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Adaptation to Extreme Environments: Macromolecular Dynamics in Complex Systems

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Adaptation to Extreme Environments: Macromolecular Dynamics in Complex Systems University of Wollongong Research Online Faculty of Science - Papers (Archive) Faculty of Science, Medicine and Health August 2005 Adaptation to extreme environments: Macromolecular dynamics in complex systems M. Tehei University of Wollongong, [email protected] Follow this and additional works at: https://ro.uow.edu.au/scipapers Part of the Life Sciences Commons, Physical Sciences and Mathematics Commons, and the Social and Behavioral Sciences Commons Recommended Citation Tehei, M.: Adaptation to extreme environments: Macromolecular dynamics in complex systems 2005. https://ro.uow.edu.au/scipapers/113 Research Online is the open access institutional repository for the University of Wollongong. For further information contact the UOW Library: [email protected] Adaptation to extreme environments: Macromolecular dynamics in complex systems Abstract What we previously thought of as insurmountable physical and chemical barriers to life, we now see as yet another niche harbouring Fextremophiles_. Extremophiles and their macromolecules had to develop molecular mechanisms of adaptation to extreme physico–chemical conditions. Using neutron spectroscopy, we have demonstrated that molecular dynamics represents one of these molecular mechanisms of adaptation. To which extent do hyper-saline conditions and extreme temperatures influence molecular dynamics? First, molecular dynamics were analysed for halophilic malate dehydrogenase from Haloarcula marismortui (Hm MalDH) under different molar solvent salt concentration conditions influencing its stability. Secondly, mean macromolecular motions were measured in-vivo in psychrophile (Aquaspirillum arcticum), mesophile (Escherichia coli and Proteus mirabilis), thermophile (Thermus thermophilus), and hyperthermophile (Aquifex pyrofilus) bacteria. The mean constant force of Hm MalDH increases progessively with increasing stability. The results show that the molecular adaptation of Hm MalDH to hyper-saline conditions is achieved through an increasing resilience of its structure dominated by enthalpic mechanisms. The study of bacteria has provided tools to quantify the macromolecular adaptation to extreme temperatures in the naturally crowded environment of the cell. The macromolecular resilience of bacteria increases with adaptation to high temperatures. Keywords Neutron scattering; Dynamics; Macromolecular adaptation; Extreme condition; Halophilic malate dehydrogenase; Bacterial adaptation Disciplines Life Sciences | Physical Sciences and Mathematics | Social and Behavioral Sciences Publication Details This article was originally published as Tehei, M, Adaptation to extreme environments: Macromolecular dynamics in complex systems, Biochimica et Biophysica Acta 1724(3), 2005, 404-410. Original article available here. This journal article is available at Research Online: https://ro.uow.edu.au/scipapers/113 Biochimica et Biophysica Acta 1724 (2005) 404 – 410 http://www.elsevier.com/locate/bba Minireview Adaptation to extreme environments: Macromolecular dynamics in complex systems Moeava Teheia,*, Giuseppe Zaccaib,c aINFM-OGG § CRS-SOFT, c/o Institut Laue-Langevin, 6 rue Jules Horowitz BP 156, 38042 Grenoble Cedex 9, France bInstitut Laue-Langevin, 6 rue Jules Horowitz BP 156, 38042 Grenoble Cedex 9, France cInstitut de Biologie Structurale, UMR 5075 CEA-CNRS-UJF, Laboratoire de Biophysique Mole´culaire, 41 rue Jules Horowitz, 38027 Grenoble Cedex 1, France Received 23 February 2005; received in revised form 3 May 2005; accepted 4 May 2005 Available online 31 May 2005 Abstract What we previously thought of as insurmountable physical and chemical barriers to life, we now see as yet another niche harbouring Fextremophiles_. Extremophiles and their macromolecules had to develop molecular mechanisms of adaptation to extreme physico–chemical conditions. Using neutron spectroscopy, we have demonstrated that molecular dynamics represents one of these molecular mechanisms of adaptation. To which extent do hyper-saline conditions and extreme temperatures influence molecular dynamics? First, molecular dynamics were analysed for halophilic malate dehydrogenase from Haloarcula marismortui (Hm MalDH) under different molar solvent salt concentration conditions influencing its stability. Secondly, mean macromolecular motions were measured in-vivo in psychrophile (Aquaspirillum arcticum), mesophile (Escherichia coli and Proteus mirabilis), thermophile (Thermus thermophilus), and hyperthermophile (Aquifex pyrofilus) bacteria. The mean constant force of Hm MalDH increases progessively with increasing stability. The results show that the molecular adaptation of Hm MalDH to hyper-saline conditions is achieved through an increasing resilience of its structure dominated by enthalpic mechanisms. The study of bacteria has provided tools to quantify the macromolecular adaptation to extreme temperatures in the naturally crowded environment of the cell. The macromolecular resilience of bacteria increases with adaptation to high temperatures. D 2005 Elsevier B.V. All rights reserved. Keywords: Neutron scattering; Dynamics; Macromolecular adaptation; Extreme condition; Halophilic malate dehydrogenase; Bacterial adaptation 1. Introduction enzymes catalyse the extraordinary range of biochemical reactions. A consensus has arisen that, to carry out their role The cell can be considered as the elementary unit of life. in and around the cell, enzymes adopt a specific tridimen- Genetic analysis of organisms leads to grouping them in sional structure and also specific atomic and molecular three distinct kingdoms: the eukaryotes (Eucarya) and two motions adapted to their biological function. Thus, they groups of prokaryotes, the eubacteria (Bacteria) and the were selected by evolution in relation to these properties. archaebacteria (Archaea). The concept of dynamics, from the Greek DoraALj, The cell is a complex system, its cytoplasm a crowded strength, pertains to forces. The forces that maintain environment of different macromolecules, of which proteins biological molecular structure and govern atomic motions are the main type, in terms of quantity and variety of in macromolecules are ‘‘weak’’ forces (hydrogen bonds, function. They constitute more than 50% of the dry weight ionic bonds, van der Waals, and hydrophobic interactions) of the cell. Their extraordinary variety makes possible the because their associated energies are similar to thermal diverse structural and functional cellular activities. Protein energy at usual temperatures. Fast atomic thermal motions on the picosecond to nanosecond timescale allow proteins to * Corresponding author. Tel.: +33 4 76207738; fax: +33 4 76207688. achieve the stability and motions, and, therefore, the E-mail address: [email protected] (M. Tehei). necessary rigidity and flexibility to perform their biological 0304-4165/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.bbagen.2005.05.007 M. Tehei, G. Zaccai / Biochimica et Biophysica Acta 1724 (2005) 404–410 405 functions (enzymatic activity, ion pump activity, ...) [1, 2]. improving their properties and stability at high temperature, Neutron spectroscopy is particularly adapted to the study of for example. Evaporite minerals (Jarosite, Kieserite) have these motions, because neutron wavelengths (åA˚ ) and been identified in the Meridiani region on Mars, which energies (åmeV) match, respectively, the amplitudes and suggests that at one time, there was a shallow ‘‘sea’’ or frequencies of molecular motions [1,3,4]. Furthermore, lake at that location [6,7]. Its chemistry was that of slightly neutron absorption is low for protein atoms and the radiation oxidising, strongly acidic water. On Earth, fossils are often penetrates deeply into the sample with negligible radiation found in evaporite deposits associated with lake beds [8,9]. damage. Important isotope effects, in particular for hydro- If traces of life exist in Martian Jarosite evaporite, the gen (H) and deuterium (D), make neutron scattering a very corresponding organisms will be likely to be adapted to an powerful technique in the study of water and complex acidic environment and will fall into the extremophile systems that can be selectively deuterium-labelled. category. Moreover, it is believed that on Mars, the process Organisms can thrive in what we call extreme environ- of lake and sea evaporation was prolonged enough to allow ments on Earth and perhaps elsewhere in the Solar System. a cellular life form to evolve in hyper-saline conditions. Macelroy [5] named these lovers (Fphilos_ to Greeks) of For such reasons, the study of the extremophile adaptation extreme environments Fextremophiles_. They had to adapt to has broad implication for exobiology. one or several physico–chemical extreme parameters: high This mini review concerns work from our laboratory on temperatures for thermophiles and hyperthermophiles that (i) the enzyme malate dehydrogenase from the extreme live above 60 -C near geysers and hydrothermal vents; halophilic Archaea Haloarcula marismortui (Hm MalDH) psychrophiles grow at temperatures below 15 -C, in glacier that were discovered in the Dead Sea and (ii) psychrophile, water and polar seas; halophiles thrive in hyper-saline mesophile, thermophile, and hyperthermophile bacterial environments like the Lac Rose in Senegal (Fig. 1). Other cells. Using neutron spectroscopy, we have demonstrated physico–chemical extreme parameters are, for example, high that molecular dynamics represents one of the molecular pressure, high radiation
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