Abstract
Biofilm formation plays a pivotal role in bioleaching activities of bacteria in both industrial and natural environments. Here, by visualizing attached bacterial cells on energetic substrates with different microscopy techniques, we obtained the first direct evidence that it is possible to positively modulate biofilm formation of the extremophilic bacterium Acidithiobacillus ferrooxidans on sulfur and pyrite surfaces by using Quorum Sensing molecules of the N-acylhomoserine lactone type (AHLs). Our results revealed that AHL-signaling molecules with a long acyl chain (12 or 14 carbons) increased the adhesion of A. ferrooxidans cells to these substrates. In addition, Card-Fish experiments demonstrated that C14-AHL improved the adhesion of indigenous A. ferrooxidans cells from a mixed bioleaching community to pyrite. Finally, we demonstrated that this improvement of cell adhesion is correlated with an increased production of extracellular polymeric substances. Our results open up a promising means to develop new strategies for the improvement of bioleaching efficiency and metal recovery, which could also be used to control environmental damage caused by acid mine/rock drainage.
Similar content being viewed by others
References
Africa CJ, van Hille RP, Harrison STL (2012) Attachment of Acidithiobacillus ferrooxidans and Leptospirillum ferriphilum cultured under varying conditions to pyrite, chalcopyrite, low-grade ore and quartz in a packed column reactor. Appl Microbiol Biotechnol. doi:10.1007/s00253-012-3939-x
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
Bellenberg S, Leon-Morales F, Holuscha D, Krok B,Vera M, Sand W (2011a). A lectin-based approach for visualization of capsular EPS after attachment and biofilm formation by acidophilic leaching bacteria. In Biohydrometallurgy: Biotech key to unlock mineral resources value. Proceedings of the 19th international Biohydromettallurgy symposium. Central South University Press, Changsha, China
Bellenberg S, Vera M, Sand W (2011b). Transcriptomic studies of capsular polysaccharide export systems involved in biofilm formation by Acidithiobacillus ferrooxidans. In Biohydrometallurgy: Biotech key to unlock mineral resources value. Proceedings of the 19th international Biohydromettallurgy symposium. Central South University Press, Changsha, China.
Carlier A, Burbank L, von Bodman SB (2009) Identification and characterization of three novel EsaI/EsaR quorum-sensing controlled stewartan exopolysaccharide biosynthetic genes in Pantoea stewartii ssp. stewartii. Mol Microbiol 74:903–913
Choudhary S, Schmidt-Dannert C (2010) Applications of quorum sensing in biotechnology. Appl Microbiol Biotechnol 86:1267–1279
Davis RA, Welty AT, Borrego J, Morales JA, Pendon JG, Ryan JG (2000) Rio Tinto estuary (Spain): 5000 years of pollution. Environ Geol 39:1107–1116
De Bruyn J, Boogerd F, Bos P, Kuenen J (1990) Floating filters, a novel technique for isolation and enumeration of fastidious, acidophilic, iron-oxidizing, autotrophic bacteria. Appl Environ Microbiol 56:2891–2894
Decho AW, Frey RL, Ferry JL (2011) Chemical challenges to bacterial AHL signalling in the environment. Chem Rev 111:86–99
Demergasso C, Galleguillos F, Soto P, Serón M, Iturriaga V (2010) Microbial succession during a heap bioleaching cycle of low grade copper sulfides: does this knowledge mean a real input for industrial process design and control? Hydrometallurgy 104:382–390
Echeverría A, Demergasso C (2009) Assessment of microbial adhesion in mixed cultures to sulfide minerals using CARD-FISH techniques. Adv Mat Res 71–73:83–86
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
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633
Galloway WR, Hodgkinson JT, Bowden SD, Welch M, Spring DR (2011) Quorum sensing in gram-negative bacteria: small-molecule modulation of AHL and AI-2 quorum sensing pathways. Chem Rev 111:28–67
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
Gonzalez-Toril E, Llobet-Brossa E, Casamayor EO, Amann R, Amils R (2003) Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 69:4853–4865
Harneit K, Goksel A, Kock D, Klock JH, Gehrke T, Sand W (2006) Adhesion to metal sulfide surfaces by cells of Acidithiobacillus ferrooxidans, Acidithiobacillus thiooxidans and Leptospirillum ferrooxidans. Hydrometallurgy 83:245–254
Janczarek M (2011) Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int J Mol Sci 12:7898–7933
Kozlova EV, Khajanchi BK, Sha J, Chopra AK (2011) Quorum sensing and c-di-GMPdependent alterations in gene transcripts and virulence-associated phenotypes in a clinical isolate of Aeromonas hydrophila. Microb Pathog 50:213–223
Labbate M, Zhu H, Thung L, Bandara R, Larsen MR, Wilcox 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
Mackintosh M (1978) Nitrogen fixation by Thiobacillus ferrooxidans. J Gen Microbiol 105:215–218
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
Marketon MM, Glenn SA, Eberhard A, Gonzalez JE (2003) Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J Bacteriol 185:325–331
Mykytczuk NC, Trevors JT, Twine SM, Ferroni GD, Leduc LG (2010) Membrane fluidity and fatty acid comparisons in psychrotrophic and mesophilic strains of Acidithiobacillus ferrooxidans under cold growth temperatures. Arc Microbiol 192:10051018
Parsek MR, Greenberg EP (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13:27–33
Rawlings DE (2002) Heavy metal mining using microbes. Annu Rev Microbiol 56:65–91
Remonsellez F, Galleguillos F, Moreno-Paz M, Parro V, Acosta M, Demergasso C (2009) Dynamic of active microorganisms inhabiting a bioleaching industrial heap of low-grade copper sulfide ore monitored by real-time PCR and oligonucleotide prokaryotic acidophile microarraymbt_112. Microbial Biotechnol 6:613–624
Riedel K, Hentzer M, Geisenberger O, Huber B, Steidle A, Wu H, Hoiby N, Givskov M, Molin S, Eberl L (2001) N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147:3249–3262
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
Rivas M, Seeger M, Jedlicki E, Holmes DS (2007) Second acyl homoserine lactone production system in the extreme acidophile Acidithiobacillus ferrooxidans. Appl Environ Microbiol 73:3225–3231
Rohwerder T, Sand W (2007) Oxidation of inorganic sulfur compounds in acidophilic prokaryotes. Eng Life Sci 7:301–309
Rohwerder T, Gehrke T, Kinzler K, Sand W (2003) Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 63:239–248
Ruiz LM, Castro M, Barriga A, Jerez CA, Guiliani N (2012) 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
Ruiz LM, Valenzuela S, Castro M, Gonzalez A, Frezza M, Soulere L, Rohwerder T, Sand W, Queneau Y, Jerez CA, Doutheau A, Guiliani N (2008) AHL communication is a widespread phenomenon in biomining bacteria and seems to be involved in mineral-adhesion efficiency. Hydrometallurgy 94:133–137
Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, Zhang LH, Heeb S, Cámara M, Williams P, Dow JM (2006) Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103:6712–6717
Sand W, Gehrke T (2006) Extracellular polymeric substances mediate bioleaching/biocorrosion via interfacial processes involving iron(III) ions and acidophilic bacteria. Res Microbiol 157:49–56
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
Schippers A, Jozsa P, Sand W (1996) Sulfur chemistry in bacterial leaching of pyrite. Appl Environ Microbiol 62:3424–3431
Stevens AM, Queneau Y, Soulère L, Von Bodman S, Doutheau A (2011) Mechanisms and synthetic modulators of AHL-dependent gene regulation. Chem Rev 111:4–27
Ueda A, Wood TK (2009) Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5:e1000483
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, The Netherlands, pp 253–264
Vera M, Pagliai F, Guiliani N, Jerez CA (2008) The chemolithoautotroph Acidithiobacillus ferrooxidans can survive under phosphate-limiting conditions by expressing a C-P lyase operon that allows it to grow on phosphonates. Appl Environ Microbiol 74:1829–1835
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
Welch M, Todd DE, Whitehead NA, McGowan SJ, Bycroft BW, Salmond GPC (2000) EMBO J 19:631–641
Xie XH, Xiao SM, Liu JS (2009) Microbial communities in acid mine drainage and their interaction with pyrite surface. Curr Microbiol 59:71–77
Zhang LH (2010) A novel C-di-GMP effector linking intracellular virulence regulon to quorum sensing and hypoxia sensing. Virulence 1:391–394.
Acknowledgments
This work was supported by grants FONDECYT 1080441, FONDECYT 1120295, and CNRS-CONICYT (PICS no. 5270). Alex González was supported by scholarships from CONICYT. Sören Bellenberg and Mario Vera acknowledge the financial support of the program of promotion of Young Scientists from University of Duisburg-Essen. We thank Dr. Michael Handford (Universidad de Chile) for proof-reading the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Alex González and Sören Bellenberg contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 1373 kb)
Rights and permissions
About this article
Cite this article
González, A., Bellenberg, S., Mamani, S. et al. 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 (2013). https://doi.org/10.1007/s00253-012-4229-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-012-4229-3