Advertisement

Chinese Science Bulletin

, Volume 59, Issue 3, pp 301–309 | Cite as

Proteomic and molecular investigations revealed that Acidithiobacillus caldus adopts multiple strategies for adaptation to NaCl stress

  • Xu Guo
  • Chengying JiangEmail author
  • Yuanming Luo
  • Mingjiang Zhang
  • Ansgar Poetsch
  • Shuangjiang LiuEmail author
Article Microbiology

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.

Keywords

Acidithiobacillus caldus SM-1 NaCl stress Proline Single-stranded DNA-binding proteins Bioleaching 

Notes

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).

References

  1. 1.
    Valenzuela L, Chi A, Beard S et al (2006) Genomics, metagenomics and proteomics in biomining microorganisms. Biotechnol Adv 24:197–211CrossRefGoogle Scholar
  2. 2.
    Gahan CS, Sundkvist JE, Sandstrom A (2009) A study on the toxic effects of chloride on the biooxidation efficiency of pyrite. J Hazard Mater 172:1273–1281CrossRefGoogle Scholar
  3. 3.
    Dopson M, Halinen AK, Rahunen N et al (2008) Silicate mineral dissolution during heap bioleaching. Biotechnol Bioeng 99:811–820CrossRefGoogle Scholar
  4. 4.
    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 93:319–329CrossRefGoogle Scholar
  5. 5.
    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 151:479–485CrossRefGoogle Scholar
  6. 6.
    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 38:243–252CrossRefGoogle Scholar
  7. 7.
    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 69:1936–1943CrossRefGoogle Scholar
  8. 8.
    Burton NP, Norris PR (2000) Microbiology of acidic, geothermal springs of montserrat: environmental rDNA analysis. Extremophiles 4:315–320CrossRefGoogle Scholar
  9. 9.
    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 89:441–448CrossRefGoogle Scholar
  10. 10.
    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 101:7079–7086Google Scholar
  11. 11.
    Chen ZW, Liu YY, Wu JF et al (2007) Novel bacterial sulfur oxygenase reductases from bioreactors treating gold-bearing concentrates. Appl Microbiol Biotechnol 74:688–698CrossRefGoogle Scholar
  12. 12.
    Mangold S, Valdes J, Holmes DS et al (2011) Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus. Front Microbiol 2:16–18CrossRefGoogle Scholar
  13. 13.
    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:e39470CrossRefGoogle Scholar
  14. 14.
    Dopson M, Lindstrom R (1999) Potential role of Thiobacillus caldus in arsenopyrite bioleaching. Appl Environ Microbiol 65:36–40Google Scholar
  15. 15.
    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 79:951–957CrossRefGoogle Scholar
  16. 16.
    Romantsov T, Guan Z, Wood JM (2009) Cardiolipin and the osmotic stress responses of bacteria. Biochim Biophys Acta 1788:2092–2100CrossRefGoogle Scholar
  17. 17.
    Hecker M, Farre JP, Volker U (2007) SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu Rev Microbiol 61:215–236CrossRefGoogle Scholar
  18. 18.
    Hecker M, Schumann W, Volker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19:417–428CrossRefGoogle Scholar
  19. 19.
    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 7:3775–3787CrossRefGoogle Scholar
  20. 20.
    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 72:248–254CrossRefGoogle Scholar
  21. 21.
    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 153:3713–3721CrossRefGoogle Scholar
  22. 22.
    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 76:3177–3186CrossRefGoogle Scholar
  23. 23.
    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 9:3046–3061CrossRefGoogle Scholar
  24. 24.
    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 121:348–354CrossRefGoogle Scholar
  25. 25.
    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 58:628–636CrossRefGoogle Scholar
  26. 26.
    Wang J, Zhao C, Meng B et al (2007) The proteomic alterations of Thermoanaerobacter tengcongensis cultured at different temperatures. Proteomics 7:1409–1419CrossRefGoogle Scholar
  27. 27.
    Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Res 53:121–147Google Scholar
  28. 28.
    Zaprasis A, Brill J, Thuring M et al (2013) Osmoprotection of Bacillus subtilis through import and proteolysis of proline-containing peptides. Appl Environ Microbiol 79:576–587CrossRefGoogle Scholar
  29. 29.
    Daciene DAG, Alexandre MB, Tereza CVR et al (2013) Response to oxidative stress in Paracoccidioides yeast cells as determined by proteomic analysis. Microbes Infect 15:347–364CrossRefGoogle Scholar
  30. 30.
    Empadinhas N, Costa MS (2008) Osmoadaptation mechanisms in prokaryotes: distribution of compatible solutes. Intern Microbiol 11:151–161Google Scholar
  31. 31.
    Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170:319–330CrossRefGoogle Scholar
  32. 32.
    Rajendrakumar CSV, Suryanarayana T, Reddy AR (1997) DNA helix destabilization by proline and betaine: possible role in the salinity tolerance process. FEBS Lett 410:201–205CrossRefGoogle Scholar
  33. 33.
    Wood JM, Bremer E, Csonka LN (2001) Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Phys A 130:437–460CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.State Key Laboratory of Microbial Resources, Institute of MicrobiologyChinese Academy of SciencesBeijingChina
  2. 2.Environmental Microbiology and Biotechnology Research Center, Institute of MicrobiologyChinese Academy of SciencesBeijingChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.Lehrstuhl for Biochemie der PflanzenRuhr UniversitaetBochumGermany

Personalised recommendations