Abstract
Acidithiobacillus caldus plays an important role in commercial bioleaching. To understand how NaCl stress adaptation occurs in A. caldus, we grew A. caldus strain SM-1 in media containing high NaCl concentrations. SM-1 grew at concentrations of up to 1.0-mol L−1 NaCl, but growth was severely inhibited at higher concentrations. Proteomic analysis showed that SM-1 used multiple strategies to respond to NaCl stress. In addition to several heat-shock proteins, enzymes involved in proline biosynthesis increased under NaCl stress. In addition, two DNA-binding proteins and a third protein of unknown function (Atc_1291), which was subsequently identified as a putative single-stranded DNA-binding protein, were up-regulated in the presence of NaCl stress. These DNA-binding proteins might play a role in response to osmotic stress. Atc_1291 was cloned and expressed in Escherichia coli. Surprisingly, we found that E. coli BL21/pET28a-atc_1291 grew to higher cell densities than E. coli BL21/pET28a, regardless of NaCl stress. Homologs to Atc_1291 were identified in several groups of Proteobacteria. The role of Atc_1291 in enhancing cell growth needs further investigation.
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Valenzuela L, Chi A, Beard S et al (2006) Genomics, metagenomics and proteomics in biomining microorganisms. Biotechnol Adv 24:197–211
Gahan CS, Sundkvist JE, Sandstrom A (2009) A study on the toxic effects of chloride on the biooxidation efficiency of pyrite. J Hazard Mater 172:1273–1281
Dopson M, Halinen AK, Rahunen N et al (2008) Silicate mineral dissolution during heap bioleaching. Biotechnol Bioeng 99:811–820
Zammit CM, Mangold S, Jonna V et al (2012) Bioleaching in brackish waters-effect of chloride ions on the acidophile population and proteomes of model species. Appl Microbiol Biotechnol 93:319–329
Huber H, Stetter KO (1989) Thiobacillus prosperus sp. nov., represents a new group of halotolerant metal-mobilizing bacteria isolated from a marine geothermal field. Arch Microbiol 151:479–485
You XY, Guo X, Zheng HJ et al (2011) Unraveling the Acidithiobacillus caldus complete genome and its central metabolisms for carbon assimilation. J Genet Genomes 38:243–252
Okibe N, Gericke M, Hallberg KB et al (2003) Enumeration and characterization of acidophilic microorganisms isolated from a pilot plant stirred-tank bioleaching operation. Appl Environ Microbiol 69:1936–1943
Burton NP, Norris PR (2000) Microbiology of acidic, geothermal springs of montserrat: environmental rDNA analysis. Extremophiles 4:315–320
Spolaore P, Joulian C, Gouin J et al (2011) Relationship between bioleaching performance, bacterial community structure and mineralogy in the bioleaching of a copper concentrate in stirred-tank reactors. Appl Microbiol Biotechnol 89:441–448
Zeng W, Qiu G, Zhou H et al (2010) Community structure and dynamics of the free and attached microorganisms during moderately thermophilic bioleaching of chalcopyrite concentrate. Bioresour Technol 101:7079–7086
Chen ZW, Liu YY, Wu JF et al (2007) Novel bacterial sulfur oxygenase reductases from bioreactors treating gold-bearing concentrates. Appl Microbiol Biotechnol 74:688–698
Mangold S, Valdes J, Holmes DS et al (2011) Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus. Front Microbiol 2:16–18
Chen L, Ren Y, Lin J et al (2012) Acidithiobacillus caldus sulfur oxidation model based on transcriptome analysis between the wild type and sulfur oxygenase reductase defective mutant. PLoS One 7:e39470
Dopson M, Lindstrom R (1999) Potential role of Thiobacillus caldus in arsenopyrite bioleaching. Appl Environ Microbiol 65:36–40
Liljeqvist M, Rzhepishevska OI, Dopson M (2013) Gene identification and substrate regulation provide insights into sulfur accumulation during bioleaching with the psychrotolerant acidophile Acidithiobacillus ferrivorans. Appl Environ Microbiol 79:951–957
Romantsov T, Guan Z, Wood JM (2009) Cardiolipin and the osmotic stress responses of bacteria. Biochim Biophys Acta 1788:2092–2100
Hecker M, Farre JP, Volker U (2007) SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu Rev Microbiol 61:215–236
Hecker M, Schumann W, Volker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19:417–428
Qi SW, Chaudhry MT, Zhang Y et al (2007) Comparative proteomes of Corynebacterium glutamicum grown on aromatic compounds revealed novel proteins involved in aromatic degradation and a clear link between aromatic catabolism and gluconeogenesis via fructose-1,6-bisphosphatase. Proteomics 7:3775–3787
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binging. Anal Biochem 72:248–254
Zhang Y, Ma YF, Qi SW et al (2007) Responses to arsenate stress by Comamonas sp. strain CNB-1 at genetic and proteomic levels. Microbiology 153:3713–3721
Zhang Y, Zhu Y, Mao S et al (2010) Proteomic analyses to reveal the protective role of glutathione in resistance of Lactococcus lactis to osmotic stress. Appl Environ Microbiol 76:3177–3186
Mao SM, Luo YM, Zhang TR (2010) Proteome reference map and comparative proteomic analysis between a wild type Clostridium acetobutylicum DSM 1731 and its mutant with enhanced butanol tolerance and butanol yield. J Proteome Res 9:3046–3061
Wang Y, Su L, Zhang L et al (2012) Bioleaching of chalcopyrite by defined mixed moderately thermophilic consortium including a marine acidophilic halotolerant bacterium. Bioresour Technol 121:348–354
Yin H, Tang M, Zhou Z et al (2012) Distinctive heat-shock response of bioleaching microorganism Acidithiobacillus ferrooxidans observed using genome-wide microarray. Can J Microbiol 58:628–636
Wang J, Zhao C, Meng B et al (2007) The proteomic alterations of Thermoanaerobacter tengcongensis cultured at different temperatures. Proteomics 7:1409–1419
Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Res 53:121–147
Zaprasis A, Brill J, Thuring M et al (2013) Osmoprotection of Bacillus subtilis through import and proteolysis of proline-containing peptides. Appl Environ Microbiol 79:576–587
Daciene DAG, Alexandre MB, Tereza CVR et al (2013) Response to oxidative stress in Paracoccidioides yeast cells as determined by proteomic analysis. Microbes Infect 15:347–364
Empadinhas N, Costa MS (2008) Osmoadaptation mechanisms in prokaryotes: distribution of compatible solutes. Intern Microbiol 11:151–161
Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170:319–330
Rajendrakumar CSV, Suryanarayana T, Reddy AR (1997) DNA helix destabilization by proline and betaine: possible role in the salinity tolerance process. FEBS Lett 410:201–205
Wood JM, Bremer E, Csonka LN (2001) Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Phys A 130:437–460
Acknowledgments
This work was supported by the National High Technology Research and Development Program of China (2012AA061501), the National Key Basic Research and Development Program of China (2010CB630903) and the National Natural Sciences Foundation of China (31171234).
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Guo, X., Jiang, C., Luo, Y. et al. Proteomic and molecular investigations revealed that Acidithiobacillus caldus adopts multiple strategies for adaptation to NaCl stress. Chin. Sci. Bull. 59, 301–309 (2014). https://doi.org/10.1007/s11434-013-0039-y
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DOI: https://doi.org/10.1007/s11434-013-0039-y