Heavy metal resistance in Cupriavidus metallidurans CH34 is governed by an intricate transcriptional network
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The soil bacterium Cupriavidus metallidurans CH34 contains a high number of heavy metal resistance genes making it an interesting model organism to study microbial responses to heavy metals. In this study the transcriptional response of strain CH34 was measured when challenged to sub-lethal concentrations of various essential or toxic metals. Based on the global transcriptional responses for each challenge and the overlap in upregulated genes between different metal responses, the sixteen metals were clustered in three groups. In addition, the transcriptional response of already known metal resistance genes was assessed, and new metal response gene clusters were identified. The majority of the studied metal response loci showed similar expression profiles when cells were exposed to different metals, suggesting complex interplay at transcriptional level between the different metal responses. The pronounced redundancy of these metal resistant regions—as illustrated by the large number of paralogous genes—combined with the phylogenetic distribution of these metal response regions within either evolutionary related or other metal resistant bacteria, provides important insights on the recent evolutionary forces shaping this naturally soil-dwelling bacterium into a highly metal-resistant strain well adapted to harsh and anthropogenic environments.
KeywordsTranscriptomics Cupriavidus metallidurans CH34 Transcriptional regulation Metal resistance Regulatory networks
This work is supported by internal funds of SCK·CEN and by the European Space Agency through the MESSAGE contracts (PRODEX agreements No. 90037 and 90094).
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300Google Scholar
- De Angelis F, Lee JK, O’Connell JD III, Miercke LJ, Verschueren KH, Srinivasan V, Bauvois C, Govaerts C, Robbins RA, Ruysschaert JM, Stroud RM, Vandenbussche G (2010) Metal-induced conformational changes in ZneB suggest an active role of membrane fusion proteins in efflux resistance systems. Proc Natl Acad Sci USA 107:11038–11043PubMedCrossRefGoogle Scholar
- Goris J, De Vos P, Coenye T, Hoste B, Janssens D, Brim H, Diels L, Mergeay M, Kersters K, Vandamme P (2001) Classification of metal-resistant bacteria from industrial biotopes as Ralstonia campinensis sp. nov., Ralstonia metallidurans sp. nov. and Ralstonia basilensis Steinle et al. 1998 emend. Int J Syst Evol Microbiol 51:1773–1782PubMedCrossRefGoogle Scholar
- Hobman JL, Yamamoto K, Oshima T (2007) Transcriptomic responses of bacterial cells to sublethal metal ion stress. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals. Springer Verlag Microbial Monographs. Springer, Berlin, pp 73–116Google Scholar
- Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A, Monchy S, Medigue C, Taghavi S, McCorkle S, Dunn J, van der Lelie D, Mergeay M (2010) The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS ONE 5:e10433PubMedCrossRefGoogle Scholar
- Mergeay M, Monchy S, Janssen P, Van Houdt R, Leys N (2009) Megaplasmids in Cupriavidus Genus and Metal Resistance In: Schwartz E (ed) Microbial Megaplasmids, vol 11. vol Microbiology Monographs. Springer, Berlin, pp 209–238Google Scholar
- Monchy S, Benotmane MA, Wattiez R, van Aelst S, Auquier V, Borremans B, Mergeay M, Taghavi S, van der Lelie D, Vallaeys T (2006) Transcriptomic and proteomic analyses of the pMOL30-encoded copper resistance in Cupriavidus metallidurans strain CH34. Microbiology 152:1765–1776PubMedCrossRefGoogle Scholar
- Reith F, Etschmann B, Grosse C, Moors H, Benotmane MA, Monsieurs P, Grass G, Doonan C, Vogt S, Lai B, Martinez-Criado G, George GN, Nies DH, Mergeay M, Pring A, Southam G, Brugger J (2009) Mechanisms of gold biomineralization in the bacterium Cupriavidus metallidurans. Proc Natl Acad Sci USA 106:17757–17762PubMedCrossRefGoogle Scholar
- Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article3Google Scholar