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Open Access Publications from the University of California

Key metabolites and mechanistic changes for salt tolerance in an experimentally evolved sulfate-reducing bacterium, desulfovibrio vulgaris

  • Author(s): Zhou, A
  • Lau, R
  • Baran, R
  • Ma, J
  • Von Netzer, F
  • Shi, W
  • Gorman-Lewis, D
  • Kempher, ML
  • He, Z
  • Qin, Y
  • Shi, Z
  • Zane, GM
  • Wu, L
  • Bowen, BP
  • Northen, TR
  • Hillesland, KL
  • Stahl, DA
  • Wall, JD
  • Arkin, AP
  • Zhoua, J
  • et al.

© 2017 Zhou et al. Rapid genetic and phenotypic adaptation of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough to salt stress was observed during experimental evolution. In order to identify key metabolites important for salt tolerance, a clone, ES10-5, which was isolated from population ES10 and allowed to experimentally evolve under salt stress for 5,000 generations, was analyzed and compared to clone ES9-11, which was isolated from population ES9 and had evolved under the same conditions for 1,200 generations. These two clones were chosen because they represented the best-adapted clones among six independently evolved populations. ES10-5 acquired new mutations in genes potentially involved in salt tolerance, in addition to the preexisting mutations and different mutations in the same genes as in ES9-11. Most basal abundance changes of metabolites and phospholipid fatty acids (PLFAs) were lower in ES10-5 than ES9-11, but an increase of glutamate and branched PLFA i17:1_9c under high-salinity conditions was persistent. ES9-11 had decreased cell motility compared to the ancestor; in contrast, ES10-5 showed higher cell motility under both nonstress and high-salinity conditions. Both genotypes displayed better growth energy efficiencies than the ancestor under nonstress or highsalinity conditions. Consistently, ES10-5 did not display most of the basal transcriptional changes observed in ES9-11, but it showed increased expression of genes involved in glutamate biosynthesis, cation efflux, and energy metabolism under high salinity. These results demonstrated the role of glutamate as a key osmolyte and i17: 1_9c as the major PLFA for salt tolerance in D. vulgaris. The mechanistic changes in evolved genotypes suggested that growth energy efficiency might be a key factor for selection. IMPORTANCE High salinity (e.g., elevated NaCl) is a stressor that affects many organisms. Salt tolerance, a complex trait involving multiple cellular pathways, is attractive for experimental evolutionary studies. Desulfovibrio vulgaris Hildenborough is a model sulfate-reducing bacterium (SRB) that is important in biogeochemical cycling of sulfur, carbon, and nitrogen, potentially for bio-corrosion, and for bioreme-diation of toxic heavy metals and radionuclides. The coexistence of SRB and high salinity in natural habitats and heavy metal-contaminated field sites laid the foundation for the study of salt adaptation of D. vulgaris Hildenborough with experimental evolution. Here, we analyzed a clone that evolved under salt stress for 5,000 generations and compared it to a clone evolved under the same condition for 1,200 generations. The results indicated the key roles of glutamate for osmoprotection and of i17:1_9c for increasing membrane fluidity during salt adaptation. The findings provide valuable insights about the salt adaptation mechanism changes during long-term experimental evolution.

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