Astrobiology Workshop, Macquarie University July 12-13 2001

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Genome Packaging and the Response to Environmental Stress in Hyperthermophilic Archaea

David Musgrave (Department of Biological Sciences, The University of Waikato, Private Bag 3105, Hamilton New Zealand)

For DNA to be used as an informational molecule it must exist in the cell on the edge of stability because all genomic processes require local controlled melting. This presents mechanistic opportunities and problems for genomic DNA from hyperthermophilic organisms whose unpackaged DNA could melt at optimal temperatures for growth. Hyperthermophilic microorganisms employ the novel positively supercoiling topoisomerase enzyme Reverse Gyrase (RG) to form positively supercoiled DNA that is intrinsically resistant to thermal denaturation. RG is presently the only archaeal gene that is uniquely found in hyperthermophiles and therefore is central to hypotheses suggesting a hypothermophilic origin of life. However suggestions that RG has evolved by the fusion of two pre-existing enzymes (1) has led to hypotheses for a lower temperature for the origin. However in addition to the action of topoisomerases, DNA topology can be manipulated significantly by DNA packaging. In the Euryarchaea minimal histone containing nucleosomes can adopt two alternate DNA topologies in a salt dependent manner (2). We have hypothesised that since internal salt concentrations are increased with increases in temperature, the genomic affects of temperature fluctuations could also be accommodated by changes in nucleosome organisation. Here I will present evidence for dynamic archaeal nucleosomes, discuss the contribution that archaeal nucleosomes make to the global regulation required for a response to stationary phase stress (3) and describe a number of recently identified archaeal genes that are also either induced or repressed by stress (4). A set of these genes, like reverse gyrase, is uniquely thermophilic in distribution and their promoters, like the histone genes, contain a putative heat shock element. Therefore the proteins that they encode might provide an alternate to RG allowing hyperthermophilic origins to be rekindled.

1. Declais, A.C., Marsault, J., Confalonieri, F. deLa Tour, C. B., and Duguet, M. (2000) Reverse gyrase, the two domains intimately co-operate to promote positive supercoiling. J.Biol Chem 275, 19498-19504

2. Musgrave, D.R., Slesarev A.L. and Forterre P. (2000) Negative constrained supercoiling in archaeal nucleosomes. Mol. Microbiol. 35, 341-349

3. Dinger, M.D., Baillie G. and Musgrave, D.R. (2000) Growth phase dependent expression and degradation of histones in the thermophillic archaeon Thermococcus zilligii. Mol Microbiol 36(4):876-85

4. Dinger, M.D. and Musgrave, D.R. (2000) Identification of archaeal genes encoding a novel stationary phase-response protein. Biochimica Biophysica Acta.1490, 115-120