Increased acid resistance of the archaeon, Metallosphaera sedula by adaptive laboratory evolution

Journal of Industrial Microbiology and Biotechnology

Volumn 43, Issue 10, 2016, Pages 1455-1465

  Ai, Chenbing ^a,b   McCarthy, Samuel ^a   Eckrich, Valerie ^a   Rudrappa, Deepak ^a   Qiu, Guanzhou ^b   Blum, Paul ^a  

^a UNIVERSITY OF NEBRASKA   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Acidity resistance; Enargite bioleaching; Genome re sequencing; Metallosphaera sedula; RNA sequencing; Transcriptional responses

Indexed keywords

ACID; PERMEASE; ARCHAEAL PROTEIN; COPPER;

ARCHAEON; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOLEACHING; CELL PH; CYTOPLASM; ENZYME MECHANISM; EVOLUTION; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENOMICS; METALLOSPHAERA SEDULA; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PSEUDOGENE; RNA SEQUENCE; TRANSCRIPTOMICS; WILD TYPE; DIRECTED MOLECULAR EVOLUTION; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HETEROTROPHY; METABOLISM; MUTATION; SULFOLOBALES;

ARCHAEAL PROTEINS; COPPER; DIRECTED MOLECULAR EVOLUTION; GENE EXPRESSION PROFILING; GENOMICS; HETEROTROPHIC PROCESSES; HYDROGEN-ION CONCENTRATION; MUTATION; SULFOLOBACEAE;

EID: 84982135080     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-016-1812-0     Document Type: Article

References (69)

1. Ai C, McCarthy S, Schackwitz W, Martin J, Lipzen A, Blum P (2015) Complete genome sequences of evolved arsenate-resistant Metallosphaera sedula strains. Genome Announc. doi:10.1128/genomeA.01142-15
2. Allen MB (1959) Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Mikrobiol 32:270–277
3. Auernik KS, Kelly RM (2008) Identification of components of electron transport chains in the extremely thermoacidophilic crenarchaeon Metallosphaera sedula through iron and sulfur compound oxidation transcriptomes. Appl Environ Microbiol 74:7723–7732
4. Batty JD, Rorke GV (2006) Development and commercial demonstration of the BioCOP™ thermophile process. Hydrometallurgy 83:83–89
5. Baykov AA, Tuominen HK, Lahti R (2011) The CBS domain: a protein module with an emerging prominent role in regulation. ACS Chem Biol 6:1156–1163
6. Beck JV (1967) The role of bacteria in copper mining operations. Biotechnol Bioeng 9:487–497
7. Brandl H (2001) Microbial leaching of metals. In: Rehm HJ, Reed G (eds) Biotechnology: special processes. Wiley, Weinheim, pp 191–224
8. Brierley C, Brierley J (1973) A chemoautotrophic and thermophilic microorganism isolated from an acid hot spring. Can J Microbiol 19:183–188
9. Brierley CL, Brierley JA (2013) Progress in bioleaching: part B: applications of microbial processes by the minerals industries. Appl Microbiol Biotechnol 97:7543–7552
10. Brierley JA (2008) A perspective on developments in biohydrometallurgy. Hydrometallurgy 94:2–7
11. Brock TD, Brock KM, Belly RT, Weiss RL (1972) Sulfolobus a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol 84:54–68
12. Cascales E, Fibriansah G, Kovács ÁT, Pool TJ, Boonstra M, Kuipers OP, Thunnissen A-MWH (2012) Crystal structures of two transcriptional regulators from Bacillus cereus define the conserved structural features of a PadR subfamily. PLoS One 7:e48015
13. Ding J, Zhang R, Yu Y, Jin D, Liang C, Yi Y, Zhu W, Xia J (2011) A novel acidophilic, thermophilic iron and sulfur-oxidizing archaeon isolated from a hot spring of tengchong, yunnan, China. Braz J Microbiol 42:514–525
14. Kostrewa Dirk, Zeller Mirijam E, Armache Karim-Jean, Seizl Martin, Leike Kristin, Thomm Michael, Cramer P (2009) RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature 462:323–330
15. Fagan MA, Ngoma IE, Chiume RA, Minnaar S, Sederman AJ, Johns ML, Harrison STL (2014) MRI and gravimetric studies of hydrology in drip irrigated heaps and its effect on the propagation of bioleaching micro-organisms. Hydrometallurgy 150:210–221
16. Friedrich T, Böttcher B (2004) The gross structure of the respiratory complex I: a lego system. Biochim Biophys Acta 1608:1–9
17. Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479:1–5
18. Fusek M, Liu X, Tang J (1990) Enzymic properties of thermopsin. J Biol Chem 265:1496–1501
19. Gauss GH, Benas P, Wiedenheft B, Young M, Douglas T, Lawrence CM (2006) Structure of the DPS-like protein from Sulfolobus solfataricus reveals a bacterioferritin-like dimetal binding site within a DPS-like dodecameric assembly. Biochemistry-US 45:10815–10827
20. Gebhard S, Busby JN, Fritz G, Moreland NJ, Cook GM, Lott JS, Baker EN, Money VA (2014) Crystal structure of PhnF, a GntR-family transcriptional regulator of phosphate transport in Mycobacterium smegmatis. J Bacteriol 196:3472–3481
21. Giaveno MA, Urbieta MS, Ulloa JR, González Toril E, Donati ER (2012) Physiologic versatility and growth flexibility as the main characteristics of a novel thermoacidophilic Acidianus strain isolated from Copahue geothermal area in Argentina. Microbial Ecol 65:336–346
22. Gleißner M, Kaiser U, Antonopoulos E, Schafer G (1997) The archaeal SoxABCD complex is a proton pump in Sulfolobus acidocaldarius. J Biol Chem 272:8417–8426
23. Goulbourne EJ, Matin M, Zychlinsky E, Matin A (1986) Mechanism of Δ pH maintenance in active and inactive cells of an obligately acidophilic bacterium. J Bacteriol 166:59–65
24. Gruber G, Manimekalai MSS, Mayer F, Muller V (2014) ATP synthases from archaea: the beauty of a molecular motor. Biochim Biophys Acta 1837:940–952
25. Halinen A-K, Rahunen N, Kaksonen AH, Puhakka JA (2009) Heap bioleaching of a complex sulfide ore. Hydrometallurgy 98:92–100
26. Hawkes RB, Franzmann PD, Plumb JJ (2006) Moderate thermophiles including “Ferroplasma cupricumulans” sp. nov. dominate an industrial-scale chalcocite heap bioleaching operation. Hydrometallurgy 83:229–236
27. He Z-G, Zhong H, Li Y (2004) Acidianus tengchongensis sp. nov., a new species of acidothermophilic archaeon isolated from an acidothermal spring. Curr Microbiol 48:159–163
28. Huber G, Spinnler C, Gambacorta A, Stetter KO (1989) Metallosphaera sedula gen. and sp. nov. represents a new genus of aerobic, metal-mobilizing, thermoacidophilic archaebacteria. Syst Appl Microbiol 12:38–47
29. Huber G, Stetter KO (1991) Sulfolobus metallicus, sp. nov., a novel strictly chemolithoautotrophic thermophilic archaeal species of metal-mobilizers. Syst Appl Microbiol 14:372–378
30. En Huillet, Velge P, Vallaeys T, Pardon P (2006) LadR, a new PadR-related transcriptional regulator from Listeria monocytogenes, negatively regulates the expression of the multidrug efflux pump MdrL. FEMS Microbiol Lett 254:87–94
31. Jan R-L, Wu J, Chaw S-M, Tsai C-W, Tsen S-D (1999) A novel species of thermoacidophilic archaeon, Sulfolobus yangmingensis sp. nov. Int J Syst Bacteriol 49:1809–1816
32. Kozubal MA, Dlakic M, Macur RE, Inskeep WP (2011) Terminal oxidase diversity and function in “Metallosphaera yellowstonensis”: gene expression and protein modeling suggest mechanisms of Fe(II) oxidation in the Sulfolobales. Appl Environ Microbiol 77:1844–1853
33. Levina N, Totemeyer S, Stokes NR, Louis P, Jones MA, Booth IR (1999) Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18:1730–1737
34. Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191
35. Liu LJ, You XY, Guo X, Liu SJ, Jiang CY (2010) Metallosphaera cuprina sp. nov., an acidothermophilic, metal-mobilizing archaeon. Int J Syst Evol Micr 61:2395–2400
36. Lubben M, Kolmerer B, Saraste M (1992) An archaebacterial terminal oxidase combines core structures of two mitochondrial respiratory complexes. EMBO J 11:805–812
37. Malcolm HR, Blount P, Maurer JA (2015) The mechanosensitive channel of small conductance (MscS) functions as a Jack-In-The Box. Biochem Biophys Acta 1848:159–166
38. Matin A (1999) pH Homeostasis in Acidophiles. In: Chadwick DJ, Cardew G (eds.) Novartis Foundation Symposium 221, Bacterial responses to pH, Wiley, New York, p 152–166
39. Maurer LM, Yohannes E, Bondurant SS, Radmacher M, Slonczewski JL (2004) pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J Bacteriol 187:304–319
40. McCarthy S, Ai C, Wheaton G, Tevatia R, Eckrich V, Kelly R, Blum P (2014) Role of an archaeal PitA transporter in the copper and arsenic resistance of Metallosphaera sedula, an extreme thermoacidophile. J Bacteriol 196:3562–3570
41. McCarthy S, Johnson T, Pavlik BJ, Payne S, Schackwitz W, Martin J, Lipzen A, Keffeler E, Blum P, Kostka JE (2016) Expanding the limits of thermoacidophily in the archaeon Sulfolobus solfataricus by adaptive evolution. Appl Environ Microbiol 82:857–867
42. Mccord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055
43. McDowall JS, Murphy BJ, Haumann M, Palmer T, Armstrong FA, Sargent F (2014) Bacterial formate hydrogenlyase complex. Proc Natl Acad Sci USA 111:E3948–E3956
44. Milcamps A, Struffi P, de Bruijn FJ (2001) The Sinorhizobium meliloti nutrient-deprivation-induced tyrosine degradation gene hmgA is controlled by a novel member of the arsR family of regulatory genes. Appl Environ Microbiol 67:2641–2648
45. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628
46. Mukherjee A, Wheaton GH, Blum PH, Kelly RM (2012) Uranium extremophily is an adaptive, rather than intrinsic, feature for extremely thermoacidophilic Metallosphaera species. Proc Natl Acad Sci USA 109(41):16702–16707
47. Peng TJ, Liu LJ, Liu C, Yang ZF, Liu SJ, Jiang CY (2014) Metallosphaera tengchongensis sp. nov., an acidothermophilic archaeon isolated from a hot spring. Int J Syst Evol Micr 65:537–542
48. Petersen J, Dixon DG (2002) Thermophilic heap leaching of a chalcopyrite concentrate. Miner Eng 15:777–785
49. Plumb JJ, Haddad CM, Gibson JAE, Franzmann PD (2007) Acidianus sulfidivorans sp. nov., an extremely acidophilic, thermophilic archaeon isolated from a solfatara on Lihir Island, Papua New Guinea, and emendation of the genus description. Int J Syst Evol Micr 57:1418–1423
50. Pradhan N, Nathsarma KC, Srinivasa Rao K, Sukla LB, Mishra BK (2008) Heap bioleaching of chalcopyrite: a review. Miner Eng 21:355–365
51. Ruan R, Liu X, Zou G, Chen J, Wen J, Wang D (2011) Industrial practice of a distinct bioleaching system operated at low pH, high ferric concentration, elevated temperature and low redox potential for secondary copper sulfide. Hydrometallurgy 108:130–135
52. Sakoh M, Ito K, Akiyama Y (2005) Proteolytic activity of HtpX, a membrane-bound and stress-controlled protease from Escherichia coli. J Biol Chem 280:33305–33310
53. Stookey LL (1970) Ferrozine-a new spectrophotometric reagent for iron. Anal Chem 42:779
54. Sun Y, MacRae T (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62:2460–2476
55. Suzuki T, Iwasaki T, Uzawa T, Hara K, Nemoto N, Kon T, Ueki T, Yamagishi A, Oshima T (2002) Sulfolobus tokodaii sp. nov. (f. Sulfolobus sp. strain 7), a new member of the genus Sulfolobus isolated from Beppu Hot Springs. Japan. Extremophiles 6:39–44
56. Takatsugi K, Sasaki K, Hirajima T (2011) Mechanism of the enhancement of bioleaching of copper from enargite by thermophilic iron-oxidizing archaea with the concomitant precipitation of arsenic. Hydrometallurgy 109:90–96
57. Takayanagi S, Kawasaki H, Sugimori K, Yamada T, Sugai A, Ito T, Yamasato K, Shioda M (1996) Sulfolobus hakonensis sp. nov., a novel species of acidothermophilic archaeon. Int J Syst Bacteriol 46:377–382
58. Tomitori H, Kashiwagi K, Igarashi K (2011) Structure and function of polyamine-amino acid antiporters CadB and PotE in Escherichia coli. Amino Acids 42:733–740
59. Tupikina OV, Minnaar SH, van Hille RP, van Wyk N, Rautenbach GF, Dew D, Harrison STL (2013) Determining the effect of acid stress on the persistence and growth of thermophilic microbial species after mesophilic colonisation of low grade ore in a heap leach environment. Miner Eng 53:152–159
60. 2 for the simultaneous determination of zinc and copper. Chemosphere 90:366–373
61. Watling HR (2006) The bioleaching of sulphide minerals with emphasis on copper sulphides—a review. Hydrometallurgy 84:81–108
62. Wiedenheft B, Mosolf J, Willits D, Yeager M, Dryden KA, Young M, Douglas T (2005) From the cover: an archaeal antioxidant: characterization of a Dps-like protein from Sulfolobus solfataricus. Proc Natl Acad Sci USA 102:10551–10556
63. Wilks JC, Kitko RD, Cleeton SH, Lee GE, Ugwu CS, Jones BD, BonDurant SS, Slonczewski JL (2008) Acid and base stress and transcriptomic responses in Bacillus subtilis. Appl Environ Microbiol 75:981–990
64. Wu A, Yin S, Qin W, Liu J, Qiu G (2009) The effect of preferential flow on extraction and surface morphology of copper sulphides during heap leaching. Hydrometallurgy 95:76–81
65. Yin S, Wu A, Hu K, Wang Y, Xue Z (2013) Visualization of flow behavior during bioleaching of waste rock dumps under saturated and unsaturated conditions. Hydrometallurgy 133:1–6
66. 3+. Curr Microbiol 53:406–411
67. You X-Y, Liu C, Wang S-Y, Jiang C-Y, Shah SA, Prangishvili D, She Q, Liu S-J, Garrett RA (2011) Genomic analysis of Acidianus hospitalis W1 a host for studying crenarchaeal virus and plasmid life cycles. Extremophiles 15:487–497
68. Yu R, Shi L, Gu G, Zhou D, You L, Chen M, Qiu G, Zeng W (2014) The shift of microbial community under the adjustment of initial and processing pH during bioleaching of chalcopyrite concentrate by moderate thermophiles. Bioresour Technol 162:300–307
69. Zaidi AH, Bakkes PJ, Lubelski J, Agustiandari H, Kuipers OP, Driessen AJM (2008) The ABC-type multidrug resistance transporter LmrCD is responsible for an extrusion-based mechanism of bile acid resistance in Lactococcus lactis. J Bacteriol 190:7357–7366