Relationship among the secretion of extracellular polymeric substances, heat resistance, and bioleaching ability of Metallosphaera sedula

Abstract

This paper describes the investigation of the secretion of extracellular polymeric substances (EPS) by an extremely thermoacidophilic archaea, Metallosphaera sedula (M. sedula), during the bioleaching of pyrite under different temperatures and discusses the relationship among the EPS secretion, its heat resistance, and its ability to bioleach pyrite. The investigation results indicate that the amount of extracellular proteins is significantly higher than the amount of extracellular polysaccharides in the extracted EPS whether free cells or attached cells; these results are quite different from the behavior of mesophilic Acidithiobacillus ferrooxidans. Although the growth of M. sedula is inhibited at 80°C, the bioleaching ability of M. sedula is only slightly lower than that at the optimum growth temperature of 72°C because of the heat resistance mechanism based on EPS secretion. The secretion of more extracellular proteins is an important heat resistance mechanism of M. sedula.

Keywords

bioleaching / extracellular polymeric substances (EPS) / heat resistance / Metallosphaera sedula

References

[1] Vilcáez J, Suto K, Inoue C. Bioleaching of chalcopyrite with thermophiles: Temperature–pH–ORP dependence. Int. J. Miner. Process., 2008, 88, 37.

[2] Kurosawa N, Itoh YH, Itoh T. Reclassification of Sulfolobus hakonensis Takayanagi et al. 1996 as Metallosphaera hakonensis comb. nov. based on phylogenetic evidence and DNA G+C content. Int. J. Syst. Evol. Microbiol., 2003, 53, 1607.

[3] Sabath N, Ferrada E, Barve A, Wagner A. Growth temperature and genome size in bacteria are negatively correlated, suggesting genomic streamlining during thermal adaptation. Genome Biol. Evol., 2013, 5, 966.

[4] Hickey DA, Singer GAC. Genomic and proteomic adaptations to growth at high temperature. Genome Biol., 2004, 5, 117.

[5] Valdes J, Ossandon F, Quatrini R, Dopson M, Holmes DS. Draft genome sequence of the extremely acidophilic biomining bacterium Acidithiobacillus thiooxidans ATCC 19377 provides insights into the evolution of the Acidithiobacillus genus. J. Bacteriol., 2011, 193, 7003.

[6] Urbieta MS, Donati ER, Chan KG, Shahar S, Sin LL, Goh KM. Thermophiles in the genomic era: biodiversity, science, and applications. Biotechnol. Adv., 2015, 33, 633.

[7] Singer GAC, Hickey DA. Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. Gene, 2003, 317, 39.

[8] Lynn DJ, Singer GAC, Hickey DA. Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res., 2002, 30, 4272.

[9] Daniel RM, Cowan DA. Biomolecular stability and life at high temperatures. Cell. Mol. Life Sci., 2000, 57, 250.

[10] Wolfstein K, Stal LJ. Production of extracellular polymeric substances (EPS) by benthic diatoms: effect of irradiance and temperature. Mar. Ecol. Prog. Ser., 2002, 236, 13.

[11] Mckew BA, Taylor JD, McGenity TJ, Underwood GJC. Resistance and resilience of benthic biofilm communities from a temperate salt marsh to desiccation and rewetting. ISME J., 2011, 5, 30.

[12] Thornton DCO. Effect of low pH on carbohydrate production by a marine planktonic diatom (Chaetoceros muelleri). Res. Lett. Ecol., 2009

[13] Mezhoud N, Zili F, Bouzidi N, Helaoui F, Ammar J, Ouada HB. The effects of temperature and light intensity on growth, reproduction and EPS synthesis of a thermophilic strain related to the genus Graesiella. Bioprocess. Biosyst. Eng., 2014, 37, 2271.

[14] Mikkelsen D, Kappler U, Webb RI, Rasch R, McEwan AG, Sly LI. Visualisation of pyrite leaching by selected thermophilic archaea: Nature of microorganism–ore interactions during bioleaching. Hydrometallurgy, 2007, 88, 143.

[15] Yang Y, Liu WH, Bhargava SK, Zeng WM, Chen M. A XANES and XRD study of chalcopyrite bioleaching with pyrite. Miner. Eng., 2016, 89, 157.

[16] Zeng WM, Qiu GZ, Zhou HB, Liu XD, Chen M, Chao WL, Zhang CG, Peng JH. Characterization of extracellular polymeric substances extracted during the bioleaching of chalcopyrite concentrate. Hydrometallurgy, 2010, 100, 177.

[17] Houghton JI, Stephenson T. Effect of influent organic content on digested sludge extracellular polymer content and dewaterability. Water Res., 2002, 36, 3620.

[18] Wuertz S, Spaeth R, Hinderberger A, Griebe T, Flemming HC, Wilderer PA. A new method for extraction of extracellular polymeric substances from biofilms and activated sludge suitable for direct quantification of sorbed metals. Water Sci. Technol., 2001, 43, 25.

[19] Bourven I, Joussein E, Guibaud G. Characterisation of the mineral fraction in extracellular polymeric substances (EPS) from activated sludges extracted by eight different methods. Bioresour. Technol., 2011, 102, 7124.

[20] Liu H, Fang HHP. Extraction of extracellular polymeric substances (EPS) of sludges. J. Biotechnol., 2002, 95, 249.

[21] Domínguez L, Rodríguez M, Prats D. Effect of different extraction methods on bound EPS from MBR sludges: Part II: Influence of extraction methods over molecular weight distribution. Desalination, 2010, 262, 106.

[22] Liao BQ, Allen DG, Droppo IG, Leppard GG, Liss SN. Surface properties of sludge and their role in bioflocculation and settleability. Water Res., 2001, 35, 339.

[23] Yu RL, Hou CW, Liu AJ, Peng TJ, Xi MC, Wu WL, Shen L, Liu YD, Li JK, Yang F, Qiu GZ, Chen M, Zeng WM. Extracellular DNA enhances the adsorption of Sulfobacillus thermosulfidooxidans strain ST on chalcopyrite surface. Hydrometallurgy, 2018, 176, 97.

[24] Zhang WJ, Cao BD, Wang DS, Ma T, Yu DH. Variations in distribution and composition of extracellular polymeric substances (EPS) of biological sludge under potassium ferrate conditioning: Effects of pH and ferrate dosage. Biochem. Eng. J., 2016, 106, 37.

[25] Fu Y, Yang HY, Fang YJ, Zhang CZ. Determination of polysaccharide content in extracellular polymers of leaching bacteria. J. Cent. South Univ. Sci. Technol., 2010, 41, 1686

[26] Wu JF, Xi CW. Evaluation of different methods for extracting extracellular DNA from the biofilm matrix. Appl. Environ. Microbiol., 2009, 75, 5390.

[27] Yu RL, Liu AJ, Liu YN, Yu ZJ, Peng TJ, Wu WL, Shen L, Liu YD, Li JK, Liu XD, Qiu GZ, Chen M, Zeng WM. Evolution of sulfobacillus thermosulfidooxidans secreting alginate during bioleaching of chalcopyrite concentrate. J. Appl. Microbiol., 2017, 112, 1586.

[28] Hoffmann C, Leroy-Dudal J, Patel S, Gallet O, Pauthe E. Fluorescein isothiocyanate-labeled human plasma fibronectin in extracellular matrix remodeling. Anal. Biochem., 2008, 372, 62.

[29] He ZG, Yang YP, Zhou S, Hu YH, Zhong H. Effect of pyrite, elemental sulfur and ferrous ions on EPS production by metal sulfide bioleaching microbes. Trans. Nonferrous Met. Soc. China, 2014, 24, 1171.

[30] Yu RL, Liu J, Tan JX, Zeng WM, Shi LJ, Gu GH, Qin WQ, Qiu GZ. Effect of pH values on the extracellular polysaccharide secreted by Acidithiobacillus ferrooxidans during chalcopyrite bioleaching. Int. J. Miner. Metall. Mater., 2014, 21, 311.

[31] Yu ZJ, Yu RL, Liu AJ, Liu J, Zeng WM, Liu XD, Qiu GZ. Effect of pH values on extracellular protein and polysaccharide secretions of Acidithiobacillus ferrooxidans during chalcopyrite bioleaching. Trans. Nonferrous Met. Soc. China, 2017, 27, 406.