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The Biofilm Lifestyle of Acidophilic Metal/Sulfur-Oxidizing Microorganisms

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Biotechnology of Extremophiles:

Part of the book series: Grand Challenges in Biology and Biotechnology ((GCBB,volume 1))

Abstract

Microrganisms are well known for their unique ability to thrive in different lifestyles (e.g. planktonic or sessile) and environments, even within extreme ones. The most common and widespread lifestyle of microbes on earth is in form of biofilms, associated colonies of microorganisms embedded in a matrix of extracellular polymeric substances (EPS). Extremely acidophilic metal/sulfur-oxidizing microorganisms (AMOM) thrive in special ecological niches characterized by harsh conditions such as low pH (below 3) and high concentration of heavy metals across a broad range of temperatures. The molecular mechanisms controlling biofilm formation in acidophilic leaching bacteria are starting to be elucidated while these operating in archaea are far less explored. In this chapter we provide an overview about the biofilm lifestyle of AMOM. This includes surface sciences, microscopy, cell-cell communication, interspecies interactions as well as molecular and high-throughput studies. Current knowledge on the EPS composition and biofilm visualization of acidophiles is also included. Future perspectives in this field include the elucidation of EPS biosynthesis pathways and a comprehensive analysis of the chemical nature of the EPS polymers. Cell-cell communication and microbial interactions within multispecies biofilms of acidophiles are considered to be crucial determinants in controlling the metabolic activity of AMOM. Either for their biotechnological applications in biomining or in mitigation of acid mine drainage (AMD) generation, further studies in both fields may presumably reveal key perspectives to influence and control bioleaching of sulfide minerals.

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References

  • Acuña J, Rojas J, Amaro AM, Toledo H, Jerez CA (1992) Chemotaxis of Leptospirillum ferrooxidans and other acidophilic chemolithotrophs: comparison with the Escherichia coli chemosensory system. FEMS Microbiol Lett 75:37–42

    Article  PubMed  Google Scholar 

  • Africa C-J, van Hille RP, Sand W, Harrison ST (2013) Investigation and in situ visualisation of interfacial interactions of thermophilic microorganisms with metal-sulphides in a simulated heap environment. Miner Eng 48:100–107

    Article  CAS  Google Scholar 

  • Aliaga Goltsman DS, Comolli LR, Thomas BC, Banfield JF (2015) Community transcriptomics reveals unexpected high microbial diversity in acidophilic biofilm communities. ISME J 9:1014–1023

    Article  CAS  PubMed  Google Scholar 

  • Alvarez S, Jerez CA (2004) Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans. Appl Environ Microbiol 70:5177–5182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amaro AM, Seeger M, Arredondo R, Moreno M, Jerez CA (1993) The growth conditions affect Thiobacillus ferrooxidans attachment to solids. In: Torma AE, Apel ML, Brierley CL (eds) Biohydrometallurgical technologies. The Minerals, Metals & Materials Society, Warrendale, PA pp 577–585

    Google Scholar 

  • Amikam D, Galperin MY (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3–6

    Article  CAS  PubMed  Google Scholar 

  • Andrews GF (1988) The selective adsorption of Thiobacilli to dislocation sites on pyrite surfaces. Biotechnol Bioeng 31:378–381

    Article  CAS  PubMed  Google Scholar 

  • Baffico GD, Diaz MM, Wenzel MT, Koschorreck M, Schimmele M, Neu TR, Pedrozo F (2004) Community structure and photosynthetic activity of epilithon from a highly acidic (pH ≤ 2) mountain stream in Patagonia, Argentina. Extremophiles 8:463–473

    Article  CAS  PubMed  Google Scholar 

  • Bagdigian RM, Myerson AS (1986) The adsorption of Thiobacillus ferrooxidans on coal surfaces. Biotechnol Bioeng 28:467–479

    Article  CAS  PubMed  Google Scholar 

  • Baker-Austin C, Potrykus J, Wexler M, Bond P, Dopson M (2010) Biofilm development in the extremely acidophilic archaeon ‘Ferroplasma acidarmanus’ Fer1. Extremophiles 14:485–491

    Article  PubMed  Google Scholar 

  • Baldensperger J, Guarraia L, Humphreys W (1974) Scanning electron microscopy of thiobacilli grown on colloidal sulfur. Arch Microbiol 99:323–329

    Article  CAS  PubMed  Google Scholar 

  • Banderas A, Guiliani N (2013) Bioinformatic prediction of gene functions regulated by quorum sensing in the bioleaching bacterium Acidithiobacillus ferrooxidans. Int J Mol Sci 14:16901–16916

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barreto M, Jedlicki E, Holmes DS (2005) Identification of a gene cluster for the formation of extracellular polysaccharide precursors in the chemolithoautotroph Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71:2902–2909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker T, Gorham N, Shiers D, Watling H (2011) In situ imaging of Sulfobacillus thermosulfidooxidans on pyrite under conditions of variable pH using tapping mode atomic force microscopy. Process Biochem 46:966–976

    Article  CAS  Google Scholar 

  • Bellenberg S, Vera M, Sand W (2011) Transcriptomic studies of capsular polysaccharide export systems involved in biofilm formation by Acidithiobacillus ferrooxidans. In: Qiu GZ, Jiang T, Qin WQ, Liu XD, Yang Y, Wang HD (eds) Biohydrometallurgy: Biotech Key to Unlock Mineral Resources Value: Proceedings of the 19th International Biohydrometallurgy Symposium. Central South University Press, Changsha, China, pp 460–464

    Google Scholar 

  • Bellenberg S, Leon-Morales C-F, Sand W, Vera M (2012) Visualization of capsular polysaccharide induction in Acidithiobacillus ferrooxidans. Hydrometallurgy 129–130:82–89

    Article  CAS  Google Scholar 

  • Bellenberg S, Diaz M, Noel N, Sand W, Poetsch A, Guiliani N, Vera M (2014) Biofilm formation, communication and interactions of leaching bacteria during colonization of pyrite and sulfur surfaces. Res Microbiol 165:773–781

    Article  CAS  PubMed  Google Scholar 

  • Bellenberg S, Barthen R, Boretska M, Zhang R, Sand W, Vera M (2015) Manipulation of pyrite colonization and leaching by iron-oxidizing Acidithiobacillus species. Appl Microbiol Biotechnol 99:1435–1449

    Article  CAS  PubMed  Google Scholar 

  • Belnap CP, Pan C, VerBerkmoes NC, Power ME, Samatova NF, Carver RL, Hettich RL, Banfield JF (2010) Cultivation and quantitative proteomic analyses of acidophilic microbial communities. ISME J 4:520–530

    Article  CAS  PubMed  Google Scholar 

  • Belnap CP, Pan C, Denef VJ, Samatova NF, Hettich RL, Banfield JF (2011) Quantitative proteomic analyses of the response of acidophilic microbial communities to different pH conditions. ISME J 5:1152–1161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, Haagensen JA, Molin S, Prensier G, Arbeille B, Ghigo JM (2004) Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51:659–674

    Article  CAS  PubMed  Google Scholar 

  • Bennke CM, Neu TR, Fuchs BM, Amann R (2013) Mapping glycoconjugate-mediated interactions of marine Bacteroidetes with diatoms. Syst Appl Microbiol 36:417–425

    Article  CAS  PubMed  Google Scholar 

  • Blake RC, Howard GT, McGinness S (1994) Enhanced yields of iron-oxidizing bacteria by in situ electrochemical reduction of soluble iron in the growth medium. Appl Environ Microbiol 60:2704–2710

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bond PL, Druschel GK, Banfield JF (2000a) Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl Environ Microbiol 66:4962–4971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bond PL, Smriga SP, Banfield JF (2000b) Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm at an extreme acid mine drainage site. Appl Environ Microbiol 66:3842–3849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brockmann S, Arnold T, Schweder B, Bernhard G (2010) Visualizing acidophilic microorganisms in biofilm communities using acid stable fluorescence dyes. J Fluoresc 20:943–951

    Article  CAS  PubMed  Google Scholar 

  • Bryant R, McGroarty K, Costerton J, Laishley E (1983) Isolation and characterization of a new acidophilic Thiobacillus species (T. albertis). Can J Microbiol 29:1159–1170

    Article  Google Scholar 

  • Bryant R, Costerton J, Laishley E (1984) The role of Thiobacillus albertis glycocalyx in the adhesion of cells to elemental sulfur. Can J Microbiol 30:81–90

    Article  CAS  PubMed  Google Scholar 

  • Castelle C, Guiral M, Malarte G, Ledgham F, Leroy G, Brugna M, Giudici-Orticoni M-T (2008) A new iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans. J Biol Chem 283:25803–25811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro L, Zhang R, Muñoz JA, González F, Blázquez ML, Sand W, Ballester A (2014) Characterization of exopolymeric substances (EPS) produced by Aeromonas hydrophila under reducing conditions. Biofouling 30:501–511

    Article  CAS  PubMed  Google Scholar 

  • Castro M, Deane SM, Ruiz L, Rawlings DE, Guiliani N (2015) Diguanylate cyclase null mutant reveals that C-Di-GMP pathway regulates the motility and adherence of the extremophile bacterium Acidithiobacillus caldus. PLoS One 10, e0116399

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cha C, Gao P, Chen Y-C, Shaw PD, Farrand SK (1998) Production of Acyl-homoserine lactone Quorum-sensing signals by Gram-negative plant-associated bacteria. Mol Plant-Microbe Interact 11:1119–1129

    Article  CAS  PubMed  Google Scholar 

  • Choudhary S, Schmidt-Dannert C (2010) Applications of quorum sensing in biotechnology. Appl Microbiol Biotechnol 86:1267–1279

    Article  CAS  PubMed  Google Scholar 

  • Clark DA, Norris PR (1996) Acidimicrobium ferrooxidans gen. nov., sp. nov.: mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142:785–790

    Article  CAS  Google Scholar 

  • Crescenzi F, Crisari A, D’Angel E, Nardella A (2006) Control of acidity development on solid sulfur due to bacterial action. Environ Sci Technol 40:6782–6786

    Article  CAS  PubMed  Google Scholar 

  • Crundwell F (2013) The dissolution and leaching of minerals: mechanisms, myths and misunderstandings. Hydrometallurgy 139:132–148

    Article  CAS  Google Scholar 

  • d’Hugues P, Joulian C, Spolaore P, Michel C, Garrido F, Morin D (2008) Continuous bioleaching of a pyrite concentrate in stirred reactors: Population dynamics and exopolysaccharide production vs. bioleaching performance. Hydrometallurgy 94:34–41

    Article  CAS  Google Scholar 

  • Danhorn T, Hentzer M, Givskov M, Parsek MR, Fuqua C (2004) Phosphorus limitation enhances biofilm formation of the plant pathogen Agrobacterium tumefaciens through the PhoR-PhoB regulatory system. J Bacteriol 186:4492–4501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Decho AW, Frey RL, Ferry JL (2010) Chemical challenges to bacterial AHL signaling in the environment. Chem Rev 111:86–99

    Article  PubMed  CAS  Google Scholar 

  • Denef VJ, VerBerkmoes NC, Shah MB, Abraham P, Lefsrud M, Hettich RL, Banfield JF (2009) Proteomics-inferred genome typing (PIGT) demonstrates inter-population recombination as a strategy for environmental adaptation. Environ Microbiol 11:313–325

    Article  CAS  PubMed  Google Scholar 

  • Denef VJ, Mueller RS, Banfield JF (2010) AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J 4:599–610

    Article  PubMed  Google Scholar 

  • Diao M, Taran E, Mahler S, Nguyen AV (2014a) A concise review of nanoscopic aspects of bioleaching bacteria–mineral interactions. Adv Colloid Interface Sci 212:45–63

    Article  CAS  PubMed  Google Scholar 

  • Diao M, Taran E, Mahler SM, Nguyen AV (2014b) Comparison and evaluation of immobilization methods for preparing bacterial probes using acidophilic bioleaching bacteria Acidithiobacillus thiooxidans for AFM studies. J Microbiol Methods 102:12–14

    Article  CAS  PubMed  Google Scholar 

  • Dispirito AA, Dugan PR, Tuovinen OH (1983) Sorption of Thiobacillus ferrooxidans to particulate material. Biotechnol Bioeng 25:1163–1168

    Article  CAS  PubMed  Google Scholar 

  • Dopson M, Johnson DB (2012) Biodiversity, metabolism and applications of acidophilic sulfur‐metabolizing microorganisms. Environ Microbiol 14:2620–2631

    Article  CAS  PubMed  Google Scholar 

  • Dopson M, Baker-Austin C, Hind A, Bowman JP, Bond PL (2004) Characterization of Ferroplasma isolates and Ferroplasma acidarmanus sp. nov., extreme acidophiles from acid mine drainage and industrial bioleaching environments. Appl Environ Microbiol 70:2079–2088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dufrêne YF (2003) Recent progress in the application of atomic force microscopy imaging and force spectroscopy to microbiology. Curr Opin Microbiol 6:317–323

    Article  PubMed  CAS  Google Scholar 

  • Dziurla MA, Achouak W, Lam BT, Heulin T, Berthelin J (1998) Enzyme-linked immunofiltration assay to estimate attachment of thiobacilli to pyrite. Appl Environ Microbiol 64:2937–2942

    CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards KJ, Schrenk MO, Hamers R, Banfield JF (1998) Microbial oxidation of pyrite; experiments using microorganisms from an extreme acidic environment. Am Mineral 83:1444–1453

    Article  CAS  Google Scholar 

  • Edwards KJ, Gihring TM, Banfield JF (1999a) Seasonal variations in microbial populations and environmental conditions in an extreme acid mine drainage environment. Appl Environ Microbiol 65:3627–3632

    CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards KJ, Goebel BM, Rodgers TM, Schrenk MO, Gihring TM, Cardona MM, Mcguire MM, Hamers RJ, Pace NR, Banfield JF (1999b) Geomicrobiology of pyrite (FeS2) dissolution: case study at Iron Mountain, California. Geomicrobiol J 16:155–179

    Article  CAS  Google Scholar 

  • Edwards KJ, Bond PL, Banfield JF (2000a) Characteristics of attachment and growth of Thiobacillus caldus on sulphide minerals: a chemotactic response to sulphur minerals? Environ Microbiol 2:324–332

    Article  CAS  PubMed  Google Scholar 

  • Edwards KJ, Bond PL, Gihring TM, Banfield JF (2000b) An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287:1796–1799

    Article  CAS  PubMed  Google Scholar 

  • Edwards KJ, Hu B, Hamers RJ, Banfield JF (2001) A new look at microbial leaching patterns on sulfide minerals. FEMS Microbiol Ecol 34:197–206

    Article  CAS  PubMed  Google Scholar 

  • Espejo RT, Romero P (1987) Growth of Thiobacillus ferrooxidans on elemental sulfur. Appl Environ Microbiol 53:1907–1912

    CAS  PubMed  PubMed Central  Google Scholar 

  • Etzel K, Klingl A, Huber H, Rachel R, Schmalz G, Thomm M, Depmeier W (2008) Etching of {111} and {210} synthetic pyrite surfaces by two archaeal strains, Metallosphaera sedula and Sulfolobus metallicus. Hydrometallurgy 94:116–120

    Article  CAS  Google Scholar 

  • Farah C, Vera M, Morin D, Haras D, Jerez CA, Guiliani N (2005) Evidence for a functional quorum-sensing type AI-1 system in the extremophilic bacterium Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71:7033–7040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer CR, Wilmes P, Bowen BP, Northen TR, Banfield JF (2012) Deuterium-exchange metabolomics identifies N-methyl lyso phosphatidylethanolamines as abundant lipids in acidophilic mixed microbial communities. Metabolomics 8:566–578

    Article  CAS  Google Scholar 

  • Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  PubMed  Google Scholar 

  • Florian B, Noël N, Sand W (2010) Visualization of initial attachment of bioleaching bacteria using combined atomic force and epifluorescence microscopy. Miner Eng 23:532–535

    Article  CAS  Google Scholar 

  • Florian B, Noël N, Thyssen C, Felschau I, Sand W (2011) Some quantitative data on bacterial attachment to pyrite. Miner Eng 24:1132–1138

    Article  CAS  Google Scholar 

  • Galloway WR, Hodgkinson JT, Bowden S, Welch M, Spring DR (2012) Applications of small molecule activators and inhibitors of quorum sensing in Gram-negative bacteria. Trends Microbiol 20:449–458

    Article  CAS  PubMed  Google Scholar 

  • García-Moyano A, González-Toril E, Aguilera A, Amils R (2007) Prokaryotic community composition and ecology of floating macroscopic filaments from an extreme acidic environment, Rio Tinto (SW, Spain). Syst Appl Microbiol 30:601–614

    Article  PubMed  CAS  Google Scholar 

  • Gehrke T, Telegdi J, Thierry D, Sand W (1998) Importance of extracellular polymeric substances from Thiobacillus ferrooxidans for bioleaching. Appl Environ Microbiol 64:2743–2747

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gehrke T, Hallmann R, Kinzler K, Sand W (2001) The EPS of Acidithiobacillus ferrooxidans-a model for structure-function relationships of attached bacteria and their physiology. Water Sci Technol 43:159–167

    CAS  PubMed  Google Scholar 

  • Ghorbani Y, Petersen J, Harrison ST, Tupikina OV, Becker M, Mainza AN, Franzidis J-P (2012) An experimental study of the long-term bioleaching of large sphalerite ore particles in a circulating fluid fixed-bed reactor. Hydrometallurgy 129:161–171

    Article  CAS  Google Scholar 

  • Gleisner M, Herbert RB, Kockum PCF (2006) Pyrite oxidation by Acidithiobacillus ferrooxidans at various concentrations of dissolved oxygen. Chem Geol 225:16–29

    Article  CAS  Google Scholar 

  • Golovacheva R (1978) Attachment of Sulfobacillus thermosulfidooxidans cells to the surface of sulfide minerals. Mikrobiologiia 48:528–533

    Google Scholar 

  • Goltsman DSA, Denef VJ, Singer SW, VerBerkmoes NC, Lefsrud M, Mueller RS, Dick GJ, Sun CL, Wheeler KE, Zemla A (2009) Community genomic and proteomic analyses of chemoautotrophic iron-oxidizing “Leptospirillum rubarum”(Group II) and “Leptospirillum ferrodiazotrophum”(Group III) bacteria in acid mine drainage biofilms. Appl Environ Microbiol 75:4599–4615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goltsman DS, Dasari M, Thomas BC, Shah MB, VerBerkmoes NC, Hettich RL, Banfield JF (2013) New group in the Leptospirillum clade: cultivation-independent community genomics, proteomics, and transcriptomics of the new species “Leptospirillum group IV UBA BS”. Appl Environ Microbiol 79:5384–5393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golyshina OV, Pivovarova TA, Karavaiko GI, Kondrateva TF, Moore ER, Abraham WR, Lunsdorf H, Timmis KN, Yakimov MM, Golyshin PN (2000) Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. Int J Syst Evol Microbiol 50:997–1006

    Article  CAS  PubMed  Google Scholar 

  • González DM, Lara RH, Alvarado KN, Valdez-Pérez D, Navarro-Contreras HR, Cruz R, García-Meza JV (2012) Evolution of biofilms during the colonization process of pyrite by Acidithiobacillus thiooxidans. Appl Microbiol Biotechnol 93:763–775

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez A, Bellenberg S, Mamani S, Ruiz L, Echeverria A, Soulere L, Doutheau A, Demergasso C, Sand W, Queneau Y, Vera M, Guiliani N (2013) AHL signaling molecules with a large acyl chain enhance biofilm formation on sulfur and metal sulfides by the bioleaching bacterium Acidithiobacillus ferrooxidans. Appl Microbiol Biotechnol 97:3729–3737

    Article  CAS  PubMed  Google Scholar 

  • Govender Y, Gericke M (2011) Extracellular polymeric substances (EPS) from bioleaching systems and its application in bioflotation. Miner Eng 24:1122–1127

    Article  CAS  Google Scholar 

  • Gray MJ, Jakob U (2015) Oxidative stress protection by polyphosphate—new roles for an old player. Curr Opin Microbiol 24:1–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grillo-Puertas M, Schurig-Briccio LA, Rodríguez-Montelongo L, Rintoul MR, Rapisarda VA (2014) Copper tolerance mediated by polyphosphate degradation and low-affinity inorganic phosphate transport system in Escherichia coli. BMC Microbiol 14:72

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  CAS  PubMed  Google Scholar 

  • Harneit K, Göksel A, Kock D, Klock J-H, Gehrke T, Sand W (2006) Adhesion to metal sulfide surfaces by cells of Acidithiobacillus ferrooxidans, Acidithiobacillus thiooxidans and Leptospirillum ferrooxidans. Hydrometallurgy 83:245–254

    Article  CAS  Google Scholar 

  • Hedrich S, Schlomann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiology 157:1551–1564

    Article  CAS  PubMed  Google Scholar 

  • Henche AL, Koerdt A, Ghosh A, Albers SV (2012) Influence of cell surface structures on crenarchaeal biofilm formation using a thermostable green fluorescent protein. Environ Microbiol 14:779–793

    Article  CAS  PubMed  Google Scholar 

  • Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11:443–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivleva N, Wagner M, Horn H, Niessner R, Haisch C (2009) Towards a nondestructive chemical characterization of biofilm matrix by Raman microscopy. Anal Bioanal Chem 393:197–206

    Article  CAS  PubMed  Google Scholar 

  • Janczarek M (2011) Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int J Mol Sci 12:7898–7933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao Y, Cody GD, Harding AK, Wilmes P, Schrenk M, Wheeler KE, Banfield JF, Thelen MP (2010) Characterization of extracellular polymeric substances from acidophilic microbial biofilms. Appl Environ Microbiol 76:2916–2922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson DB (1998) Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol Ecol 27:307–317

    Article  CAS  Google Scholar 

  • Johnson DB (2014) Biomining—biotechnologies for extracting and recovering metals from ores and waste materials. Curr Opin Biotechnol 30:24–31

    Article  CAS  PubMed  Google Scholar 

  • Jones GC, Corin KC, van Hille RP, Harrison STL (2011) The generation of toxic reactive oxygen species (ROS) from mechanically activated sulphide concentrates and its effect on thermophilic bioleaching. Miner Eng 24:1198–1208

    Article  CAS  Google Scholar 

  • Jones DS, Albrecht HL, Dawson KS, Schaperdoth I, Freeman KH, Pi Y, Pearson A, Macalady JL (2012) Community genomic analysis of an extremely acidophilic sulfur-oxidizing biofilm. ISME J 6:158–170

    Article  CAS  PubMed  Google Scholar 

  • Kanao T, Kamimura K, Sugio T (2007) Identification of a gene encoding a tetrathionate hydrolase in Acidithiobacillus ferrooxidans. J Biotechnol 132:16–22

    Article  CAS  PubMed  Google Scholar 

  • Karatan E, Michael AJ (2013) A wider role for polyamines in biofilm formation. Biotechnol Lett 35:1715–1717

    Article  CAS  PubMed  Google Scholar 

  • Kim KS, Rao NN, Fraley CD, Kornberg A (2002) Inorganic polyphosphate is essential for long-term survival and virulence factors in Shigella and Salmonella spp. Proc Natl Acad Sci U S A 99:7675–7680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knickerbocker C, Nordstrom D, Southam G (2000) The role of “blebbing” in overcoming the hydrophobic barrier during biooxidation of elemental sulfur by Thiobacillus thiooxidans. Chem Geol 169:425–433

    Article  CAS  Google Scholar 

  • Koerdt A, Gödeke J, Berger J, Thormann KM, Albers S-V (2010) Crenarchaeal biofilm formation under extreme conditions. PLoS One 5, e14104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koerdt A, Jachlewski S, Ghosh A, Wingender J, Siebers B, Albers S-V (2012) Complementation of Sulfolobus solfataricus PBL2025 with an α-mannosidase: effects on surface attachment and biofilm formation. Extremophiles 16:115–125

    Article  CAS  PubMed  Google Scholar 

  • Labbate M, Zhu H, Thung L, Bandara R, Larsen MR, Willcox MD, Givskov M, Rice SA, Kjelleberg S (2007) Quorum-sensing regulation of adhesion in Serratia marcescens MG1 is surface dependent. J Bacteriol 189:2702–2711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laishley E, Bryant R, Kobryn B, Hyne J (1986) Microcrystalline structure and surface area of elemental sulphur as factors influencing its oxidation by Thiobacillus albertis. Can J Microbiol 32:237–242

    Article  CAS  Google Scholar 

  • Lamarche MG, Wanner BL, Crepin S, Harel J (2008) The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 32:461–473

    Article  CAS  PubMed  Google Scholar 

  • Lawrence J, Swerhone G, Leppard G, Araki T, Zhang X, West M, Hitchcock A (2003) Scanning transmission X-ray, laser scanning, and transmission electron microscopy mapping of the exopolymeric matrix of microbial biofilms. Appl Environ Microbiol 69:5543–5554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawrence JR, Korber DR, Neu TR (2007) Analytical imaging and microscopy techniques. In: Hurst CJ, Crawford RL, Garland JL, Lipson DA, Mills AL, Stetzenbach LD (eds) Manual of environmental microbiology. ASM Press, Washington, DC, pp 40–68

    Google Scholar 

  • Lei J, Huaiyang Z, Xiaotong P, Zhonghao D (2009) The use of microscopy techniques to analyze microbial biofilm of the bio-oxidized chalcopyrite surface. Miner Eng 22:37–42

    Article  CAS  Google Scholar 

  • Li Z, Wang Y, Yao Q, Justice NB, Ahn TH, Xu D, Hettich RL, Banfield JF, Pan C (2014) Diverse and divergent protein post-translational modifications in two growth stages of a natural microbial community. Nat Commun 5:4405

    CAS  PubMed  PubMed Central  Google Scholar 

  • Little B, Ray B, Pope R, Franklin M, White DC (2000) Spatial and temporal relationships between localised corrosion and bacterial activity on iron-containing substrata. In: Sequeira CAC (ed) Microbial corrosion. European Federation of Corrosion Publications; Institute of Materials, London, pp 21–35

    Google Scholar 

  • Lo I, Denef VJ, VerBerkmoes NC, Shah MB, Goltsman D, DiBartolo G, Tyson GW, Allen EE, Ram RJ, Detter JC (2007) Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446:537–541

    Article  CAS  PubMed  Google Scholar 

  • Mangold S, Harneit K, Rohwerder T, Claus G, Sand W (2008) Novel combination of atomic force microscopy and epifluorescence microscopy for visualization of leaching bacteria on pyrite. Appl Environ Microbiol 74:410–415

    Article  CAS  PubMed  Google Scholar 

  • Manz B, Volke F, Goll D, Horn H (2003) Measuring local flow velocities and biofilm structure in biofilm systems with Magnetic Resonance Imaging (MRI). Biotechnol Bioeng 84:424–432

    Article  CAS  PubMed  Google Scholar 

  • Marketon MM, Glenn SA, Eberhard A, González JE (2003) Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J Bacteriol 185:325–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marshall K, Stout R, Mitchell R (1971) Mechanism of the initial events in the sorption of marine bacteria to surfaces. J Gen Microbiol 68:337–348

    Article  CAS  Google Scholar 

  • Martínez P, Gálvez S, Ohtsuka N, Budinich M, Cortés MP, Serpell C, Nakahigashi K, Hirayama A, Tomita M, Soga T (2013) Metabolomic study of Chilean biomining bacteria Acidithiobacillus ferrooxidans strain Wenelen and Acidithiobacillus thiooxidans strain Licanantay. Metabolomics 9:247–257

    Article  PubMed  CAS  Google Scholar 

  • Meyer G, Schneider-Merck T, Böhme S, Sand W (2002) A simple method for investigations on the chemotaxis of A. ferrooxidans and D. vulgaris. Acta Biotechnol 22:391–399

    Article  CAS  Google Scholar 

  • Mikkelsen D, Kappler U, Webb R, Rasch R, McEwan A, Sly L (2007) Visualisation of pyrite leaching by selected thermophilic archaea: nature of microorganism–ore interactions during bioleaching. Hydrometallurgy 88:143–153

    Article  CAS  Google Scholar 

  • Mitsunobu S, Zhu M, Takeichi Y, Ohigashi T, Suga H, Makita H, Sakata M, Ono K, Mase K, Takahashi Y (2015) Nanoscale identification of extracellular organic substances at the microbe–mineral interface by scanning transmission X-ray microscopy. Chem Lett 44:91–93

    Article  CAS  Google Scholar 

  • Moreno-Paz M, Gomez M, Arcas A, Parro V (2010). Environmental transcriptome analysis reveals physiological differences between biofilm and planktonic modes of life of the iron oxidizing bacteria Leptospirillum spp. in their natural microbial community. BMC Genomics 11:404.

    Google Scholar 

  • Mosier AC, Justice NB, Bowen BP, Baran R, Thomas BC, Northen TR, Banfield JF (2013) Metabolites associated with adaptation of microorganisms to an acidophilic, metal-rich environment identified by stable-isotope-enabled metabolomics. MBio 4:e00484–12

    Article  PubMed  PubMed Central  Google Scholar 

  • Mosier AC, Li Z, Thomas BC, Hettich RL, Pan C, Banfield JF (2015) Elevated temperature alters proteomic responses of individual organisms within a biofilm community. ISME J 9:180–194

    Article  CAS  PubMed  Google Scholar 

  • Mueller RS, Dill BD, Pan C, Belnap CP, Thomas BC, Verberkmoes NC, Hettich RL, Banfield JF (2011) Proteome changes in the initial bacterial colonist during ecological succession in an acid mine drainage biofilm community. Environ Microbiol 13:2279–2292

    Article  CAS  PubMed  Google Scholar 

  • Murr L, Berry V (1976) Direct observations of selective attachment of bacteria on low-grade sulfide ores and other mineral surfaces. Hydrometallurgy 2:11–24

    Article  CAS  Google Scholar 

  • Neu T, Lawrence J (2009) Extracellular polymeric substances in microbial biofilms. In: Moran AP, Holst O, Brennan PJ, von Itzstein M (eds) Microbial glycobiology: structures, relevance and applications. Elsevier, San Diego, pp 735–758

    Google Scholar 

  • Neu TR, Lawrence JR (2014a) Advanced techniques for in situ analysis of the biofilm matrix (structure, composition, dynamics) by means of laser scanning microscopy. In: Donelli G (ed) Microbial biofilms: methods and protocols, methods in molecular biology. Springer, New York, pp 43–64

    Chapter  Google Scholar 

  • Neu TR, Lawrence JR (2014b) Investigation of microbial biofilm structure by laser scanning microscopy. Adv Biochem Eng Biotechnol 146:1–51

    PubMed  Google Scholar 

  • Neu TR, Lawrence JR (2015) Innovative techniques, sensors, and approaches for imaging biofilms at different scales. Trends Microbiol 23:233–242

    Article  CAS  PubMed  Google Scholar 

  • Neu TR, Marshall KC (1990) Bacterial polymers: physicochemical aspects of their interactions at interfaces. J Biomater Appl 5:107–133

    Article  CAS  PubMed  Google Scholar 

  • Neu TR, Marshall KC (1991) Microbial “footprints”—a new approach to adhesive polymers. Biofouling 3:101–112

    Article  Google Scholar 

  • Nicolaus B, Manca MC, Romano I, Lama L (1993) Production of an exopolysaccharide from two thermophilic archaea belonging to the genus Sulfolobus. FEMS Microbiol Lett 109:203–206

    Article  CAS  Google Scholar 

  • Noël N, Florian B, Sand W (2010) AFM & EFM study on attachment of acidophilic leaching organisms. Hydrometallurgy 104:370–375

    Article  CAS  Google Scholar 

  • Nooshabadi AJ, Rao KH (2014) Formation of hydrogen peroxide by sulphide minerals. Hydrometallurgy 141:82–88

    Article  CAS  Google Scholar 

  • Norris PR, Johnson DB (1998) Acidophilic microorganisms. In: Horikoshi K, Grant WD (eds) Extremophiles: microbial life in extreme environments. Wiley-Liss, New York, pp 133–153

    Google Scholar 

  • Norris PR, Burton NP, Foulis NA (2000) Acidophiles in bioreactor mineral processing. Extremophiles 4:71–76

    Article  CAS  PubMed  Google Scholar 

  • Ohmura N, Kitamura K, Saiki H (1993) Selective adhesion of Thiobacillus ferrooxidans to pyrite. Appl Environ Microbiol 59:4044–4050

    CAS  PubMed  PubMed Central  Google Scholar 

  • Orell A, Navarro CA, Arancibia R, Mobarec JC, Jerez CA (2010) Life in blue: copper resistance mechanisms of bacteria and archaea used in industrial biomining of minerals. Biotechnol Adv 28:839–848

    Article  CAS  PubMed  Google Scholar 

  • Orell A, Fröls S, Albers S-V (2013) Archaeal biofilms: the great unexplored. Annu Rev Microbiol 67:337–354

    Article  CAS  PubMed  Google Scholar 

  • Otto K, Silhavy TJ (2002) Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci U S A 99:2287–2292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parsek MR, Greenberg E (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13:27–33

    Article  CAS  PubMed  Google Scholar 

  • Peltola M, Neu TR, Raulio M, Kolari M, Salkinoja‐Salonen MS (2008) Architecture of Deinococcus geothermalis biofilms on glass and steel: a lectin study. Environ Microbiol 10:1752–1759

    Article  CAS  PubMed  Google Scholar 

  • Priester JH, Horst AM, Van De Werfhorst LC, Saleta JL, Mertes LA, Holden PA (2007) Enhanced visualization of microbial biofilms by staining and environmental scanning electron microscopy. J Microbiol Methods 68:577–587

    Article  CAS  PubMed  Google Scholar 

  • Ram RJ, VerBerkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake RC, Shah M, Hettich RL, Banfield JF (2005) Community proteomics of a natural microbial biofilm. Science 308:1915–1920

    Article  CAS  PubMed  Google Scholar 

  • Rao NN, Kornberg A (1996) Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli. J Bacteriol 178:1394–1400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rawlings DE (2002) Heavy metal mining using microbes. Annu Rev Microbiol 56:65–91

    Article  CAS  PubMed  Google Scholar 

  • Remonsellez F, Orell A, Jerez CA (2006) Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism. Microbiology 152:59–66

    Article  CAS  PubMed  Google Scholar 

  • Rendueles O, Ghigo J-M (2012) Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol Rev 36:972–989

    Article  CAS  PubMed  Google Scholar 

  • Reuter K, Pittelkow M, Bursy J, Heine A, Craan T, Bremer E (2010) Synthesis of 5-hydroxyectoine from ectoine: crystal structure of the non-heme iron(II) and 2-oxoglutarate-dependent dioxygenase EctD. PLoS One 5, e10647

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rimstidt JD, Vaughan DJ (2003) Pyrite oxidation: A state-of-the-art assessment of the reaction mechanism. Geochim Cosmochim Acta 67:873–880

    Article  CAS  Google Scholar 

  • Rivas M, Seeger M, Holmes DS, Jedlicki E (2005) A Lux-like quorum sensing system in the extreme acidophile Acidithiobacillus ferrooxidans. Biol Res 38:283–297

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez Y, Ballester A, Blazquez ML, Gonzalez F, Munoz JA (2003) New information on the pyrite bioleaching mechanism at low and high temperature. Hydrometallurgy 71:37–46

    Article  CAS  Google Scholar 

  • Rodriguez-Leiva M, Tributsch H (1988) Morphology of bacterial leaching patterns by Thiobacillus ferrooxidans on synthetic pyrite. Arch Microbiol 149:401–405

    Article  CAS  Google Scholar 

  • Rohwerder T, Sand W (2003) The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 149:1699–1710

    Article  CAS  PubMed  Google Scholar 

  • Rojas-Chapana JA, Giersig M, Tributsch H (1996) The path of sulfur during the bio-oxidation of pyrite by Thiobacillus ferrooxidans. Fuel 75:923–930

    Article  CAS  Google Scholar 

  • Rüberg S, Pühler A, Becker A (1999) Biosynthesis of the exopolysaccharide galactoglucan in Sinorhizobium meliloti is subject to a complex control by the phosphate-dependent regulator PhoB and the proteins ExpG and MucR. Microbiology 145:603–611

    Article  PubMed  Google Scholar 

  • Ruiz LM, Castro M, Barriga A, Jerez CA, Guiliani N (2011) The extremophile Acidithiobacillus ferrooxidans possesses a c-di-GMP signalling pathway that could play a significant role during bioleaching of minerals. Lett Appl Microbiol 54:133–139

    Article  PubMed  CAS  Google Scholar 

  • Sampson M, Phillips C, Ball A (2000a) Investigation of the attachment of Thiobacillus ferrooxidans to mineral sulfides using scanning electron microscopy analysis. Miner Eng 13:643–656

    Article  CAS  Google Scholar 

  • Sampson MI, Phillips CV, Blake RCI (2000b) Influence of the attachment of acidophilic bacteria during the oxidation of mineral sulfides. Miner Eng 13:373–389

    Article  CAS  Google Scholar 

  • Sand W, Gerke T, Hallmann R, Schippers A (1995) Sulfur chemistry, biofilm, and the (in) direct attack mechanism—a critical evaluation of bacterial leaching. Appl Microbiol Biotechnol 43:961–966

    Article  CAS  Google Scholar 

  • Sand W, Gehrke T, Hallmann R, Schippers A (1998) Towards a novel bioleaching mechanism. Miner Process Extract Metall Rev 19:97–106

    Article  CAS  Google Scholar 

  • Sand W, Gehrke T, Jozsa PG, Schippers A (2001) (Bio) chemistry of bacterial leaching—direct vs. indirect bioleaching. Hydrometallurgy 59:159–175

    Article  CAS  Google Scholar 

  • Sanhueza A, Ferrer I, Vargas T, Amils R, Sánchez C (1999) Attachment of Thiobacillus ferrooxidans on synthetic pyrite of varying structural and electronic properties. Hydrometallurgy 51:115–129

    Article  CAS  Google Scholar 

  • Schaeffer W, Holbert P, Umbreit W (1963) Attachment of Thiobacillus thiooxidans to sulfur crystals. J Bacteriol 85:137–140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schippers A (2007) Microorganisms involved in bioleaching and nucleic acid-based molecular methods for their identification and quantification. In: Donati ER, Sand W (eds) Microbial processing of metal sulfides. Springer, Dordrecht, pp 3–33

    Chapter  Google Scholar 

  • Schippers A, Sand W (1999) Bacterial leaching of metal sulfides proceeds by two indirect mechanisms via thiosulfate or via polysulfides and sulfur. Appl Environ Microbiol 65:319–321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schippers A, Jozsa P, Sand W (1996) Sulfur chemistry in bacterial leaching of pyrite. Appl Environ Microbiol 62:3424–3431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seeger M, Jerez CA (1993) Phosphate-starvation induced changes in Thiobacillus ferrooxidans. FEMS Microbiol Lett 108:35–41

    Article  CAS  PubMed  Google Scholar 

  • Seneviratne CJ, Wang Y, Jin L, Wong SS, Herath TD, Samaranayake LP (2012) Unraveling the resistance of microbial biofilms: has proteomics been helpful? Proteomics 12:651–665

    Article  CAS  PubMed  Google Scholar 

  • Sharma P, Das A, Rao KH, Forssberg K (2003) Surface characterization of Acidithiobacillus ferrooxidans cells grown under different conditions. Hydrometallurgy 71:285–292

    Article  CAS  Google Scholar 

  • Shrihari RK, Modak JM, Kumar R, Gandhi KS (1995) Dissolution of particles of pyrite mineral by direct attachment of Thiobacillus ferrooxidans. Hydrometallurgy 38:175–187

    Article  CAS  Google Scholar 

  • Smirnova GV, Oktyabrsky ON (2005) Glutathione in bacteria. Biochem (Mosc) 70:1199–1211

    Article  CAS  Google Scholar 

  • Smith K, Borges A, Ariyanayagam MR, Fairlamb AH (1995) Glutathionylspermidine metabolism in Escherichia coli. Biochem J 312:465–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solari JA, Huerta G, Escobar B, Vargas T, Badilla-Ohlbaum R, Rubio J (1992) Interfacial phenomena affecting the adhesion of Thiobacillus ferrooxidans to sulphide mineral surfaces. Colloid Surf 69:159–166

    Article  CAS  Google Scholar 

  • Staudt C, Horn H, Hempel D, Neu T (2003) Screening of lectins for staining lectin-specific glycoconjugates in the EPS of biofilms. In: Lens P, O’Flaherty V, Moran AP, Stoodley P, Mahony T (eds) Biofilms in medicine, industry and environmental technology. IWA Publishing, London, pp 308–327

    Google Scholar 

  • Stevens AM, Queneau Y, Soulere L, Sv B, Doutheau A (2010) Mechanisms and synthetic modulators of AHL-dependent gene regulation. Chem Rev 111:4–27

    Article  PubMed  CAS  Google Scholar 

  • Stoodley P, Sauer K, Davies D, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209

    Article  CAS  PubMed  Google Scholar 

  • Stourman NV, Branch MC, Schaab MR, Harp JM, Ladner JE, Armstrong RN (2011) Structure and function of YghU, a nu-class glutathione transferase related to YfcG from Escherichia coli. Biochemistry 50:1274–1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tapia J, Munoz J, Gonzalez F, Blazquez M, Malki M, Ballester A (2009) Extraction of extracellular polymeric substances from the acidophilic bacterium Acidiphilium 3.2 Sup (5). Water Sci Technol 59:1959–1967

    Article  CAS  PubMed  Google Scholar 

  • Taylor ES, Lower SK (2008) Thickness and surface density of extracellular polymers on Acidithiobacillus ferrooxidans. Appl Environ Microbiol 74:309–311

    Article  CAS  PubMed  Google Scholar 

  • Telegdi J, Keresztes Z, Pálinkás G, Kálmán E, Sand W (1998) Microbially influenced corrosion visualized by atomic force microscopy. Appl Phys A Mater Sci Process 66:S639–S642

    Article  CAS  Google Scholar 

  • Tributsch H, Rojas-Chapana JA (2000) Metal sulfide semiconductor electrochemical mechanisms induced by bacterial activity. Electrochim Acta 45:4705–4716

    Article  CAS  Google Scholar 

  • Tuovinen O (1990) Biological fundamentals of mineral leaching processes. In: Ehrich HL, Brierley CL (eds) Microbial mineral recovery. McGraw-Hill, New York, pp 55–77

    Google Scholar 

  • Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43

    Article  CAS  PubMed  Google Scholar 

  • Valdes J, Pedroso I, Quatrini R, Holmes DS (2008) Comparative genome analysis of Acidithiobacillus ferrooxidans, A. thiooxidans and A. caldus: insights into their metabolism and ecophysiology. Hydrometallurgy 94:180–184

    Article  CAS  Google Scholar 

  • Valdes J, Ossandon F, Quatrini R, Dopson M, Holmes DS (2011) Draft genome sequence of the extremely acidophilic biomining bacterium Acidithiobacillus thiooxidans ATCC 19377 provides insights into the evolution of the Acidithiobacillus genus. J Bacteriol 193:7003–7004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valenzuela S, Banderas A, Jerez CA, Guiliani N (2007) Cell-cell communication in bacteria. A promising new approach to improve bioleaching efficiency? In: Donati ER, Sand W (eds) Microbial processing of metal sulfides. Springer, Dordrecht, pp 253–264

    Chapter  Google Scholar 

  • Vera M, Guiliani N, Jerez CA (2003) Proteomic and genomic analysis of the phosphate starvation response of Acidithiobacillus ferrooxidans. Hydrometallurgy 71:125–132

    Article  CAS  Google Scholar 

  • Vera M, Krok B, Bellenberg S, Sand W, Poetsch A (2013a) Shotgun proteomics study of early biofilm formation process of Acidithiobacillus ferrooxidans ATCC 23270 on pyrite. Proteomics 13:1133–1144

    Article  CAS  PubMed  Google Scholar 

  • Vera M, Schippers A, Sand W (2013b) Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation-part A. Appl Microbiol Biotechnol 97:7529–7541

    Article  CAS  PubMed  Google Scholar 

  • Vogler K, Umbreit W (1941) The necessity for direct contact in sulfur oxidation by Thiobacillus thiooxidans. Soil Sci 51:331–338

    Article  CAS  Google Scholar 

  • Wagner M, Ivleva NP, Haisch C, Niessner R, Horn H (2009) Combined use of confocal laser scanning microscopy (CLSM) and Raman microscopy (RM): Investigations on EPS–matrix. Water Res 43:63–76

    Article  CAS  PubMed  Google Scholar 

  • Wakao N, Mishina M, Sakurai Y, Shiota H (1984) Bacterial pyrite oxidation III. Adsorption of Thiobacillus ferrooxidans cells on solid surfaces and its effect on iron release from pyrite. J Gen Appl Microbiol 30:63–77

    Article  CAS  Google Scholar 

  • Waksman SA (1932) Principles of soil microbiology. Tindall & Cox, Bailliere, London

    Google Scholar 

  • Wanner BL (1996a) Phosphorus assimilation and control of phosphate regulon. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. ASM Press, Washington, DC, pp 1357–1381

    Google Scholar 

  • Wanner BL (1996b) Signal transduction in the control of phosphate-regulated genes of Escherichia coli. Kidney Int 49:964–967

    Article  CAS  PubMed  Google Scholar 

  • Waters CM, Lu W, Rabinowitz JD, Bassler BL (2008) Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Bacteriol 190:2527–2536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss R (1973) Attachment of bacteria to sulphur in extreme environments. J Gen Microbiol 77:501–507

    Article  CAS  Google Scholar 

  • Wheaton G, Counts J, Mukherjee A, Kruh J, Kelly R (2015) The confluence of heavy metal biooxidation and heavy metal resistance: Implications for bioleaching by extreme thermoacidophiles. Minerals 5:397–451

    Google Scholar 

  • Whitfield C (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75:39–68

    Article  CAS  PubMed  Google Scholar 

  • Wilmes P, Remis JP, Hwang M, Auer M, Thelen MP, Banfield JF (2009) Natural acidophilic biofilm communities reflect distinct organismal and functional organization. ISME J 3:266–270

    Article  CAS  PubMed  Google Scholar 

  • Wilmes P, Bowen BP, Thomas BC, Mueller RS, Denef VJ, Verberkmoes NC, Hettich RL, Northen TR, Banfield JF (2010) Metabolome-proteome differentiation coupled to microbial divergence. MBio 1:e00246–10

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia JL, Wu S, Zhang RY, Zhang CG, He H, Jiang HC, Nie ZY, Qiu GZ (2011) Effects of copper exposure on expression of glutathione-related genes in Acidithiobacillus ferrooxidans. Curr Microbiol 62:1460–1466

    Article  CAS  PubMed  Google Scholar 

  • Xia JL, Liu HC, Nie ZY, Peng AA, Zhen XJ, Yang Y, Zhang XL (2013) Synchrotron radiation based STXM analysis and micro-XRF mapping of differential expression of extracellular thiol groups by Acidithiobacillus ferrooxidans grown on Fe2+ and S0. J Microbiol Methods 94:257–261

    Article  CAS  PubMed  Google Scholar 

  • Yelton AP, Comolli LR, Justice NB, Castelle C, Denef VJ, Thomas BC, Banfield JF (2013) Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea. BMC Genomics 14:485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng W, Qiu G, Zhou H, Liu X, Chen M, Chao W, Zhang C, Peng J (2010) Characterization of extracellular polymeric substances extracted during the bioleaching of chalcopyrite concentrate. Hydrometallurgy 100:177–180

    Article  CAS  Google Scholar 

  • Zhang R, Bellenberg S, Castro L, Neu TR, Sand W, Vera M (2014) Colonization and biofilm formation of the extremely acidophilic archaeon Ferroplasma acidiphilum. Hydrometallurgy 150:245–252

    Article  CAS  Google Scholar 

  • Zhang R, Neu T, Bellenberg S, Kuhlicke U, Sand W, Vera M (2015a) Use of lectins to in situ visualize glycoconjugates of extracellular polymeric substances in acidophilic archaeal biofilms. Microb Biotechnol 8:448–461

    Article  CAS  PubMed  Google Scholar 

  • Zhang R, Neu T, Zhang Y, Bellenberg S, Kuhlicke U, Li Q, Sand W, Vera M (2015b) Visualization and analysis of EPS glycoconjugates of the thermoacidophilic archaeon Sulfolobus metallicus. Appl Microbiol Biotechnol 99:7343–7356

    Google Scholar 

  • Zhou H, Zhang R, Hu P, Zeng W, Xie Y, Wu C, Qiu G (2008) Isolation and characterization of Ferroplasma thermophilum sp. nov., a novel extremely acidophilic, moderately thermophilic archaeon and its role in bioleaching of chalcopyrite. J Appl Microbiol 105:591–601

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Li Q, Jiao W, Jiang H, Sand W, Xia J, Liu X, Qin W, Qiu G, Hu Y (2012) Adhesion forces between cells of Acidithiobacillus ferrooxidans, Acidithiobacillus thiooxidans or Leptospirillum ferrooxidans and chalcopyrite. Colloids Surf B 94:95–100

    Article  CAS  Google Scholar 

  • Zhu J, Wang Q, Zhou S, Li Q, Gan M, Jiang H, Qin W, Liu X, Hu Y, Qiu G (2015) Insights into the relation between adhesion force and chalcopyrite-bioleaching by Acidithiobacillus ferrooxidans. Colloids Surf B 126:351–357

    Article  CAS  Google Scholar 

  • Zippel B, Neu T (2011) Characterization of glycoconjugates of extracellular polymeric substances in tufa-associated biofilms by using fluorescence lectin-binding analysis. Appl Environ Microbiol 77:505–516

    Article  CAS  PubMed  Google Scholar 

  • Zolghadr B, Klingl A, Koerdt A, Driessen AJ, Rachel R, Albers S-V (2010) Appendage-mediated surface adherence of Sulfolobus solfataricus. J Bacteriol 192:104–110

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to acknowledge the excellent technical assistance of Ute Kuhlicke (Department of River Ecology, Helmholtz Centre for Environmental Research-UFZ, Magdeburg) in CLSM and image processing. Ruiyong Zhang appreciates China Scholarship Council (CSC) for financial support (No. 2010637124).

Conflict of Interest

Ruiyong Zhang, Sören Bellenberg, Thomas R. Neu, Wolfgang Sand, and Mario Vera declare that they have no conflict of interest.

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Authors and Affiliations

  1. Aquatische Biotechnologie, Biofilm Centre, Universität Duisburg – Essen, Universitätsstraße 5, 45141, Essen, Germany

    Ruiyong Zhang, Sören Bellenberg & Wolfgang Sand

  2. Department of River Ecology, Helmholtz Centre for Environmental Research – UFZ, Brückstrasse 3a, 39114, Magdeburg, Germany

    Thomas R. Neu

  3. Institute for Biological and Medical Engineering, Schools of Engineering, Biological Sciences and Medicine, Pontificia Universidad Católica de Chile, Vicuña Mackenna 4860, 7820436 Macul, Santiago, Chile

    Mario Vera

  4. Department of Hydraulic and Environmental Engineering, School of Engineering, Pontificia Universidad Católica de Chile, Vicuña Mackenna 4860, 7820436 Macul, Santiago, Chile

    Mario Vera

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  1. Federal University of Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Saint Barthélemy

    Pabulo H Rampelotto

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Zhang, R., Bellenberg, S., Neu, T.R., Sand, W., Vera, M. (2016). The Biofilm Lifestyle of Acidophilic Metal/Sulfur-Oxidizing Microorganisms. In: Rampelotto, P. (eds) Biotechnology of Extremophiles:. Grand Challenges in Biology and Biotechnology, vol 1. Springer, Cham. https://doi.org/10.1007/978-3-319-13521-2_6

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