, supported by FCT (RECI/BBB-BQB/0230/2012). We thank Dr. Rasmus Larsen for the identification of the mgS gene from Caloglossa leprieurii and Dr. Clélia Neves for confirming the activity. We want to extent our acknowledgment to our co-workers in the many papers dealing with mannosylglycerate.

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Authors and Affiliations

  1. Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Avenida da República-EAN, 2780-157, Oeiras, Portugal

    Nuno Borges, Carla D. Jorge, Luís G. Gonçalves, Susana Gonçalves, Pedro M. Matias & Helena Santos

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  1. Nuno Borges
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  2. Carla D. Jorge
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  3. Luís G. Gonçalves
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  4. Susana Gonçalves
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  5. Pedro M. Matias
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  6. Helena Santos
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Correspondence to Helena Santos.

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Communicated by G. Antranikian.

C. D. Jorge and L. G. Gonçalves equally contributed.

This article is part of a special issue based on the 10th International Congress on Extremophiles held in Saint Petersburg, Russia, September 7–11, 2014.

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Borges, N., Jorge, C.D., Gonçalves, L.G. et al. Mannosylglycerate: structural analysis of biosynthesis and evolutionary history. Extremophiles 18, 835–852 (2014). https://doi.org/10.1007/s00792-014-0661-x

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