Abstract
Mercury adsorption on the cell surface and intracellular uptake by bacteria represent the key first step in the production and accumulation of highly toxic mercury in living organisms. In this work, the biophysical characteristics of mercury bioaccumulation are studied in intact cells of photosynthetic bacteria by use of analytical (dithizone) assay and physiological photosynthetic markers (pigment content, fluorescence induction, and membrane potential) to determine the amount of mercury ions bound to the cell surface and taken up by the cell. It is shown that the Hg(II) uptake mechanism (1) has two kinetically distinguishable components, (2) includes co-opted influx through heavy metal transporters since the slow component is inhibited by Ca2+ channel blockers, (3) shows complex pH dependence demonstrating the competition of ligand binding of Hg(II) ions with H+ ions (low pH) and high tendency of complex formation of Hg(II) with hydroxyl ions (high pH), and (4) is not a passive but an energy-dependent process as evidenced by light activation and inhibition by protonophore. Photosynthetic bacteria can accumulate Hg(II) in amounts much (about 105) greater than their own masses by well-defined strong and weak binding sites with equilibrium binding constants in the range of 1 (μM)−1 and 1 (mM)−1, respectively. The strong binding sites are attributed to sulfhydryl groups as the uptake is blocked by use of sulfhydryl modifying agents and their number is much (two orders of magnitude) smaller than the number of weak binding sites. Biofilms developed by some bacteria (e.g., Rvx. gelatinosus) increase the mercury binding capacity further by a factor of about five. Photosynthetic bacteria in the light act as a sponge of Hg(II) and can be potentially used for biomonitoring and bioremediation of mercury-contaminated aqueous cultures.
Similar content being viewed by others
Abbreviations
- BChl:
-
Bacteriochlorophyll
- Q A and Q B :
-
Primary and secondary quinone acceptors, respectively
- RC:
-
Reaction center
References
Abdia O, Kazemia M. (2015) A review study of biosorption of heavy metals and comparison between different biosorbents. J Mater Environ Sci 6(5):1386–1399
Ahluwalia SS, Goyal D (2007) Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour Technol 98(12):2243–2257
Armitage JP (2001) Light responses in purple photosynthetic bacteria. Compr Ser Photosci 1:117–150
Asztalos E, Italiano F, Milano F, Maróti P, Trotta M (2010) Early detection of mercury contamination by fluorescence induction of photosynthetic bacteria. Photochem Photobiol Sci 9:1218–1223
Asztalos E, Sipka G, Kis M, Trotta M, Maróti P (2012) The reaction center is the sensitive target of the mercury(II) ion in intact cells of photosynthetic bacteria. Photosynth Res 112(2):129–140
Bae W, Mehra RK, Mulchandani A, Chen W (2001) Genetic Engineering of Escherichia coli for Enhanced Uptake and Bioaccumulation of Mercury. Appl Environ Microbiol 67(11):5335–5338
Bakkaloglu I, Butter TJ, Evison LM, Holland FS, Hancock IC (1998) Screening of various types biomass for removal and recovery of heavy metals (Zn, Cu, Ni) by biosorption, sedimentation and desorption. Water Sci Technol 38:269–277
Barton L (2005) Structural and Functional Relationships in Prokaryotes. Springer Science & Business Media, Berlin
Chang JS, Law R, Chang CC (1997) Biosorption of lead, copper and cadmium by biomass of Pseudomonas aeruginosa PU21. Water Res 31:1651–1658
Daguené V, McFall E, Yumvihoze E, Shurong X, Amyot M (2012) Divalent base cations hamper HgII uptake. Environ Sci Technol 46:6645–6653
Deng X, Jia P (2011) Construction and characterization of a photosynthetic bacterium genetically engineered for Hg2+ uptake. Bioresour Technol 102:3083–3088
Deng X, Wang P (2012) Isolation of marine bacteria highly resistant to mercury and their bioaccumulation process. Bioresour Technol 121:342–347
Flemming H-C, Wingender J (2001) Relevance of microbial extracellular polymeric substances (EPSs). Part I. Structural and ecological aspects. Water Sci Technol 43:1–8
Gabr RM, Hassan SHA, Shoreit AAM (2008) Biosorption of lead and nickel by living and non-living cells of Pseudomonas aeruginosa ASU 6a. Int Biodeterior Biodegradation 62:195–203
Gao J-L, Wraight CA (1990) Sulfhydryl modifying reagents inhibit QA – oxidation in reaction centers from Rhodobacter sphaeroides and Capsulatus, but not Rhodopseudomonas viridis. Photosynth Res 26(3):171–179
Georgalis Y, Philipp M, Aleksandrova R, Krüger JK (2012) Light scattering studies on Ficoll PM70 solutions reveal two distinct diffusive modes. J Colloid Interface Sci 386(1):141–147
Giotta L, Agostiano A, Italiano F, Milano F, Trotta M (2006) Heavy metal ion influence on the photosynthetic growth of Rhodobacter sphaeroides. Chemosphere 62:1490–1499
Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374
Gourdon R, Bhende S, Rus E, Sofer SS (1990) Comparison of cadmium biosorption by Gram-positive and Gram-negative bacteria from activated sludge. Biotechnol Lett 12:839–842
Goyer RA, Cherian MG (2012) Toxicology of metals: biochemical aspects. Springer Science & Business Media, Berlin
Greenberg AE, Clesceri LS, Eaton AD (1992) Standard methods for the examination of water and wastewater, 18th edition. A.P.H.A., Washington
Greenwood NN, Earnshaw A (1997) Chemistry of the elements, 2nd edn. Butterworth-Heinemann, Oxford
Grégoire D, Poulain AJ (2014) A little bit of light goes a long way: the role of phototrophs on mercury cycling. Metallomics 6(3):396–407
Gregoire DS, Poulain AJ (2016) A physiological role for Hg(II) during phototrophic growth. Nat Geosci 9(2):121–125
Hentzer M, Teitzel GM, Balzer GJ, Heydorn A, Molin S, Givskov M, Parsek MR (2001) Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 183:5395–5401
Hess P, Lansman JB, Tsien RW (1984) Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature 311:538–544
Hinkle PM, Kinsella PA, Osterhoudt KC (1987) Cadmium uptake and toxicity via voltage-sensitive calcium channels. J Biol Chem 262(34):16333–16337
Hongve D, Haaland S, Riise G, Blakar I, Norton S (2012) Decline of acid rain enhances mercury concentrations in fish. Environ Sci Technol 46(5):2490–2491
Hunt S (1986) Diversity of biopolymer structure and its potential for ionbinding applications. In: Eccles H, Hunt S (eds) Immobilisation of ions by bio-sorption. Ellis Horwood Ltd., West Sussex, pp 15–46
Italiano F, Buccolieri A, Giotta L, Agostiano A, Valli L, Milano F, Trotta M (2009) Response of the carotenoids mutant Rhodobacter sphaeroides growing cells to cobalt and nickel exposure. Int Biodeterior Biodegr 63(7):948–957
Kane AL, Al-Shayeb B, Holec PV, Rajan S, Le Mieux NE, Heinsch SC, Psarska S, Aukema KG, Sarkar CA, Nater EA, Gralnick JA (2016) Toward bioremediation of methylmercury using silica encapsulated Escherichia coli harboring the mer operon. PLoS ONE 11(1): e0147036. doi:10.1371/journal.pone.0147036
Kelly DJ, Thomas GH (2001) The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea. FEMS Microbiol Rev 25(4):405–424
Kelly CA, Rudd JW, Holoka MH (2003) Effect of pH on mercury uptake by an aquatic bacterium: implications for Hg cycling. Environ Sci Technol 37(13):2941–2946
Kis M, Asztalos E, Sipka G, Maróti P (2014) Assembly of photosynthetic apparatus in Rhodobacter sphaeroides as revealed by functional assessments at different growth phases and in synchronized and greening cells. Photosynth Res 122:261–273
Kis M, Sipka G, Asztalos E, Rázga Z, Maróti P (2015) Purple non-sulfur photosynthetic bacteria monitor environmental stresses. J Photochem Photobiol B 151:110–117
Kocsis P, Asztalos E, Gingl Z, Maróti P (2010) Kinetic bacteriochlorophyll fluorometer. Photosynth Res 105:73–82
Labrenz M, Druschel GK, Thomsen-Ebert T, Gilbert B, Welch SA, Kemner KM, Logan GA, Summons RE, De Stasio G, Bond PL, Lai B, Kelly SD, Banfield JF (2000) Formation of sphalerite (ZnS) deposits in natural biofilms of sulfate-reducing bacteria. Science 290:1744–1747
Langston WJ, Bebianno MJ (1998) Metal metabolism in aquatic environments. Springer Science & Business Media, Berlin
LaVoie SP, Mapolelo DT, Cowart DM, Polacco BJ, Johnson MK, Scott RA, Miller SM, Summers AO (2015) Organic and inorganic mercurials have distinct effects on cellular thiols, metal homeostasis, and Fe-binding proteins in Escherichia coli. J Biol Inorg Chem 20(8):1239–1251
Le Faucheur S, Tremblay Y, Fortin C, Campbell PGC (2011) Acidification increases mercury uptake by a freshwater alga Chlamydomonas reinhardtii. Environ Chem 8(6):612–622
Liehr SK, Chen H-J, Lin S-H (1994) Metals removal by algal biofilms. Water Sci Technol 30:59–68
Ma Z, Jacobsen FE, Giedroc DP (2009) Metal transporters and metal sensors: how coordination chemistry controls bacterial metal homeostasis. Chem Rev 109(10):4644–4681
Mailman M, Stepnuk L, Cicek N, Bodaly RA (2006) Strategies to lower methyl mercury concentrations in hydroelectric reservoirs and lakes: a review. Science of the total. Sci Total Environ 368(1):224–235
Malik A (2004) Metal bioremediation through growing cells. Environ Int 30:261–278
Maróti P, Wraight CA (1988) Flash-induced H+ binding by bacterial photosynthetic reaction centers: comparison of spectrometric and conductometric methods. Biochim Biophys Acta 934:314–328
Matsushita T, Hirata H, Kusaka I (1988) Calcium channel blockers inhibit bacterial chemotaxis. FEBS Lett 236(2):437–440
Mehta SK, Gaur JP (2005) Use of algae for removing heavy metal ions from wastewater: progress and prospects. Crit Rev Biotechnol 25:113–152
Milano F, Dorogi M, Szebényi K, Nagy L, Maróti P, Váró Gy, Giotta L, Agostiano A, Trotta M (2007) Enthalpy/entropy driven activation of the first interquinone electron transfer in bacterial photosynthetic reaction centers embedded in vesicles of physiologically important phospholipids. Bioelectrochemistry 70:18–22
Moore MD, Kaplan S (1994) Members of the family Rhodospirillaceae reduce heavy metal oxyanions to maintain redox poise during photosynthetic growth. ASM News 60:17–23
Munoz R, Guieysse B (2006) Algal-bacterial processes for the treatment of hazardous contaminants: a review. Water Res 40(15):2799–2815
Nabi S (2014) Toxic effects of mercury. Springer, New Delhi, p 268
Najera I, Lin CC, Kohbodi GA, Jay JA (2005) Effect of chemical speciation on toxicity of mercury to Escherichia coli biofilms and planktonic cells. Environ Sci Technol 39(9):3116–3120
Nevo Y, Nelson N (2006) The NRAMP family of metal-ion transporters. Biochimica et Biophysica Acta 1763: 609–620
Patra M, Sharma A (2000) Mercury toxicity in plants. Bot Rev 66(3):379–422
Puranik PR, Paknikar KM (1999) Biosorption of lead, cadmium, and zinc by Citrobacter strain MCM B-181: characterization studies. Biotechnol Prog 15:228–237
Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE (2001) A prokaryotic voltage-gated sodium channel. Science 294(5550):2372–2375
Schaefer JK, Rocks SS, Zheng W, Gu B, Liang L, Morel FMM (2011) Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria. Proc Natl Acad Sci USA 108:8714–8719
Sigel H, Sigel A, eds. (2009) Metallothioneins and related chelators (metal ions in life sciences). Metal ions in life sciences 5. Royal Society of Chemistry, Cambridge, ISBN 1-84755-899-2
Singh A, Kuhad RC, Ward OP (2009) Biological remediation of soil: an overview of global market and available technologies. Advances in applied bioremediation. Springer, Berlin
Siström WR (1962) The kinetics of the synthesis of photopigments in Rhodopseudomonas sphaeroides. J Gen Microbiol 28:607–616
Sloof JE, Viragh A, Vanderveer A (1995) Kinetics of cadmium uptake by green-algae. Water Air Soil Pollut 83(1–2):105–122
Spoering AL, Lewis K (2001) Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 183:6746–6751
Steunou AS, Liotenberg S, Soler M-N, Briandet R, Barbe V, Astier Ch, Ouchane S (2013) EmbRS a new two-component system that inhibits biofilm formation and saves Rubrivivax gelatinosus from sinking. Microbiol Open 2(3):431–446
Teitzel G, Parsek M (2003) Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Environ Microbiol 69:2313–2320
Théraulaz F, Thomas OP (1994) Complexometric determination of Mercury(lI) in waters by spectrophotometry of its dithizone complex. Mikrochim Acta 113:53–59
Torres M, Goldberg J, Jensen TE (1998) Heavy metal uptake by polyphosphate bodies in living and killed cells of Plectonema boryanum (Cyanophyceae). Microbios 96:141–147
Turksen, Kursad (Ed.) (2015) Bioprinting in regenerative medicine. Springer International Publishing, Berlin. doi:10.1007/978-3-319-21386-6$4
Vijayadeep C, Sastry P (2014) Effect of heavy metal uptake by E. coli and Bacillus sps. J Bioremediation Biodegr 5:238
Wiener JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM (2003) Ecotoxicology of mercury, Chap. 16. In Hoffman DJ, Rattner BA, Burton GA, Cairns J (eds) Handbook of ecotoxicology, 2nd edition. CRC Press, Boca Raton, pp. 409–463
Winkelmann G, Winge DR (1994) Metal ions in fungi. Marcel Dekker, Inc, New York
Youssef NH, Couger MB, McCully AL, Criado AEG, Elshahed MS (2015) Assessing the global phylum level diversity within the bacterial domain: a review. J Adv Res 6(3):269–282
Acknowledgements
We are grateful to Prof. James Smart, University of Tennessee, Martin, USA, for discussions and careful reading of the manuscript. Thanks to COST (CM1306), GINOP-2.3.2-15-2016-00001, OTKA-K 112688, and EFOP − 3.6.2–16 for financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kis, M., Sipka, G. & Maróti, P. Stoichiometry and kinetics of mercury uptake by photosynthetic bacteria. Photosynth Res 132, 197–209 (2017). https://doi.org/10.1007/s11120-017-0357-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-017-0357-z