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�:The activity of heterotrophic bacteria on the DOM - metal complex affects copper speciation and bioavailability in aquatic ecosystem

Patr�cia F. M. Nogueira(1*), Marcelo M. Nogueira(2), Maria da Gra�a G. Mel�o(3), Ana T. Lombardi(4)


Universidade de S�o Paulo, Instituto de F�sica de S�o Carlos, Grupo de Nanomedicina e Nanotoxicologia , Avenida S�o Carlense 400, S�o Carlos, SP, Brazil. (1*), pmayrink1@yahoo.com.br
Universidade de S�o Paulo, Escola de Engenharia de S�o Carlos, N�cleo de Estudos de Ecossistemas Aqu�ticos, Avenida S�o Carlense 400, S�o Carlos, SP, Brazil. (2)
Universidade Federal de S�o Carlos, Via Washington Luiz, Km 235, CP 676, 13565-905, S�o Carlos, SP, Brazil. Dept. Hirobiologia(3); Dept. Bot�nica(4) 





















Abstract 
Metals are mainly released into the environment by industrial processes where dissolved organic materials (DOM) are present.  This investigation focused on modification of copper species in the presence of aquatic heterotrophic bacteria assemblage and natural dissolved organic materials. Copper dynamics during bacteria growth was evaluated through the determination of dissolved and particulate copper. The results showed a reduction of organic carbon, an increase of free Cu2+ ions followed by adsorbed and internalized copper. This study demonstrated a relevant environmental consequence of heterotrophic bacteria activity upon DOM-metal complex, where free copper, a more toxic copper species, were released into the environment.


Keywords: copper; toxicity; bacteria; dissolved organic matter



















Introduction
The speciation of trace metals in natural waters is widely recognised as a key to understanding the ecotoxicological impacts. In natural freshwater systems, the toxicity is strongly dependent on metals� speciation, where the key species is the free metal ion (M+), which is usually presumed to be in equilibrium with various dissolved or particulate ligands and with the epithelial or cell surfaces of aquatic organisms [1]. So, in aquatic ecosystems trace metals may interact with a variety of molecules that may include inorganic (HCO3-, CO32-, SO42-, HS-, Cl-) and organic ligands (humic and fulvic acids, biological molecules, colloidal particles), and surface of the organisms [2]. The bioavailability and toxicity of trace metals to microorganisms are related to their ability to cross biological surfaces [3], which is lesser when metal is complexed [4, 5]. The importance of natural DOM in the environment has been recognized due to its metal complex capacity [6], and also as energy source for heterotrophic bacteria assemblage [7]. These organisms represent important components in aquatic systems, responsible for the regeneration of nutrients and transfer of carbon and energy [8, 9]. 
The microbiota can affect the fate of many contaminants by contributing to their removal through uptake, degradation, or transformation [10]. However, the introduction of metals in the environment can produce considerable modifications of the microbial communities and their activities [11]. The modes of interaction between metal speciation and microorganisms are dominates by the presence and activity of microorganisms in natural aquatic ecosystems and can be having diversity forms: accumulation and efflux [3]; ligand excretion [4, 5, 12] and adsorption onto cell wall [13]. Therefore, the bioavailability and toxicity of trace metals to microorganisms are related to their ability to cross biological surfaces, which is influenced by metal speciation, the physic and chemistry of the medium, and size and nature of microorganisms [3]. Thus, as supported by literature data, DOM-complexed copper is usually less to toxic microorganisms than free Cu2+ ions [4, 5, 12]. 
	Among trace metals, copper is an essential metal for microorganisms survival because its redox properties.  It can be converted into oxidized (Cu2+) and reduced (Cu1+) states as catalytic cofactor in enzymatic reactions. Some copper dependent enzymes are Cu/Zn superoxide dismutase (antioxidant defense), cytochrome c oxidase (mitochondrial respiration), lysyl oxidase (development of connective tissue), and trypsinase (melanin biosynthesis) [14] may be mentioned. Nevertheless, toxic effects are observed when the concentration of copper exceeds that required for the healthy growth of organisms. It has been shown that inside the cell, copper ions can accumulate and react to generate hydroxyl radicals that damage proteins, lipids and nucleic acids [15]. Consequently, cellular healthy functioning is dependent on copper regulation by the organism, such as its transport, distribution and storage.
Information regarding the interactions of metals with aquatic biota and natural DOM are thus of great ecological interest and may give insights regarding metal transport and transformations in aquatic ecosystems. However, few investigations address copper speciation as it may be affected by microorganisms activity in the presence of natural DOM. The aims of the present research were to evaluate the influence of bacteria assemblage activity on copper speciation under laboratory controlled conditions. 

Materials and Methods
The experiments were performed using autoclaved (120 (C, 30 min) reconstituted freshwater with hardness as 44.0 mg CaCO3 L-1, pH 6.8 and 160 �S cm-1 conductivity [16]. The reconstituted freshwater was prepared using glass distilled water to which CaSO4.2H2O (1.5 g L-1), KCl (0.2 g L-1), NaHCO3 (4.8 g L-1), MgSO4.7H2O (6.1 g L-1) were added. 
Only polycarbonate and Teflon� laboratory materials were used throughout. As routine, these were washed with 1.0 mol L-1 HCl (7 days) and rinsed with glass distilled water prior to use. The 0.2 �m acetate filters (Sartorius) were washed with 1.0 mol L-1 HCl (12 hours) and rinsed with glass distilled.
Suwannee River Natural Organic Matter (DOM) commercialized by the International Humic Substances Society was used as natural dissolved organic material for the experiments. It was added in a concentration of 10.0 mg.L-1, quantified as 7.0 mg.L-1 total organic carbon using an organic carbon analyzer (TOC-5000 Analyzer, Shimadzu, Japan). 
Copper was furnished as CuCl2 (Titrisol, Merck) in a total initial dissolved concentration of 1.8(10-6 mol.L-1. Copper was quantified as particulate, total dissolved and free Cu2+ ions. 

DOM copper complex capacity
The DOM complexation capacity for copper binding was previously determined to adjust the concentration of total copper to be added in the beginning of the experiments, so few copper would remain as free Cu2+ species.
 The copper complexing properties (K� and CL) were previously determined through copper titrations. Titrations were performed by incrementally adding copper from 8x10-7 to 4.4x10-5 mol.L-1 and detected as free Cu2+ ions using ion selective electrode (Analion, Ribeir�o Preto, Brazil). Three replicate titrations were performed on 10 mg L-1 aqueous solution of the DOM previously filtered through acid cleaned (HNO3 1.0 mol L-1) 0.2 �m membrane filter. Titrations were buffered with PIPES (piperazine-N,N�-bis[2-ethanesulfonic acid], Sigma-Aldrich) at pH 6.8 and a final concentration of 7x10-3 mol.L-1. Ionic strength was kept at 10-1 mol L-1 using ultrapure NaNO3 (Fluka Chemie, MicroSelect). Blank copper titrations were performed on reconstituted freshwater without DOM. Titration data were converted from millivolts to pCu = -log [Cu2+] by means of the Nernst equation, in which the electrode slope (29 - 30 mV) was obtained from daily performed electrode calibration curves. Scatchard Plots were used to obtain K� and CL (�mol L-1) values; mean CL value have delineated the total copper concentration to be added at the beginning of the experiments.

Experimental design
Heterotrophic bacteria were obtained by sequential filtration of natural freshwater (700 mL) collected from freshwater lake in triplicate. The water were first filtered through a glass fiber filter (GF/C, Whatman) to remove predators and then on an acetate membrane filter with 0.2 �m pore size (Sartorius) to retained bacteria and to be used as inoculums. Bacteria cultures were performed on 1000 mL polycarbonate Erlenmeyer flasks filled with 700 mL of the reconstituted water to which one filter with a fraction of natural bacteria community was inoculated. Heterotrophic bacteria density was observed to different treatments with three replicates each: DOM (control) and DOM+Cu, while the copper dynamic was evaluated in the DOM+Cu treatment.
After inoculation, the experimental flasks were incubated in the dark on a shaker at 60 rpm (Nova �tica, Brazil) temperature of 25(C ( 2 [17] and a pH 6.8. Bacteria density was quantified through light absorption (540 nm, Shimadzu Spectrophotometer, Japan) [18] at 0, 2, 4, 6, 12, 24 and 48  hours of incubation. Only to report internalized and adsorbed copper per unit bacteria cells, these organisms were counted on 0.2 (m pore size black filters (Ispore, Millipore), under an epifluorescence microscope, after culture samples were preserved with formalin 4% and stained with 0.125 mg.mL-1 of DAPI (4�,6-diamidino-2-phenylindole) [19].  In the same time of incubation, samples (50 mL) were taken and filtered through 0.2 (m pore size acetate membrane filters (Sartorius). These filters were further used for the determination of adsorbed and internalized copper, and the filtrate was used for dissolved copper determinations (total and free copper ions) and total organic carbon (TOC-5000 Analyzer, Shimadzu, Japan). 

Copper determinations
Total dissolved copper was determined in 10 mL filtrate samples. They were acidified using ultra pure HNO3 (Fluka Chimie, Switzerland) to a final concentration of 2.0 mol L-1 and followed to Atomic Absorption Spectroscopy (AAS-GF) analysis using a Varian AA220 instrument (Mulgrave, Australia) equipped with graphite furnace (Eletrochemical Trace Analyser, MD394). 
Free Cu2+ ions were determined immediately after sampling in 40 mL aliquots of the filtrate using ion selective electrode (ORION, USA) under controlled experimental conditions. Potential readings were obtained using a Digimed DMPH-2 pH meter with 0.01 mV resolution at constant temperature (25 (C + 1) together with a glass double-junction reference electrode Ag/AgCl (ANALION, Brazil). NaNO3 was used as internal bridge at a concentration of 1.0 mol L-1. Sample ionic strength was adjusted to 0.1 mol L-1 using high purity NaNO3 (MicroSelect, Fluka, Switzerland). Copper measurements were reproducible to � 4 % and metal-ion buffers were used for electrode calibration [20] to extend the lower limit of free copper ions determination to 5x10-12 mol.L-1. Daily Cu-ISE calibration curves were performed.
For particulate copper determination (adsorbed onto bacteria cell surface and internalized), an aliquot of bacteria culture (50 mL) was filtered through 0.2 (m pore size acetate membrane filter (Sartorius). For adsorbed copper, the filter was rinsed with 5 mL of 2x10-2 mol L-1 EDTA (C10H16N2O8) at pH 7.0 and let bacteria cell contact with EDTA for 30 s [21]. The 5 mL EDTA solution was completed to 50 mL with glass distilled water and filtered (0.2 (m - Sartorius) and the filter was dried overnight (60 �C), acid digestion (HNO3) [16] and followed to internalized copper determination through AAS-GF. The filtrate was acidified (HNO3 - 2.0 mol L-1) for adsorbed copper determination through AAS-GF. 

Results and Discussion
DOM copper complex capacity
Scatchard Plot Analysis of DOM titration data showed that two copper complexing ligands were present (Figure 1).  Stronger (K�1) ligands with log conditional stability constant of 7.47 present at 3.7x10-6 mol L-1 concentration, and weaker ligands with log conditional stability constant of 5.00 at a concentration of 7.6x10-6 mol L-1 were detected in the DOM. The results of complexation showed that the DOM (SR-NOM) have a stronger complexation capacity (3.5 x10-6 mol.L-1) of copper. Natural organic matter (NOM) plays a predominant role in complexing metals in aquatic environment [1]. The capacity of complexation of dissolved SR-NOM in this work is higher than copper concentration (1.7x10-6 mol.L-1) used, demonstrating that all of most copper inoculated was complexed, few remaining as the highly bioavailable free Cu2+ ion species. 
FIGURE 1

Bacteria density on dissolved organic carbon 
Heterotrophic bacteria density and DOC as function of experimental time is reported in figure 2. It shows that the higher population density was quantified at 24 and 48 h of incubation and copper affected the growth. At this experimental time, total dissolved organic carbon was 4 mg C L-1, value that corresponded to 57% of total furnished carbon as natural DOM (figure 2). The observed dissolved organic carbon (DOC) reduction in bacteria cultures could either be due to use as energy source by the bacteria community [7, 22] and/or its adsorption of DOM onto charged bacteria cell surface [13, 23].
 In this study, the increased of bacteria density and a reduction of DOM concentration is an indicative that a refractory organic matter was used as energy source by bacteria assemblage. The results are according to literature dates  where Docherty et al. [22] reports on the degradation of refractory organic matter by bacteria and obtained a significant positive correlation between the concentration of humic materials and microbial community activity and composition. The authors followed the degradation of natural DOM of several molecular weights and concluded that microbial community growth could be supported by a variety of different DOM types, raveling metabolic versatility in relation to its adjustment and adaptations to new carbon sources in the environment. Also, the authors showed that high molecular weight DOM, normally considered as refractory organic materials were used by the bacteria.
However, Moran and Hodson [24] and Ellis et al. [25] showed that refractory materials are difficult of degradation by microorganisms. Moran and Hodson [24] showed that the labile fraction of DOM from a lake supported a fourfold higher secondary production than humic substances from the same environment. Ellis et al. [25] showed that microbial growth rate in refractory humic acid treatments was lower than in more labile amino acid and carbohydrate treatments. 
FIGURE 2 

Copper dynamic in the experiments
Figure 3 reports free Cu2+ ions, adsorbed and internalized copper concentrations in the experiments as function of time after bacteria inoculation. It shows an increase of free Cu2+ ions about 2 h bacteria incubation (p<0.001, ANOVA), which decreased afterwards (p<0.001, ANOVA). While free Cu2+ ions concentration was kept low (10-9 mol.L-1), a gradational increase of adsorbed copper was observed; this being followed by a sharp increase of internalized copper (p<0.001, ANOVA), which finally decreased at 48 h incubation. In 48 h of incubation all species of copper appear low probably because of an increased of bacteria cell number. Total dissolved copper concentration decreased and remained nearly constant (0.91x10-6 + 0.05x10-6 mol L-1) during the whole incubation period.
FIGURE 3
In this study, the low adsorbed copper in 0.5 hour, a increase of free Cu2+ ions detected in 2 h of incubation time and the decrease of DOC concentration, again suggest DOM degradation by the microorganisms. So, with less dissolved organic matter in the medium, a higher free Cu2+ ions concentration will detected.
The role of chemical speciation on metal bioavalability is often successful in predicting a reduction in trace metal effects due to complexation (eg. Organic ligands) or competition (eg. H+, Ca2+), both processes result in a decreased interaction of the metal with uptake sites on the surface of the organisms [26, 27]. How showed in this study, the heterotrophic bacteria activity upon DOM make available toxic specie of copper (free Cu2+ ions). The activity of bacteria on copper- DOM complex have an ecological consequences since them may modify the copper speciation in the environment, not only through the excretion of DOM [28], but also by DOM modification [29].  
Considering that organism-metal interaction depends on metal speciation, the increase of free Cu2+ ions as result of bacteria activity may affect such interactions and consequently metal bioavailability. This is supported by Worms et al. [3], which discuss that the impact of metals on aquatic organisms and presupposes direct or indirect interactions between metals and organisms, such as binding to biological ligands and transfer through the biological membranes. 
Ours studies demonstrated that the increase of free Cu2+ ions was followed by an increase of adsorbed (12h) and internalized (24h) copper in the bacteria. In the same time the bacteria density in DOM-Cu treatment was lower than control. These results indicate that copper internalization flux across the plasma membrane and toxicity is a function of the free metal ion concentration in the bulk solution. The effect of natural organic ligands on metal speciation and its availability and toxicity to bacteria has been discussed in literature [30, 31, 32]. Kungolos et al. [31] demonstrated that copper bioaccumulation in the photobacterium Vibrio fischeri decreased with the addition of humic acid, and that free Cu2+ ions were responsible for the toxic effects observed. Smiejan et al. [32] found that Cd uptake by the freshwater bacterium Rhodospirillum rubrum was a function of free Cd2+ ion concentration. Keung et al. [30] showed that Cd and Zn uptake by the bacteria Bacillus firmus correlated best with the free metal concentration than to hidrophilic metal-complexes.
These results is according to the free ion activity model (FIAM) that explain the relation between the free metal ion concentration in the bulk solution and the biological responses in organisms [33].  The FIAM assumes that the plasma membrane is the primary site for metal uptake, consequently metal internalization flux across the plasma membrane is a function of the free metal ion concentration in the solution. Finally, van Leeuwen et al. [34] proposed that organic complexed metal ions, like a DOM-Cu complex have lower diffusion coefficient across microorganisms cell wall, thus resulting in lower internalization.  So, the free ion concentration is show to correlate best to bioavailability and toxicity.
Conclusion
The complexes of metals are the predominant form that was finding in the aquatic ecosystems (> 90 %),   so this is ecological important the determination of quantitative contribution of these complexes to the metal take up processes to the organisms. From the present results, we conclude that bacteria activity upon DOM-metal complex have modified the speciation of copper in its surrounding environment, turning low availability copper-DOM complexes onto the highly bioavailable free Cu2+ ions species.

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Figure captions
Figure 1 � Ion selective electrode calibration curve using metal buffers. Free copper concentration (mol.L-1) plotted as function of potential readings (mV). 
Figure 2 - Bacteria density curve (absorbance at 540 nm) and dissolved organic carbon concentration (mg.L-1) as function of time. Values are mean +SD of three experimental replicates. 
Figure 3 - Particulate copper (x10-8�gCu.cel-1) and free copper ions (x10-7 mol.L-1) as function of experimental time for experimental treatments. Values are mean +SD of three experimental replicates. 
























Figure 1




















Figure 2


 EMBED Origin50.Graph  














Figure 3
 EMBED Origin50.Graph  


















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Youez - 2016 - github.com/yon3zu
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