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Salt Stress in Desulfovibrio vulgaris Hildenborough: an Integrated Genomics Approach

Aindrila Mukhopadhyay,^1,2, Zhili He,^1,4 Eric J. Alm,^1,2 Adam P. Arkin,^1,2,7 Edward E. Baidoo,^1,2 Sharon C. Borglin,^1,3 Wenqiong Chen,^1,6 Terry C. Hazen,^1,3 Qiang He,^1,4 Hoi-Ying Holman,^1,3 Katherine Huang,^1,2 Rick Huang,^1,3 Dominique C. Joyner,^1,3 Natalie Katz,^1,3 Martin Keller,^1,6 Paul Oeller,^1,6 Alyssa Redding,^1,7 Jun Sun,^1,6 Judy Wall,^1,5 Jing Wei,^1,6 Zamin Yang,^1,4 Huei-Che Yen,^1,5 Jizhong Zhou,^1,4 and Jay D. Keasling^1,2,7*

Virtual Institute of Microbial Stress and Survival,¹ Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California,² Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California,³ Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee,⁴ Biochemistry and Molecular Microbiology & Immunology Departments, University of Missouri, Columbia, Missouri,⁵ Diversa Inc., San Diego, California,⁶ Departments of Chemical Engineering and Bioengineering, University of California, Berkeley, California⁷

Received 15 December 2005/ Accepted 14 March 2006

The ability of Desulfovibrio vulgaris Hildenborough to reduce, and therefore contain, toxic and radioactive metal waste has made all factors that affect the physiology of this organism of great interest. Increased salinity is an important and frequent fluctuation faced by D. vulgaris in its natural habitat. In liquid culture, exposure to excess salt resulted in striking elongation of D. vulgaris cells. Using data from transcriptomics, proteomics, metabolite assays, phospholipid fatty acid profiling, and electron microscopy, we used a systems approach to explore the effects of excess NaCl on D. vulgaris. In this study we demonstrated that import of osmoprotectants, such as glycine betaine and ectoine, is the primary mechanism used by D. vulgaris to counter hyperionic stress. Several efflux systems were also highly up-regulated, as was the ATP synthesis pathway. Increases in the levels of both RNA and DNA helicases suggested that salt stress affected the stability of nucleic acid base pairing. An overall increase in the level of branched fatty acids indicated that there were changes in cell wall fluidity. The immediate response to salt stress included up-regulation of chemotaxis genes, although flagellar biosynthesis was down-regulated. Other down-regulated systems included lactate uptake permeases and ABC transport systems. The results of an extensive NaCl stress analysis were compared with microarray data from a KCl stress analysis, and unlike many other bacteria, D. vulgaris responded similarly to the two stresses. Integration of data from multiple methods allowed us to develop a conceptual model for the salt stress response in D. vulgaris that can be compared to those in other microorganisms.

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