Abstract
Anthropogenic activities such as mining, smelting, and industrial use have caused serious problems of metal(loid) pollution in nearly every country in the world. A wide range of environmental microorganisms are capable of transforming metal(loid)s into nanomaterials, i.e., biogenic nanomaterials (bio-NMs), in the environment. Although the impacts of various metal(loid)s on the ecosystems have been extensively studied, the potential influence of the bio-NMs generated in the environment to environmental organisms is largely unexplored. Using tellurium nanomaterials transformed from tellurite by a metal-reducing bacterium as model bio-NMs, we demonstrated that the bio-NMs significantly decreased siderophore production in an environmental bacterium Pseudomonas aeruginosa in both planktonic cultures and biofilms. Transcriptomic analysis revealed that the bio-NMs inhibited the expression of genes involved in biosynthesis and transport of siderophores. Siderophores secreted by certain bacteria in microbial communities can be considered as public goods that can be exploited by local communities, playing an important role in shaping microbial communities. The inhibition of siderophore production by the bio-NMs implies that bio-NMs may have an important influence on the ecosystems through altering specific functions of environmental bacteria. Taken together, this study provides a novel insight into the environmental impacts of metal(loid)s.
Similar content being viewed by others
References
Buckling A, Harrison F, Vos M, Brockhurst MA, Gardner A, West SA, Griffin A (2007) Siderophore-mediated cooperation and virulence in Pseudomonas aeruginosa. FEMS Microbiol Ecol 62(2):135–141
Cao B, Ahmed B, Kennedy DW, Wang Z, Shi L, Marshall MJ, Fredrickson JK, Isern NG, Majors PD, Beyenal H (2011) Contribution of extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms to U (VI) immobilization. Environ Sci Technol 45(13):5483–5490
Cao B, Majors PD, Ahmed B, Renslow RS, Silvia CP, Shi L, Kjelleberg S, Fredrickson JK, Beyenal H (2012) Biofilm shows spatially stratified metabolic responses to contaminant exposure. Environ Microbiol 14(11):2901–2910
Chen C-Y, Nace G, Irwin P (2003) A 6x6 drop plate method for simultaneous colony counting and MPN enumeration of Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli. J Microbiol Methods 55:475–479
Chua SL, Tan SY, Rybtke MT, Chen Y, Rice SA, Kjelleberg S, Tolker-Nielsen T, Yang L, Givskov M (2013) Bis-(3′-5′)-cyclic dimeric GMP regulates antimicrobial peptide resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 57(5):2066–2075
Cordero OX, Ventouras L-A, DeLong EF, Polz MF (2012) Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc Natl Acad Sci U S A 109(49):20059–20064
Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49(1):711–745
Crusz S, Popat R, Rybtke M, Camara M, Givskov M, Tolker-Nielsen T, Diggle S, Williams P (2012) Bursting the bubble on bacterial biofilms: a flow cell methodology. Biofouling 28(8):835–842
Ding Y, Peng N, Du Y, Ji L, Cao B (2014) Disruption of putrescine biosynthesis in Shewanella oneidensis enhances biofilm cohesiveness and performance in Cr (VI) immobilization. Appl Environ Microbiol 80(4):1498–1506
Dopp E, Hartmann LM, Florea AM, Rettenmeier AW, Hirner AV (2004) Environmental distribution, analysis, and toxicity of organometal(loid) compounds. Crit Rev Toxicol 34(3):301–333
Drenkard E (2003) Antimicrobial resistance of Pseudomonas aeruginosa biofilms. Microbes Infect 5(13):1213–1219
Greenwald J, Hoegy F, Nader M, Journet L, Mislin GL, Graumann PL, Schalk IJ (2007) Real time fluorescent resonance energy transfer visualization of ferric pyoverdine uptake in Pseudomonas aeruginosa. A role for ferrous iron. J Biol Chem 282(5):2987–2995
Gristina AG, Hobgood CD, Webb LX, Myrvik QN (1987) Adhesive colonization of biomaterials and antibiotic resistance. Biomaterials 8(6):423–426
Habimana O, Steenkeste K, Fontaine-Aupart MP, Bellon-Fontaine MN, Kulakauskas S, Briandet R (2011) Diffusion of nanoparticles in biofilms is altered by bacterial cell wall hydrophobicity. Appl Environ Microbiol 77(1):367–368
Han X, Gu JD (2010) Sorption and transformation of toxic metals by microorganisms. In: Mitchell R, Gu J (eds) Environ microbiol, 2nd edn. Willy, New York, pp 153–176
Hannauer M, Yeterian E, Martin LW, Lamont IL, Schalk IJ (2010) An efflux pump is involved in secretion of newly synthesized siderophore by Pseudomonas aeruginosa. FEBS Lett 584(23):4751–4755
Harrison F, Paul J, Massey RC, Buckling A (2007) Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. ISME J 2(1):49–55
Hockin SL, Gadd GM (2003) Linked redox precipitation of sulfur and selenium under anaerobic conditions by sulfate-reducing bacterial biofilms. Appl Environ Microbiol 69(12):7063–7072
Kalathil S, Lee J, Cho M (2011) Electrochemically active biofilm-mediated synthesis of silver nanoparticles in water. Green Chem 13:1482–1485
Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK (2007) The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 117(4):877–888
Kim D-H, Kanaly R, Hur HG (2012) Biological accumulation of tellurium nanorod structures via reduction of tellurite by Shewanella oneidensis MR-1. Bioresour Technol 125:127–131
Klonowska A, Heulin T, Vermeglio A (2005) Selenite and tellurite reduction by Shewanella oneidensis. Appl Environ Microbiol 71(9):5607–5609
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods (San Diego, Calif) 25(4):402–408
Mohanty A, Kathawala MH, Zhang J, Chen WN, Loo JSC, Kjelleberg S, Yang L, Cao B (2014a) Biogenic tellurium nanorods as a novel antivirulence agent inhibiting pyoverdine production in Pseudomonas aeruginosa. Biotechnol Bioeng 111(5):858–865
Mohanty A, Wu Y, Cao B (2014b) Impacts of engineered nanomaterials on microbial community structure and function in natural and engineered ecosystems. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-6000-4
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628
Moscoso H, Saavedra C, Loyola C, Pichuantes S, Vasquez C (1998) Biochemical characterization of tellurite-reducing activities of Bacillus stearothermophilus V. Res Microbiol 149(6):389–397
Narayanan KB, Sakthivel N (2010) Biological synthesis of metal nanoparticles by microbes. Adv Colloid Interf Sci 156(1–2):1–13
Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270(45):26723–26726
Ng CK, Sivakumar K, Liu X, Madhaiyan M, Ji L, Yang L, Tang C, Song H, Kjelleberg S, Cao B (2013) Influence of outer membrane c-type cytochromes on particle size and activity of extracellular nanoparticles produced by Shewanella oneidensis. Biotechnol Bioeng 110(7):1831–1837
Peek ME, Bhatnagar A, McCarty NA, Zughaier SM (2012) Pyoverdine, the major siderophore in Pseudomonas aeruginosa, evades NGAL recognition. Interdiscip Perspect Infect Dis 2012:10
Peralta-Videa JR, Zhao LJ, Lopez-Moreno ML, de la Rosa G, Hong J, Gardea-Torresdey JL (2011) Nanomaterials and the environment: a review for the biennium 2008–2010. J Hazard Mater 186(1):1–15
Peulen T-O, Wilkinson KJ (2011) Diffusion of nanoparticles in a biofilm. Environ Sci Technol 45(8):3367–3373
Prosser BL, Taylor D, Dix BA, Cleeland R (1987) Method of evaluating effects of antibiotics on bacterial biofilm. Antimicrob Agents Chemother 31(10):1502–1506
Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28(3):142–149
Saha R, Saha N, Donofrio RS, Bestervelt LL (2013) Microbial siderophores: a mini review. J Basic Microbiol 53(4):303–317
Schalk IJ, Guillon L (2013) Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol 15(6):1661–1673
Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13(11):2844–2854
Schofield EJ, Veeramani H, Sharp JO, Suvorova E, Bernier-Latmani R, Mehta A, Stahlman J, Webb SM, Clark DL, Conradson SD (2008) Structure of biogenic uraninite produced by Shewanella oneidensis strain MR-1. Environ Sci Technol 42(21):7898–7904
Singh RS, Rangari VK, Sanagapalli S, Jayaraman V, Mahendra S, Singh VP (2004) Nano-structured CdTe, CdS and TiO2 for thin film solar cell applications. Sol Energy Mater Sol Cells 82(1):315–330
Sintubin L, Verstraete W, Boon N (2012) Biologically produced nanosilver: current state and future perspectives. Biotechnol Bioeng 109(10):2422–2436
Sivakumar K, Wang VB, Chen X, Bazan GC, Kjelleberg S, Loo SCJ, Cao B (2014) Membrane permeabilization underlies the enhancement of extracellular bioactivity in Shewanella oneidensis by a membrane-spanning conjugated oligoelectrolyte. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-5973-3
Staupendahl G, Schindler K (1982) Optical tuning of a tellurium cavity: optical modulation and bistability in the infrared region at room temperature. Opt Quant Electron 14(2):157–167
Stewart PS (1996) Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob Agents Chemother 40(11):2517–2522
Stewart PS (2003) Diffusion in biofilms. J Bacteriol 185(5):1485–1491
Stewart PS, William Costerton J (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358(9276):135–138
Stoodley P, Sauer K, Davies D, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56(1):187–209
Suzuki Y, Kelly SD, Kemner KM, Banfield JF (2002) Radionuclide contamination: nanometre-size products of uranium bioreduction. Nature 419(6903):134
Trutko SM, Akimenko VK, Suzina NE, Anisimova LA, Shlyapnikov MG, Baskunov BP, Duda VI, Boronin AM (2000) Involvement of the respiratory chain of gram-negative bacteria in the reduction of tellurite. Arch Microbiol 173(3):178–186
Tsiulyanu D, Marian S, Miron V, Liess HD (2001) High sensitive tellurium based NO2 gas sensor. Sensors Actuators B Chem 73(1):35–39
Turner RJ, Borghese R, Zannoni D (2012) Microbial processing of tellurium as a tool in biotechnology. Biotechnol Adv 30(5):954–963
Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15(1):22–30
Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647
West SA, Buckling A (2003) Cooperation, virulence and siderophore production in bacterial parasites. Proc R Soc Lond [Biol] 270(1510):37–44
Winkelmann G, Drechsel H (2001) Microbial siderophores. In: Rehm H.-J, Reed G (eds) Biotechnology set, 2nd edn. Wiley-VCH Verlag GmbH, Weinheim, doi:10.1002/9783527620999.ch5g
Xie YP, He YP, Irwin PL, Jin T, Shi XM (2011) Antibacterial activity and mechanism of action of zinc oxide nanoparticles against Campylobacter jejuni. Appl Environl Microbiol 77(7):2325–2331
Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, Tolker-Nielsen T (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153(5):1318–1328
Yang L, Nilsson M, Gjermansen M, Givskov M, Tolker-Nielsen T (2009) Pyoverdine and PQS mediated subpopulation interactions involved in Pseudomonas aeruginosa biofilm formation. Mol Microbiol 74(6):1380–1392
Yeterian E, Martin LW, Guillon L, Journet L, Lamont IL, Schalk IJ (2010) Synthesis of the siderophore pyoverdine in Pseudomonas aeruginosa involves a periplasmic maturation. Amino Acids 38(5):1447–1459
Yurkov V, Jappé J, Verméglio A (1996) Tellurite resistance and reduction by obligately aerobic photosynthetic bacteria. Appl Environ Microbiol 62(11):4195–4198
Zannoni D (2010) Bacterial processing of metalloids as a tool in biotechnology. J Biotechnol 150:S52–S53
Zhang Y, Ng CK, Cohen Y, Cao B (2014) Cell growth and protein expression of Shewanella oneidensis in biofilms and hydrogel-entrapped cultures. Mol BioSyst 10(5):1035–1042
Acknowledgments
This research was supported by the National Research Foundation and Ministry of Education Singapore under its Research Centre of Excellence Programme, Singapore Centre on Environmental Life Sciences Engineering (SCELSE) (M4330005.C70) and a Start-up Grant (M4080847.030) from the College of Engineering, Nanyang Technological University, Singapore.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 171 kb)
Rights and permissions
About this article
Cite this article
Mohanty, A., Liu, Y., Yang, L. et al. Extracellular biogenic nanomaterials inhibit pyoverdine production in Pseudomonas aeruginosa: a novel insight into impacts of metal(loid)s on environmental bacteria. Appl Microbiol Biotechnol 99, 1957–1966 (2015). https://doi.org/10.1007/s00253-014-6097-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-014-6097-5