Tellurite Removal by a Tellurium-Tolerant Halophilic Bacterial Strain, Thermoactinomyces Sp. QS-2006

Ann Microbiol (2012) 62:1031–1037 DOI 10.1007/s13213-011-0343-1

ORIGINAL ARTICLE

Tellurite removal by a tellurium-tolerant halophilic bacterial strain, Thermoactinomyces sp. QS-2006

Mohammad Ali Amoozegar & Maryam Khoshnoodi & Maryam Didari & Javad Hamedi & Antonio Ventosa & Susan A. Baldwin

Received: 26 March 2011 /Accepted: 5 August 2011 /Published online: 2 September 2011 # Springer-Verlag and the University of Milan 2011

Abstract Among the 25 strains of moderately halophilic (TEM) coupled with Energy Dispersive X-ray (EDX) bacteria isolated from the hypersaline environments of showed that tellurium compounds were adsorbed to the Iran, a Gram-positive and moderately halophilic bacterial bacterium wall and inside the cytoplasm. strain isolated from a saline soil was identified as Thermoactinomyces sp. strain QS-2006. This strain was Keywords Bioremediation . Halophilic bacteria . Microbial found to tolerate high concentrations of tellurite with metal resistance . Tellurite . Thermoactinomyces growth occurring up to a concentration of 500 mM Te. When the strain was cultured aerobically in medium containing 0.1–3.0 mM potassium tellurite, tellurium was Introduction removed from the soluble toxic oxyanion form under a wide range of conditions including pH (7–10), temperature The rare element, tellurium (Te) is among the least (30–45°C), agitation (0–220 rpm), and various concentrations abundant in the earth’s crust (<10 ppb) (Ollivier et al. of salts including NaCl , KCl , NaNO3 and NaCH3COOH 2008). It belongs to the same group (VIA) of the periodic (0.5–1.5 M). Maximum tellurite removal (95.5%) occurred table as selenium and sulfur, and is an essential trace in a medium containing 1–3% NaCl with a pH of 7.5 element in a manner similar to Se (Chasteen et al. 2009; incubated at 35°C. Transmission Electron Microscope Pérez et al 2007; Taylor 1996). The oxidized forms of tellurium are highly soluble, environmentally mobile, toxic M. A. Amoozegar (*) : M. Khoshnoodi : M. Didari and bioavailable in the environment in contrast to their Extremophiles Laboratory, Department of Microbiology, elemental counterparts (Chasteen et al. 2009; Pearion and School of Biology, College of Science, University of Tehran, Jablonski 1999; Summers and Jacoby 1977; Summers and – Tehran, Iran P. O. Box 14155 6455 Silver 1978). For example, tellurite (TeO −2) is highly toxic e-mail: [email protected] 3 toward most microorganisms at concentrations as low as − J. Hamedi 1 μgml 1 (Pearion and Jablonski 1999). However, tellurite- Microbial Biotechnology Laboratory, resistant bacteria do exist in nature and they are often Department of Microbiology, capable of reducing tellurite to its less toxic elemental form School of Biology, College of Science, University of Tehran, Te(0), which can appear as black deposits inside the cell Tehran, Iran (Pérez et al 2007). Tellurium contamination in the environment is increasing A. Ventosa because Te compounds are used as additives to steel, Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Sevilla, primarily for increasing its ductility, as brighteners in Sevilla, Spain electroplating, as promoters for petroleum cracking cata- lysts and as coloring agents in the manufacturing of colored S. A. Baldwin glasses (Rajwade and Paknikar 2003). Tellurium is isolated Department of Chemical and Biological Engineering, University of British Columbia, in the process of copper and lead production as a by- Vancouver, British Columbia, Canada product (Chasteen et al. 2009). Thus, the wide usage of 1032 Ann Microbiol (2012) 62:1031–1037 these metalloids and their emergence in the environment Bacterial strains, culture conditions and identification has renewed interest in methods for Te bioremediation. Indeed, a recent study found that tellurite-resistant Twenty-five moderately halophilic Gram-positive bacterial organisms comprise ∼10% of the total culturable microbial strains were isolated from saline or hypersaline soil samples population (Ollivier et al. 2008). For example, Te-resistant from different regions of Iran. In order to preserve the organisms have been isolated from hydrothermal vents strains, they were cultured in nutrient agar (Merck) plus (Csotonyi et al. 2006), salt marsh sediments (Ollivier et al. 10% (w/v) NaCl (Merck) and were incubated at 30°C for 2008), hypersaline soils (Amoozegar et al. 2008; Kabiri et 10 days. al. 2009) and heavy metal-contaminated sediments (Chien Among the strains isolated, strain QS-2006 exhibited and Han 2009). These organisms were related to the most resistance to tellurite at concentrations as high Gammaproteobacteria of the genera Pseudoalteromonas as 500 mM and grew well at 5% (w/v) NaCl. and Shewanella (Csotonyi et al. 2006; Klonowska et al. Therefore, it was chosen for further study. The strain 2005; Rathgeber et al. 2002), marine isolates within the was taxonomically identified by the University of family Bacillaceae, Rhodotorula spp. yeast (Ollivier et al. Tehran Microorganisms Collection (UTMC), Tehran, 2008), Paenibacillus sp. (Chien and Han 2009), and Iran. Biochemical and physiological characterizations that halophilic bacteria in the genus Salinicoccus (Amoozegar were used for the taxonomic classification were performed in et al. 2008), and the genus Halomonas (Kabiri et al. a basal culture media containing 10% (w/v) NaCl. 2009). Besides volatilization and evasion of Te (Ollivier Scanning electron microscopy (SEM) was used for et al 2008), reduction of either tellurate Te(VI) or tellurite morphological examinations (Zeiss DSM 960 A). The Te(IV) to elemental tellurium Te(0) (Baesman et al. 2007; intact arrangements of spores and mycelia were observed Csotonyi et al. 2006; Pearion and Jablonski 1999)aswell on International Streptomyces Project (ISP) 2 agar as production of exopolysaccharides (Chien and Han containing 10% NaCl after 7 days of cultivation at 2009) have been reported as mechanisms for tellurium 30°C using the cover-slip technique (Kawato and resistance. Shinobu 1959). Strain QS-2006 was prepared for SEM There is a particular interest in halotolerant and according to the method of Chun et al. (2000). The halophilic species for bioremediation since many contam- bacteria were fixed for 10 min in 2% w/v glutaraldehyde inated environments are saline. Indeed, certain halophilic and washed once in distilled water. The cells were then bacteria have been found to be useful for removal of post-fixed in 4% w/v aqueous OsO4 for 24 h before being tellurite, selenite and chromate (Amoozegar et al. 2005, dehydrated with a graded ethanol-water series and dried 2007, 2008; Kabiri et al. 2009). One group of organisms, for 24 h. Gram-positive bacteria, which are abundant in most soils, were of particular interest to us since they have very Determination of tellurium oxyanion tolerance flexible metabolisms and have been used for metal removal (Amoroso et al. 2001; Clausen 2000; Lebeau et al. 2002). The tolerance of strain QS-2006 to the tellurium oxyanion In this work, we characterize one particular tellurite- was measured by the agar dilution method (Rathgeber et al. resistant halophilic bacterial strain, which was isolated from 2002; Washington and Sutter 1980). Melted nutrient agar saline soil. We explored the use of this organism for (20 ml) supplemented with tellurite in concentration range removal of Te from its mobile and toxic form, tellurite, in of 0.1–600 mM was poured into 8-cm plates. Then, 10 ml an aqueous solution. To our knowledge, this is the first of the QS-2006 spore suspension containing approximately report of tellurite removal by a halophilic bacterial strain 1.5×108 CFU ml−1 was inoculated on each plate using a with highest tolerance toward tellurite. sampler followed by incubation at 30°C for 10 days. Each plate was prepared in triplicate.

Materials and methods Characterization of tellurite bioremoval

Chemicals Cells were cultured in 100-ml Erlenmeyer flasks containing 25 ml of basal medium supplemented with 5% (w/v) NaCl Diethyldithiocarbamate (DDTC) was obtained from Sigma at different concentrations of potassium tellurite. The basal (St. Louis, MO, USA), and potassium tellurite was acquired medium that we used was Czapek Dox medium containing from Merck (Darmstadt, Germany). The stock solutions 5% (w/v) NaCl (Atlas 1993). This medium was inoculated were prepared in distilled water, then sterilized by passing with 1% of 1.5×108 CFU ml−1 of the spore suspensions through a 0.22-μm filter and maintained at 4°C. Working and incubated aerobically at 30°C on a rotary shaker solutions were stored at 4°C for up to 5 days. (150 rpm) for 10 days, and pH was adjusted at 7.0. The Ann Microbiol (2012) 62:1031–1037 1033 cells were centrifuged at 2,700g for 30 min and the concentration. This strain was called QS-2006 and was supernatant used for determination of residual potassium selected for further study due to its high tolerance for tellurite by a colorimetric method using diethyldithiocarbamate tellurite and because we noticed the formation of black and (DDTC) as described by Turner et al. (1992). gray deposits in the liquid and solid media, respectively. Tellurite removal capacity of the strain was evaluated at The appearance of these precipitates suggested that tellurite different initial concentrations of potassium tellurite (0.1– may have been reduced to elemental tellurium. 3 mM). Later, tellurite removal capacity was tested in basal Strain QS-2006 was filamentous, Gram-positive, strictly media supplemented with 1 mM potassium tellurite at aerobic and fast growing. The strain formed well-developed different concentrations of NaCl (0–20%), different values and branched substrate mycelium, and spores were oval to of pH (7–10) and at different temperatures (30–45°C). rod-shaped with wrinkled surfaces (Fig. 1). The colonies Mixing rate was also changed from static to 220 rpm. The appeared flat or ridged with entire or filamentous margins. effects of various salts was determined by replacing sodium The cell wall peptidoglycan layer contained meso- chloride in the basal medium with sodium acetate, sodium diaminopimelic acid but no characteristic sugars (Becker et nitrate and potassium chloride at concentrations of 0.1, 0.5 al. 1965). Strain QS-2006 was able to grow at temperatures and 1 M, respectively. All these experiments were ranging from 10 to 40°C with optimal growth at 30°C. performed in triplicate. Negative controls were run to Growth was observed within the pH range of 6.0–8.0 and in confirm that tellurite removal involved the presence of NaCl concentrations up to 20 % (w/v) with optimal growth bacteria and were not due to the other experimental at 5% (w/v) NaCl (Table 1). Based on the combined conditions, such as high agitation or high Te concentrations. chemotaxonomic, phenotypic and genetic information, QS- Dry weight was used to determine cell biomass. An 2006 was classified as Firmicutes; Bacilli; Bacillales; aliquot of cell suspension was centrifuged and the pellet unclassified Bacillales in genus Thermoactinomyces. washed several times with distilled water. The washed cells were dried in an oven at 100°C until a constant weight was Effect of different medium conditions on tellurite obtained. bioremoval

Transmission Electron Microscopy (TEM) The effect of initial tellurite concentration on tellurite removal was investigated in basal medium supple- TEM was used to locate Te-containing compounds in and mented with potassium tellurite in the concentration around the bacteria cells. The Thermoactinomyces sp. QS- range 0.1–3.0 mM Te for an incubation period of 2006 cells were first grown in basal medium supplemented 10 days. As shown in Fig. 2, for those cultures where with 1 mM potassium tellurite until the mid-exponential the initial Te concentration was 1 mM Te or greater, up to phase of growth. When the cultures turned black, cells were 80–90±3% of tellurite was removed after 5–10 days of harvested and fixed for 7 h in glutaraldehyde followed by incubation. Whereas when initial Te concentrations were washing with distilled water (Iterson and Leene 1964). Thin less than 1.0 mM, the maximum tellurite removal was sections were prepared by a LKB ultratome (Leica Ultracut much less, only 48–55 ±6% even after 10 days incuba- R). The unstained ultra thin sections were examined by using a TEM (model EM900; Zeiss West Germany) operating at 50 kV. An energy dispersive x-ray (EDX) analysis system operating at 200 kV on another TEM (CM200FEG; Philips) was used to determine the elemental composition of the black deposits.

Results

Screening of halophilic Gram-positive bacterial strains resistant to tellurite

Of the 25 Gram-positive bacterial strains isolated from different saline and hypersaline soils in Iran, 13 were halophilic. One particular strain from a hypersaline soil in Qom tolerated high concentrations of potassium tellurite, Fig. 1 SEM image of Thermoactinomyces sp. strain QS-2006 up to 500 mM in nutrient agar at 5% (w/v) NaCl (scale bar 10 μm) 1034 Ann Microbiol (2012) 62:1031–1037

Table 1 Comparison of phenotypic characteristic of strain QS-2006 increased to 10, which resulted in only 45±2% removal from other Thermoactinomyces species (Fig. 3). Both Te removal and cell growth were significantly Characteristic T. vulgarisa T. thalpophilusa Strain affected by temperature, with higher cell concentrations at QS-2006 the lower temperature of 30°C but higher tellurite removals at the higher temperature of 35°C. No growth was observed Aerial mycelium at 45°C. Abundant + + + The effect of aeration on removal of potassium tellurite –– – Transient by Thermoactinomyces sp. strain QS-2006 was examined White + + + under static (no shaking) and aerobic (shaking) conditions. Growth at: The maximum potassium tellurite removal (98 ± 5%) and –– 10°C + cell biomass concentration (115 g/l) were observed at the 30°C – ++highest agitation rate tested, 220 rpm (Fig. 4). When 40°C – ++varying the medium salinity, maximum tellurite removal 55°C + + – was observed in the presence of 1–3 ±1% (w/v) NaCl Degradation of: (Fig. 5). However, above 3 ±1 % (w/v), tellurite removal Casein + + + decreased dramatically. The strain QS-2006 could also Gelatin + + – reduce tellurite when introduced to other types of salts but Starch – ++amounts removed were less than those observed with Keratin –– + NaCl (Fig. 6). When sodium nitrate was added, a Growth in the presence of: maximum removal of 37±5 % was observed at 0.5 M, NaCl 20 % (w/v) NT – + for potassium chloride the maximum (30 ±4%) occurred NaCl 5.0% (w/v) + – + at 1.5 M. However, with the increase of sodium acetate NaCl 1.0% (w/v) + + + and sodium nitrate concentrations from 0.5 M to 1 M, tellurite removal decreased. The cell growth was not + positive, − negative, NT not tested affected by the concentrations of these salts, except that a ’ From Bergey s Manual of Systematic Bacteriology (Lucey 1986) no growth was observed in the medium with 1.5 M sodium acetate. tion. For the lower Te concentrations, there was no significant correlation between maximum removal and Transmission electron microscopic observations and EDX initial Te concentration. Theredoesseemtobeatrend analysis towards slower tellurite removalratesearlyoninthe cultures with higher initial Te concentrations. Since the Using transmission electron microscopy (TEM), black best overall Te removal was observed with an initial deposits were located attached to the cell wall and some concentration of 1 mM, the subsequent experiments were were located inside the cytoplasm or near the cytoplasm carried out with this concentration. membrane (Fig. 7a, b). With EDX analysis these were The culture medium pH did not affect maximum Te identified as Te by EDX (Fig. 7C). No intracellular deposits removal in the range from 7 to 8.5, except when the pH was were observed in bacteria grown in the control medium.

Fig. 2 The effect of initial potassium tellurite concentration on Te removal by the strain QS-2006 in basal medium containing 5% (w/v) NaCl (pH 7.5) Ann Microbiol (2012) 62:1031–1037 1035

Fig. 5 The effect of NaCl concentrations on the tellurite removal and growth of the strain QS-2006 in basal medium containing 1 mM Fig. 3 The effect of initial pH (left) and temperature (right) on cell potassium tellurite (pH 7.5) after 10 days . No growth and Te removal growth and tellurite removal of the strain QS-2006 in basal medium were observed at 20% (w/v) NaCl. Data points represent the means of containing 5% (w/v) NaCl and 1 mM potassium tellurite after 10 days. three separate experiments, and error bars the standard deviations Data points represent the means of three separate experiments, and error bars the standard deviations 50% even after 10 days incubation. In general, halophilic microorganisms have exceptional properties including high Discussion concentrations of anions and cations for necessary for growth, hence they are not only naturally tolerant to some elements Moderately halophilic bacteria comprise a diverse group that are toxic to other microorganisms but they also have a of prokaryotes and can be used for bioremediation of requirement for these elements. It seems that the presence of K metal-polluted environments (Amoozegar et al. 2008; in the chemical structure of the oxyanion studied was one of Kabiri et al. 2009). Most tellurite-resistant microorganisms reasons for the higher reduction and removal of tellurite with characterized to date can tolerate tellurite at concentrations increased tellurite concentrations in the medium. Potassium ranging from 0.01 to 150 mM (Amoozegar et al. 2005, and sodium are necessary elements for the activity of enzymes 2007, 2008; Chien and Han 2009;Kabirietal.2009; and pumps in halophiles; therefore, it seems that these Pearion and Jablonski 1999; Rajwade and Paknikar 2003; elements enhanced the toxic metal tolerance and removal Rathgeber et al. 2002; Soudi et al. 2009). Here, we report (Margesin and Schinner 2001). a very high tolerance to tellurite (500 mM) by a halophilic Te oxyanion removal and growth of the strain was Gram-positive strain. detected in the absence of any salts and over a range of Strain QS-2006 showed high efficiency in detoxifying moderate NaCl concentrations, as well as in the tellurite. It could reduce more than 90±3% of 1 mM presence of low concentrations of other salts (NaCl, potassium tellurite to less toxic elemental tellurium after NaNO ,andCHCOONa). The culture also grew well 5 days, while, when initial Te concentrations were less than 3 3 under these conditions. The ability of this strain to remove 1.0 mM, the maximum tellurite removal was only about tellurite in the presence of different types of salts and over a relatively wide range of concentrations makes it very promising for use in remediating polluted environments

Fig. 4 The effect of the mixing rate on tellurite removal and growth Fig. 6 The effect of various salts on the tellurite removal of the strain of the strain QS-2006 in basal medium containing 1 mM potassium QS-2006 in basal medium containing 1 mM potassium tellurite tellurite (pH 7.5) after 10 days. Data points represent the means of (pH 7.5) after 10 days. Data points represent the means of three three separate experiments, and error bars the standard deviations separate experiments, and error bars the standard deviations 1036 Ann Microbiol (2012) 62:1031–1037

Fig. 7 Transmission electron micrograph of strain QS-2006 and X-ray energy dispersive spectrum of the intracellular deposits: a cells cultured in basal medium without tellurite; b cells cultured in basal medium containing 1 mM tellurite; c X-ray energy-dispersive spectrum of the intracellular deposits in the cells cultured in basal medium containing 1 mM tellurite. Bars (a)1μm; (b)2μm

that are often moderately saline. The same observation can Metallic tellurium particles were also found outside be made with respect to pH and temperature. It was the cells, where they may be located due to a system of interesting that, although Te removal increased when the tellurium efflux or due to secretion of an extracellular temperature was increased from 30 to 35°C, the cell enzyme. Similarly, another study of two strict anaerobes growth was much less. Bacillus selenitireducens and Sulfurospirillum barnesii Thermoactinomyces sp. strain QS-2006 appeared to observed that, although Te(0) crystals occurred intracel- accumulate Te as electron-dense, black intracellular deposits. lularly, most were found outside the cell (Baesman et al. These deposits have previously been shown in several other 2007). They also observed that reduction of either strains of bacteria and archaea to consist of elemental tellurate Te(VI) or tellurite Te(IV) to elemental tellurium tellurium (Amoozegar et al. 2007, 2008; Borghese et al. Te(0) resulted in the formation of unique crystalline Te(0) 2004;ChienandHan2009; Klonowska et al. 2005; Pearion nanoarchitectures, which differed between the two micro- and Jablonski 1999; Rajwade and Paknikar 2003; Soudi et organisms (Baesman et al. 2007). al. 2009; Yamada et al. 1997). The localization of tellurium Biological transformation of tellurite to elemental tellurium in the cytoplasm or near the cytoplasmic membrane has also could offer an important mechanism for the removal of toxic been reported for other tellurite-reducing bacteria, such as tellurite from polluted environments, particularly in the Shewanella oneidensis (Kabiri et al. 2009). The utilization of presence of salt. Therefore, this strain may be a good tellurite as a terminal electron acceptor has been documented candidate for bioremediation of highly polluted effluents from in isolates from hydrothermal vents (Baesman et al. 2007; industrial and mining operations. Conventional chemical Rathgeber et al. 2002). Anaerobic tellurate respiration has methods for removing toxic oxyanions are expensive and been suggested to be a significant component in biogeo- require high energy or large quantities of chemical reagents, chemical cycling of Te under the extreme conditions found at while microbial reduction of these toxic oxyanions is cost hydrothermal vents (Lebeau et al. 2002). effective and supports green technology. Ann Microbiol (2012) 62:1031–1037 1037

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