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Recent Developments for Remediating Acidic Mine Waters Using Sulfidogenic Bacteria.

1. Introduction

Metal mining provides everyday goods and services essential to society. However, this activity has at times caused extensive and sometimes severe pollution of air, vegetation, and water bodies [1]. Streams draining active or abandoned mines and mine spoils are widely considered as hazardous to human health and the environment, but on the other hand, they may also be alternative potential sources of valuable metals [2, 3].

Currently, millions of tons of ores are processed every year by the mining industry and are disposed in the form of waste rocks and mine tailings. As higher-grade ores are diminishing, the primary ores that are processed by mining companies are of increasingly lower grade (metal content) and the growing amount of waste material produced by mining operations is consequently significant. The use of lower grade ore was made possible by the development of the flotation technique in the late 19th century, which allowed the separation of metal sulfide minerals from gangue minerals that have no commercial value [4]. As a result of selective flotation, about 95 to 99% of the ground primary ores end up as fine-grain tailings, in the case of copper ores. The composition of tailings is directly dependent on that of the ore, and therefore they are highly variable, though pyrite (Fe[S.sub.2]) is frequently the most reactive and dominant sulfide mineral present in tailings wastes [4-6].

Pyritic mine tailings therefore have the potential to become extremely acidic when in contact with surface water. Under oxidizing conditions, pyrite-bearing wastes produce sulfuric acid. The acidic water further dissolves other metals contained in mine waste, resulting in low pH water enriched with soluble sulfate, Fe, Al, and other transition metals, known as acid mine drainage (AMD) (Figure 1) [7, 8].

2. Remediation of Acidic Mine Water

Waters draining from abandoned metal mines and mine wastes are often acidic (pH < 4) and contain elevated concentrations of dissolved metals and metalloids and high osmotic potential associated with concentration of sulfate salts [14]. In most cases, active chemical treatment and passive biological treatment can provide effective remediation of AMD [15] (details and literature of the advantages and disadvantages of these treatment and others are presented in Table 1). A major drawback to both approaches is that the immobilized metals are contained in "sludge" (chemical treatment) or within spent compost (biological treatment) and need to be disposed in specially designated landfill sites, precluding their recovery and recycling. Changes in redox conditions during storage can lead to remobilization of metals (and metalloids such as arsenic) in both sludge and spent composts. In addition, potentially useful and valuable metal resources are not recovered using conventional approaches for remediating mine waters [3,16].

A radically different approach for remediating AMD which, like compost bioreactors, derives from the abilities of some microorganisms to generate alkalinity and to immobilize metals, is referred to generally as "active biological treatment." Microbiological processes that generate alkalinity are mostly reductive processes and include denitrification, methanogenesis, and dissimilatory reduction of sulfate, ferric iron, and manganese (IV), which tend to be limited in AMD. Considering that AMD usually contains elevated concentrations of both ferric iron and sulfate, the ability of some bacteria to use these compounds as terminal electron acceptors suggests that these reactions can be highly useful for mine water remediation. Acidic environments in which sulfur or sulfide minerals are subjected to biologically-accelerated oxidative dissolution characteristically contain large concentrations of soluble sulfate [17]. Therefore, microbial sulfate reduction might be anticipated to occur within anaerobic zones in both acidic and nonacidic environments. Biological sulfidogenesis generates hydrogen sulfide as a result of a reductive metabolic process using sulfate reducing bacteria (SRB). Biological sulfidogenesis has the additional benefits of being a proton-consuming reaction, allowing the increase in pH of the mine water treated contributing towards mitigation and remediation. The hydrogen sulfide generated can be used in controlled situations to selectively precipitate many potentially toxic metals (such as copper and zinc) often present in AMD at elevated concentrations [3, 18]. Active biological treatment has many advantages over alternative strategies for treating mine waters, one of the most important being its potential for recovering metals that are commonly present in AMD.

There have been few successful applications of SRB-mediated active AMD treatment systems, even though this possibility has long been appreciated. One major reason for this is that SRB happens preferentially between pH 6 and 8 [19], whereas AMD generally has a pH between 2 and 4 and commonly pH < 3 [20]. Under these circumstances, a neutralization step is necessary before AMD effluents are subjected to bacterial sulfate reduction or, alternatively, "off-line" systems need to be used. The latter is necessary by the fact that current systems use neutrophilic SRB or sulfur reducing bacteria, and direct exposure to the inflowing acidic solution being treated would be lethal to these microorganisms. Therefore, a separate vessel in which sulfide generated by the bacteria is contacted with the acidic, metal-laden waste water, is required [16, 21]. Examples of this technology are the Biosulfide and Thiopaq processes (Figure 2) operated under the auspices of two biotechnology companies, BioTeq (Canada) and Paques B. V. (The Netherlands), which are currently in operation in various parts of the world.

The Biosulfide process has two stages, one chemical and the other biological. Metals are removed from AMD in the chemical stage by precipitation with biogenic sulfide produced in the biological stage by SRB under anaerobic condition. In this system, hydrogen sulfide is generated by the reduction of elemental sulfur, or other sulfur source, in the presence of an electron donor, such as acetic acid. The gas is passed to an anaerobic agitated contactor in which copper can be precipitated as a sulfide, usually without pH adjustment and without significant precipitation of other heavy metals present in the water. The end result is a high value copper product, usually containing more than 50% of the metal. Other metals such as nickel, zinc, and cobalt can also be recovered as separate high-grade sulfide products, although pH control using an alkali source is usually required to selectively precipitate the metal as a sulfide phase. The high-grade metal sulfide precipitate is then recovered by conventional clarification and filtration to produce a filter cake which can be shipped to a smelter [12].

The Thiopaq process uses another system that involves the use of two biological continuous reactors connected in series (I) to an anaerobic upflow sludge blanket (UASB) reactor for the reduction of oxidized sulfur species. In this reactor, ethanol or hydrogen is utilized by the SRB as electron donor, producing sulfide (mostly HS-) for the precipitation of metal sulfides (which can proceed in the same reactor depending on the toxicity of the wastewater), and (II) an aerobic submerged fixed film (SFF) reactor where the excess sulfide is oxidized to elemental sulfur, using sulfide-oxidizing bacteria. In this process, metals such as Zn and Cd can be precipitated down to very low concentrations [22].

The Paques B. V. process has been successfully implemented at an industrial scale at the gold mine Pueblo Viejo, located in the Dominican Republic. A copper recovery plant installed in 2014 based on sulfide precipitation is used to recover the copper liberated from the gold extraction process. The sulfidogenic bioreactor generates [H.sub.2]S to recover up to 12,000 ton of copper per year generating value and reducing the amount of copper sent to the tailing dam [23]. Application of this process has also been demonstrated on a pilot-scale at the Kennecott Bingham Canyon copper mine in Utah, where >99% of copper present in a pH 2.6 waste stream was recovered [22, 24,25].

Sulfate reduction activity has been reported in low pH ecosystems, for example, in acidic lakes, wetlands, and acid mine drainage [19,26,27]. However, few acidophilic/tolerant SRB have been cultured [16, 26, 28-30]. A major potential advantage of using acidophilic sulfidogens would be to allow simpler engineering designs and reduce operational costs by using single on-line reactor vessels that could be used to both generate sulfide and selectively precipitate target metal(s). Precipitation and removal of many soluble transition metals, often present in AMD emanating from metal mines, may be achieved by ready biomineralization as their sulfides. The produced metal sulfides have different solubilities; therefore metals can be precipitated together or selectively by controlling concentrations of the key reactant [S.sup.2-], which may be achieved by controlling pH ([S.sup.2-] + [H.sup.+] [Left and right arrow] [HS.sup.-]). Copper sulfide, for example, is far less soluble than ferrous sulfide (respective log [K.sub.sp] values of -35.9 and -18.8) and therefore CuS precipitates at pH 2, whereas FeS needs much higher pH to precipitate. Diez-Ercilla et al. [31] have also demonstrated that selective precipitation of metal sulfides occurs naturally in Cueva de la Mora pit lake (SW Spain) and the geochemical calculations match perfectly with the results of chemical and mineralogical composition. Nancucheo and Johnson [3] showed that it was possible to selectively precipitate stable metal sulfides in inline reactor vessel testing two synthetic AMDs in acidic conditions (pH 2.2-4.8). In the first bioreactor, with a composition of feeding similar to AMD at the abandoned Cwm Rheidol lead-zinc mine in mid-Wales, zinc was efficiently precipitated (>99%) as sulfide inside the reactor while both aluminum and ferrous iron remain in solution (>99%) and were washed out of the reactor vessel. The second sulfidogenic bioreactor was challenged with a synthetic AMD based on that from Mynydd Parys, North Wales. Throughout the test period, all the copper present in the feed liquor was precipitated (confirmed as copper sulfide) within the bioreactor, but none of the ferrous iron was present in the solids. Although the initial pH at which the bioreactor was operated (from pH 3.6 to 2.5) caused some coprecipitation of zinc with the copper, by progressively lowering the bioreactor pH and the concentration of the electron donor in the influent liquor, it was possible to precipitate >99% of the copper within the bioreactor as CuS and to maintain >99% of the zinc, iron, and aluminum in solution. Glycerol was used as energy and carbon source (electron donor) and the generalized reaction is [1]

4[C.sub.3][H.sub.8][O.sub.3] + 10[H.sup.+] + 7S[O.sub.4.sup.2-] + [Cu.sup.2+] + [Zn.sup.2+] + [Fe.sup.2+] [right arrow] 12C[O.sub.2] + 5[H.sub.2]S + CuS + ZnS + [Fe.sup.2+] + 16[H.sub.2]O (1)

This low sulfidogenic bioreactor system was also demonstrated to be effective at processing complex acidic water draining from the Mauriden mine in Sweden [18]. Throughout the test period, zinc was removed from the synthetic mine water as ZnS, from which the metal could be recovered, as in the case at the Budel zinc refinery in The Netherlands [24]. Recently, Falagan et al. [32] have operated this sulfidogenic reactor to mediate the precipitation of aluminum in acidic mine waters as hydroxysulfate minerals. Besides, this bioreactor was tested to demonstrate the recovery of over 99% of the copper present in a synthetic mine water drained from a copper mine in Carajas in the State of Para, Brazil [33]. The sulfidogenic system was also operated under different temperatures. Although there were large variations in rates of sulfate reduction measured at each temperature, the bioreactor operated effectively over a wide temperature range (30-45[degrees]C) which can have major advantages in some situations where temperatures are relatively high for example in mine sites located in northern Brazil and in other regions where high temperatures are observed. Therefore, there would be no requirements to have temperature control (heating or cooling) to preserve the integrity of the acidophilic SRB reactor [33]. The perceived advantages of this system are that there are simple engineering and relatively low operational cost. The system can be configured to optimize mine water remediation and metal recovery according to the nature of the mine water, which are the constraining factors in using active biological technologies to mitigate AMD.

Metalloids such as arsenic are a common constituent of mine waters. Battaglia-Brunet and colleagues [34] demonstrated that As (III) can be removed by precipitation as a sulfide. The results demonstrated the feasibility of continuous treatment of an acidic solution (pH 2.75-5) containing up to 100 mgAs(V). Under this approach, As(V) was reduced to As (III) directly or indirectly (via [H.sub.2]S) by the SRB and orpiment ([As.sub.2][S.sub.3]) generated within the bioreactor. In addition, this process was also observed to occur naturally in an acidic pit lake [31].

Recently, Florentino and colleagues [35] studied the microbiological suitability of using acidophilic sulfur reducing bacteria for metal recovery. These authors demonstrated that the Desulfurella strain TR1 was able to perform sulfur reduction to precipitate and recover metals such as copper from acidic waste water and mining water, without the need to neutralize the water before treatment. One drawback on the of use sulfur reducing microorganisms is that a suitable electron donor needs to be added for sulfate reduction. Even though sulfate is present in AMD, the additional cost of electron donors (such as glycerol) for sulfate reduction is higher than the cost of the combined addition of elemental sulfur and electron donors. Subsequently elemental sulfur as an electron acceptor can be more economically attractive for the application of biogenic sulfide technologies. On the other hand, cheaper electron donor such organic waste material may be used but their variable composition makes it less suitable for controlled high rate technologies. Besides, dead algal biomass can release organic products suitable to sustain the growth of SRB. Therefore, Diez-Ercilla et al. [31] have proposed that under controlled eutrophication it could be possible to decrease the metal concentrations in acidic mine pit lakes.

3. Microbiology in Remediating Acidic Mine Waters

Based on 16S rRNA sequence analysis, microorganisms that catalyze the dissimilatory reduction of sulfate to sulfide include representatives of five phylogenetic lineages of bacteria (Deltaproteobacteria, Clostridia, Nitrospirae, Thermodesulfobiaceae, and Thermodesulfobacteria) and two major subgroups (Crenarchaeota and Euryarchaeota) of the Archaea domain (Table 2 shows a summary of sulfidogenic microorganisms used for their main characteristics). SRB are highly diverse in terms of the range of organic compounds used as a carbon source and energy, though polymeric organic materials generally are not utilized directly by SRB [13]. In addition, some SRB can grow autotrophically using hydrogen as electron donor and fixing carbon dioxide, though others have requirement for organic carbon such as acetate, when growing on hydrogen. Besides, many SRB can also use electron acceptors other than sulfate for growth, such as sulfur, sulfite, thiosulfate, nitrate, arsenate, iron, or fumarate [78].

Most species of SRB that have been isolated from acidic mine waste such as Desulfosarcina, Desulfococcus, Desulfovibrio, and Desulfomonile are neutrophiles and are active at neutral pH [14,25]. Besides, for a long time the accepted view was that sulfate reducing activity was limited to slightly acidic to near neutral pH explained by the existence of microniches of elevated pH around the bacteria [21,31]. Attempts to isolate acidophilic or acid-tolerant strains of SRB (aSRB) have mostly been unsuccessful, until recently [79]. One of the reasons for the failure to isolate aSRB has been the use of organic acids such as lactate (carbon and energy source) which are toxic to many acidophiles. In acidic media, these compounds exist predominantly as nondissociated lipophilic molecules and, as such can transverse bacterial membranes, where they dissociate in the circumneutral internal cell cytoplasm, causing a disequilibrium and the influx of further undissociated acids, and acidification of the cytosol [80]. In contrast, glycerol can be used as carbon and energy source as it is uncharged at low pH. In addition, many SRB are incomplete substrate oxidizers, producing acetic acid as a product, enough to limit the growth of aSRB even at micromolar concentration. To circumvent this problem and for isolating aSRB, overlay plate can be used to remove acetic acid. This technique uses a double layer where the lower layer is inoculated with an active culture of Acidocella (Ac.) aromatica while the upper layer is not. Therefore, the heterotrophic acidophiles metabolize the small molecular weight compounds (such as acetic acid) that derive from acid hydrolysis of commonly used gelling agents such agar. The advantage of Ac. aromatica is its use of a limited range of organic donors and that it does not grow on yeast extract, glucose, glycerol, or many other small molecular weight organic compounds that are commonly metabolized by acidophilic heterotrophic microorganisms. Overlay plates are considered to be more versatile and efficient, particularly for isolating acidophilic sulfidogens from environmental samples, given that these microorganisms cannot completely metabolize the substrate [20]. Using this technique, aSRB and nonsulfidogens have been isolated from acidic sulfidogenic bioreactors. Two acidophilic sulfidogens (Desulfosporosinus (D.) acididurans and Peptococcaceae strain CEB3) and strain IR2 were all isolated from a low pH sulfidogenic bioreactor at different stages of operation, previously inoculated with an undefined microbial mat found at abandoned copper mine in Spain [3]. Although not yet fully characterized, Peptococcaceae CEB3 appears to be a more thermotolerant and acidophilic SRB that can oxidize glycerol to C[O.sub.2] [33].

In addition, D. acididurans grew successfully together with Ac. aromatica in a pH controlled bioreactor, showing an example of microbial syntrophy where this heterotrophic bacterium converted acetic acid into C[O.sub.2] and [H.sub.2] [17]. D. acididurans tolerates relatively high concentrations of aluminum and ferrous iron and can grow in a pH range of 3.8-7, with and optimum pH at 5.5. The temperature range for growth was 15-40[degrees]C with (optimum pH at 30[degrees]C), and it can use ferric iron nitrate, sulfate, elemental sulfur, and thiosulfate as electron acceptors [78]. D. acidophilus, the second acidophilic SRB validly described [26] isolated from a sediment sample collected in a decantation pond receiving acid mine effluent (pH ~ 3.0), showed high tolerance to NaCl. SRB belonging to the genus Desulfosporosinus are known to thrive in low pH environments together with members of the closely related genus Desulfitobacterium which have also been detected in reactors operating at low pH. Interestingly, Desulfitobacterium is a genus with members that can use sulfite as electron acceptor, but not sulfate. Some bacteria, phylogenetically related to sulfur reducers, have been also detected in AMD bioreactors as well in natural acidic conditions [29].

4. Natural Attenuation for the Design of AMD Remediation Strategies

Natural remediation of metal pollutants generally involves the catalytic action of microbial activities that can accelerate the precipitation reaction of soluble toxic compounds resulting in their accumulation in precipitates [81]. Such information from natural systems can be useful for the design of engineered systems. Natural attenuation of transition metals in AMD has been described, for example, at the Carnoules mine in France [81] and the Iberian Pyrite Belt (IPB) in Spain [10]. Rowe and colleagues [82] described in detail such process at a small site at the abandoned Cantareras copper mine, which is located in the Tharsis, mine district in the IPB. They reported that SRB other than Desulfosporosinus spp. were responsible for precipitating copper (as CuS) in a microbial mat found at the bottom layer and dissolved organic carbon (DOC) originated from photosynthetic and chemosynthetic primary producers serving as substrates for the aSRB. The pH of AMD obtained from this bottom layer was extremely acidic (pH < 3), and the dark grey coloration was due to the accumulation of copper sulfide, presumably as a result of biosulfidogenesis. No iron sulfides (e.g., hydrotroilite; FeS x n[H.sub.2]O) were detected, presumably due to the low pH of the mine water even at depth. Because the solubility product of CuS (log Ksp at 25[degrees]C is -35.9) is much lower than that of FeS (-18.8), this sulfide mineral precipitates in acidic waters whereas FeS does not.

Furthermore, Sanchez-Andrea and colleagues [83] described in detail the importance of sulfidogenic bacteria of the Tinto River sediments (Spain) and their role in attenuating acid mine drainage as an example of performing natural bioremediation. The results showed that, for attenuation in layers where sulfate reducing genera such as Desulfosporosinus and Desulfurella were abundant, pH was higher and redox potential and levels of dissolved metals and iron were lower. They suggested that sulfate reducers and the consequent precipitation of metals as sulfides biologically drive the attenuation of acid rock drainage. Lastly, the isolation and further understanding of anaerobic acidophiles in natural environments such as Cantareras and Rio Tinto have led to the proposal of new approaches to selectively precipitate toxic metals from AMD, turning a pollution problem into a potential source of metals [3, 83].

5. Concluding Remarks

Mining companies are increasing the extraction of mineral resources guided by a higher market demand, and also supported by productivity improvement resultant from advances on prospection and extraction technologies. Increased production consequently results in a higher generation of residues that is a global concern. The mining process has been significantly developed; however, pollution is still one of the main challenges of the mining industry and will require innovative management tools.

Given the fact that protecting aquatic and terrestrial ecosystems from pollutants generated from mine wastes is a major concern, new strategies must be employed such as the application of robust and empirically design bioreactors as part of an integrated system for remediation of acidic mine water and metal recovery. Using novel acidophilic and acid-tolerant sulfidogenic microorganisms that are the key components for bioremediation and knowledge about the microbial interactions that occur in extremely acidic, metal-rich environments will help in the development of new methods for bioremediation purposes.

https://doi.org/ 10.1155/2017/7256582

Conflicts of Interest

The authors declare that there are no conflicts of interest regarding the publication of this paper.

Acknowledgments

The authors acknowledge the financial support by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) to Jose O. Siqueira and Guilherme Oliveira and Vale and the sponsorship of SENAI/SESI Innovation Call. Ivan Nancucheo is supported by Fondecyt, Chile (no. 11150170).

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Ivan Nancucheo, (1) Jose A. P. Bitencourt, (2) Prafulla K. Sahoo, (2) Joner Oliveira Alves, (3) Jose O. Siqueira, (2) and Guilherme Oliveira (2)

(1) Facultad de IngenierOa y Tecnologia, Universidad San Sebastian, Lientur 1457, 4080871 ConcepciOn, Chile

(2) Instituto Tecnologico Vale, Rua Boaventura da Silva 955, 66055-090 Belem, PA, Brazil

(3) SENAI Innovation Institute for Mineral Technologies, Av. Com. Bras de Aguiar 548, 66035-405 Belem, PA, Brazil

Correspondence should be addressed to Ivan Nancucheo; inancucheo@gmail.com and Guilherme Oliveira; guilherme.oliveira@itv.org

Received 27 March 2017; Revised 31 July 2017; Accepted 23 August 2017; Published 3 October 2017

Academic Editor: Raluca M. Hlihor

Caption: Figure 1: Illustration of streams of acidic waters draining from active or abandoned mines and mine spoils. (a) AMD from a copper mine in the State of Para, Brazil, that has been remediated with limestone treatment, (b) acidic water released from abandoned underground metalliferous mine in the Republic of South Africa (reproduced from Akcil and Koldas [9]), (c) acidic mine water draining from an abandoned sulfur mine, northern Chile, (d) AMD discharge in the Lomero-Poyatos mine, Spain (reproduced from Espana et al. [10]), (e) acidic water draining from Coal mines, Jaintia Hills, and (f) AMD originated from mine tailings, Canada, (reproduced from Burtnyski [11]).

Caption: Figure 2: Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al. [12], Muyzer and Stams [13]).
Table 1: Summary of the various types of treatment for AMD (compiled
from Sahoo et al. [15], Gazea et al. [36], Trumm [37], Taylor et al.
[38], Roy Chowdhury et al. [39], Johnson and Hallberg [22], Skousen
[40], Skousen et al. [41], and Seervi et al. [42]).

System type              Applicability          Support materials

Biological
Aerobic wetland      Moderate acidity, net    Organic matter, soil,
(AeW)                alkaline mine drainage      limestone gravel

Anaerobic wetland    Net-acidic water with     Organic matter, such
(AnW)                  high Al, Fe and DO      as compost, sawdust,
                                                hay, and limestone
                                                     gravel,

Vertical flow        Net-acidic water with      Limestone, organic
wetland (VFW)          high Al, Fe and DO             matter

Sulfate reducing       Small flows or to      Organic substrate such
bioreactor (SRB)        situations, very         as hay, alfalfa,
                     acidic and metal rich       sawdust, paper,
                             water              woodchips, crushed
                                              limestone and compost
                                                    or manure

Pyrolusite           Moderate pH and where      Limestone, organic
limestone beds       majority of acidity is     substrate, aerobic
                         related to Mn            microorganism

Permeable reactive    Groundwater, low DO        Organic matter,
barriers (PRB)                                limestone, zero valent
                                                       iron

Iron-oxidizing            Acidic water        Fe-oxidizing bacteria
bioreactor                                         and archaea

Phytoremediation        Any AMD-impacted       Metal tolerant plant
                             sites                   species

Geochemical
Anoxic limestone     Acidic water with low      Limestone gravel,
drain (ALD)                Al, Fe, DO             compacted soil

Alkalinity                Acidic water           Organic matter,
producing system                                    limestone
(APS)

Open limestone       Required steep slopes,         Limestone
channel (OLC)        net-acidic water with
                       high Al, Fe and DO

Limestone leach            Low pH and               Limestone,
bed (LLB)               metal-free water

Steel-slag leach       Highly acidic and            Steel slag
bed (SLB)               metal-free water

Limestone              Sites that offer a       Crushed limestone
diversion wells      suitable topographical         aggregate
(LDW)                        fall

Limestone sand          Streamflow water       Sand-sized limestone

Low-pH Fe               Shallow channels      Limestone or sandstone
oxidation channels                                  aggregate

Sulfide                 Pit wall faces,         Inorganic coating:
passivation/            sulfide bearing       phosphate, silica, fly
microencapsulation     wastes rocks piles        ash, limestone;
                                              organic coating: humic
                                                  acid, lipids,
                                                   polyethylene
                                                    polyamine,
                                               alkoxysilanes, fatty
                                                acid, oxalic acid,
                                                     catechol

Electrochemical        Tailing/waste rock     Conductive steel mesh,
cover                                          cathode, metal anode

Physical
Dry cover            Sulfide bearing wastes     Fine-grained soil,
                           rock piles           organic materials,
                                                synthetic material
                                                (plastic liners),
                                                   vegetation

Wet cover                Sulfide wastes            Under water

Gas redox and          Underground mines          C[O.sub.2] and
displacement                                      C[H.sub.4] gas
system (GaRDS)

System type                Mechanisms               Limitation

Biological
Aerobic wetland      Oxidation, hydrolysis,      Required longer
(AeW)                    precipitation          detention time and
                                                huge surface area

Anaerobic wetland      Sulfate reduction,         Required long
(AnW)                  metal precipitate          residence time
                     as sulfides, microbial
                      generated alkalinity

Vertical flow            Sulfate and Fe         High capital cost,
wetland (VFW)           reduction, acid       potential for armoring
                         neutralization         and plugging with
                                                    hydroxides

Sulfate reducing       Microbial sulfate        High capital cost,
bioreactor (SRB)           reduction             extremely low pH
                                               severely impact the
                                                 efficiency of S
                                                reducing bacteria

Pyrolusite              Hydrolysis of Mn         Not suitable for
limestone beds                                    drainage which
                                              contains high Fe, high
                                                   maintenance

Permeable reactive     Sulfate reduction,
barriers (PRB)       sulfide precipitates,
                         neutralization

Iron-oxidizing            Fe oxidation
bioreactor

Phytoremediation        Phytoextraction       Success depends on the
                              and              proper selection of
                       phytostabilization           the metal-
                                              hyperaccumulator plant

Geochemical
Anoxic limestone           Limestone            Fe-oxide armoring
drain (ALD)            dissolution, raise        limestone limit
                       pH, precipitation         permeability and
                                                  cause plugging

Alkalinity             Anoxic condition,
producing system        neutralization,
(APS)                    precipitation

Open limestone             Limestone             Armoring or the
channel (OLC)             dissolution,            coating of the
                         neutralization          limestone, large
                                                amount is needed,
                                                  decreases the
                                              neutralizing capacity

Limestone leach      Limestone dissolution,      Armoring with Fe
bed (LLB)                neutralization             hydroxides

Steel-slag leach       Raise alkalinity,         Not suitable for
bed (SLB)                neutralization         metal-laden water

Limestone               Hydraulic force,        Required refilling
diversion wells         hydrolysis, and        with limestone every
(LDW)                    neutralization             2-4 weeks

Limestone sand         neutralizing acid            Coating of
                                                    limestone

Low-pH Fe                Fe oxidation,         It removes some Fe,
oxidation channels       adsorption and       but removal efficiency
                        coprecipitation            has not been
                                                    determined

Sulfide                 Prevent sulfide             Long-term
passivation/         oxidation by inorganic   effectiveness is still
microencapsulation    and organic coating      in question, organic
                                                coating expensive

Electrochemical          Reducing DO by        High capital cost of
cover                   electrochemical       anodes, no information
                            process             available on large
                                                scale application

Physical
Dry cover            Minimize oxidation by          Short term
                       physical barrier,          effectiveness
                         neutralization
                          precipitates

Wet cover               Disposing waste          Require rigorous
                       under water anoxic      engineering design,
                           conditions            high maintenance

Gas redox and             Gas mixtures          Its only feasible
displacement               physically            where partial or
system (GaRDS)            displace 02          complete flooding is
                                                  not feasible

Table 2: Isolated sulfidogenic microorganisms and their main
characteristics.

Microorganism            Temperature         pH (a)
                         ([degrees]C)

Thermocladium             45-82 (75)        2.6-5.9
modestius                                    (4.0)

Caldivirga                   70-90          2.3-6.4
maquilingensis                             (3.7-4.2)

Archaeoglobus                 nd              6.0
lithotrophicus

Archaeoglobus                 nd              6.9
veneficus

Archaeoglobus                 nd            4.5-7.5
profundus

Archaeoglobus             60-75 (70)        5.5-7.5
fulgidus                                     (6,0)

Thermodesulfatator        55-80 (70)        6.0-6.7
indicus                                      (6.25)

Thermo                    50-80 (75)        6.3-6.8
desulfobacterium                             (6.5)
hydrogeniphilum

Thermo                       41-83          6.0-8.0
desulfobacterium                             (7.0)
commune

Thermo                        nd            6.0-8.0
desulfobacterium                             (7.0)
thermophilum

Thermo                        75            4.5-7.0
desulfobacterium                             (7.0)
hveragerdense

Thermo desulfobium            69            4.0-6.0
narugense                                  (5.5-6.0)

Desulfotomaculum spp.         nd            2.3-5.5
(30 species)

Desulfosporosinus            10-37          6.1-7.5
meridiei

Desulfosporosinus        8-39 (32-35)       5.7-8.2
youngii                                    (7.0-7.3)

Desulfosporosinus            37-48          6.0-6.5
orientis

Desulfosporomusa             4-37           6.1-8.0
polytropa

Thermo desulfovibrio         41-83          6.0-8.0
yellowstonii                                 (7.0)

Thermo desulfovibrio          55            4.5-7.0
islandicus                                   (7.0)

Desulfohalobium spp.          nd            5.5-8.0
(6 species)                                (6.5-7.0)

Desulfocaldus                 58               nd
terraneus

Desulfomicrobium spp.        25-30             nd
(4 species)

Desulfonatronovibrio         37-40         9.0-10.2
hydrogenovorans                            (9.0-9.7)

Desulfonatronum spp.     20-45 (37-45)     8.0-10.0
(3 species)                                  (9.0)

Desulfovibrio spp.       25-44 (25-35)         nd
(47 species)

Desulfomonile spp.        30-30 (37)        6.5-7.8
(2 species)                                (6.8-7.0)

Syntrophobacteraceae         31-60          7.0-7.5
(8 genera)

Desulfobacterium              30            6.9-7.5
anilini

Desulfarculus baarsii        35-39            7.3

Desulfobacteraceae           10-40             nd
(12 genera)

Desulfosporosinus            25-40          3.6-5.2
acidophilus                                  (5.2)

Desulfosporosinus            15-40          3.8-7.0
acididurans                                  (5.5)

Microorganism            Carbon and electron source    Electron acceptor

Thermocladium            Glycogen, starch, proteins       Sulfur,
modestius                                              thiosulfate,
                                                        L-cysteine

Caldivirga                 Glycogen, beef extract         Sulfur,
maquilingensis            peptone, tryptone, yeast     thiosulfate,
                                  extract               L-cysteine

Archaeoglobus                     Acetate                Sulfate,
lithotrophicus                                          L-cysteine

Archaeoglobus           [H.sub.2], acetate, formate,     Sulfite,
veneficus                 pyruvate, yeast extract,      thiosulfate
                         citrate, lactate, starch,
                                  peptone

Archaeoglobus               [H.sub.2], acetate,          Sulfate,
profundus                 pyruvate, yeast extract,     thiosulfate,
                           lactate, meat extract,         sulfite
                          peptone, crude oil with
                             acetate [H.sub.2],
                            C[O.sub.2], formate,
                            formamide, D(-)-and

Archaeoglobus              L(+)-lactate, glucose,        Sulfate,
fulgidus                  starch, calamine acids,      thiosulfate,
                         peptone, gelatin, casein,        sulfite
                        meat extract, yeast extract

Thermodesulfatator         [H.sub.2], C[O.sub.2];         Sulfate
indicus                   stimulated by methanol,
                        monomethylamine, glutamate,
                        peptone, fumarate, tryptone,
                            isobutyrate, 3-CH 3
                        butyrate, ethanol, propanol
                        and low amounts of acetate.

Thermo                     [H.sub.2], C[O.sub.2];         Sulfate
desulfobacterium           stimulated by acetate,
hydrogeniphilum         fumarate, 3-methylbutyrate,
                         glutamate, yeast extract,
                            peptone or tryptone

Thermo                     [H.sub.2], C[O.sub.2],        Sulfate,
desulfobacterium             pyruvate, lactate          thiosulfate
commune

Thermo                     [H.sub.2], C[O.sub.2],        Sulfate,
desulfobacterium             pyruvate, lactate          thiosulfate
thermophilum

Thermo                  [H.sub.2], pyruvate, lactate     Sulfate,
desulfobacterium                                          sulfite
hveragerdense

Thermo desulfobium         [H.sub.2], C[O.sub.2]         Sulfate,
narugense                                                nitrate,
                                                        thiosulfate

Desulfotomaculum spp.      [H.sub.2], C[O.sub.2],        Sulfide,
(30 species)               formate, some (organic         sulfur,
                             acids; lipids; or         thiosulfate,
                         monoaromatic hydrocarbons)    Acetate, some
                                                       (Fe (III), Mn
                                                       (IV), U (VI) or
                                                         Cr (VI))

Desulfosporosinus          [H.sub.2], C[O.sub.2],      Sulfate, some
meridiei                  acetate, some (lactate,        (nitrate)
                             pyruvate, ethanol)

Desulfosporosinus       Beef extract, yeast extract,     Fumarate,
youngii                 formate, succinate, lactate,     sulfate,
                           pyruvate, ethanol and         sulfite,
                                  toluene               thiosulfate

Desulfosporosinus          [H.sub.2], C[O.sub.2],        Sulfate,
orientis                formate, lactate, pyruvate,      sulfite,
                        malate, fumarate, succinate,   thiosulfate,
                        methanol, ethanol, propanol,      sulfur
                        butanol, butyrate, valerate,
                                 palmitate

Desulfosporomusa           [H.sub.2], C[O.sub.2],        Sulfate,
polytropa               formate, lactate, butyrate,    Fe[(OH).sub.3]
                         several alcohols, organic
                         acids, carbohydrates, some
                           amino acids, choline,
                                  betaine

Thermo desulfovibrio       [H.sub.2], C[O.sub.2],        Sulfate,
yellowstonii             acetate, formate, lactate,    thiosulfate,
                                  pyruvate                sulfite

Thermo desulfovibrio        [H.sub.2], pyruvate,         Sulfate,
islandicus                    lactate, formate            nitrate

Desulfohalobium spp.    [H.sub.2], lactate, ethanol,      Sulfite
(6 species)                       acetate

Desulfocaldus           [H.sub.2], C[O.sub.2], amino     Cystine,
terraneus                   acids, proteinaceous       sulfur, sulfate
                           substrates and organic
                         acids, producing ethanol,
                            acetate, propionate,
                                isovalerate/
                             2-methylbutyrate,

Desulfomicrobium spp.       [H.sub.2], lactate,          Sulfate,
(4 species)              pyruvate, Ethanol, formate    sulfoxyanions

Desulfonatronovibrio         [H.sub.2], formate          Sulfate,
hydrogenovorans                                          sulfite,
                                                        thiosulfate

Desulfonatronum spp.     [H.sub.2], formate, Yeast       Sulfate,
(3 species)              extract, ethanol, lactate       sulfite,
                                                        thiosulfate

Desulfovibrio spp.         [H.sub.2], C[O.sub.2],        Sulfate,
(47 species)                 acetate, lactate,            nitrate
                               carbohydrates,

Desulfomonile spp.         [H.sub.2], C[O.sub.2],        Sulfate,
(2 species)             benzoate, pyruvate, organic      sulfite,
                              carbon, halogens         thiosulfate,
                                                        sulfur, Fe
                                                          (III),
                                                         Nitrate,
                                                          U (VI)

Syntrophobacteraceae       [H.sub.2], C[O.sub.2],        Sulfate,
(8 genera)               acetate, formate, lactate,      sulfite,
                                 pyruvate,              thiosulfate

Desulfobacterium           [H.sub.2], C[O.sub.2],        Sulfate,
anilini                    butyrate, higher fatty        sulfite,
                        acids, other organic acids,     thiosulfate
                                  alcohols

Desulfarculus baarsii      [H.sub.2], C[O.sub.2],        Sulfate,
                           butyrate, higher fatty        sulfite,
                        acids, other organic acids,     thiosulfate
                                  alcohols

Desulfobacteraceae      [H.sub.2], C[O.sub.2], Long-     Sulfate,
(12 genera)             chain fatty acids, Alcohols,     sulfite,
                         Polar aromatic compounds,      thiosulfate
                           and in some cases even
                            Aliphatic, aromatic
                                hydrocarbons

Desulfosporosinus           [H.sub.2], lactate,           Sulfate
acidophilus             pyruvate, glycerol, glucose
                                and fructose

Desulfosporosinus       [H.sub.2], formate, lactate,   Ferric iron,
acididurans             butyrate, fumarate, malate,      nitrate,
                            pyruvate, glycerol,          sulfate,
                          methanol, ethanol, yeast       elemental
                         extract, xylose, glucose,        sulfur,
                                  fructose              thiosulfate

Microorganism                        Source                Reference

Thermocladium           Hot springs (water, mud), Japan     [43-45]
modestius

Caldivirga               Hot springs (water, solfataric       [46]
maquilingensis              soil mud), Mt Maquiling,
                                  Philippines

Archaeoglobus                         nd                    [47, 48]
lithotrophicus

Archaeoglobus           Walls of active black smoker at       [44]
veneficus                    middle Atlantic Ridge

Archaeoglobus           Deep sea hydrothermal system off    [49, 50]
profundus                       Guaymas, Mexico

Archaeoglobus             Marine hydrothermal system,       [49, 51]
fulgidus                         Nerone, Italy

Thermodesulfatator        Marine hydrothermal system,         [52]
indicus                       Central Indian Ridge

Thermo                    Marine hydrothermal system,         [53]
desulfobacterium                 Guaymas Basin
hydrogeniphilum

Thermo                  Hot springs (water, sediment and    [54, 55]
desulfobacterium        mats) Yellowstone National Park,
commune                               USA

Thermo                                 nd                     [55]
desulfobacterium
thermophilum

Thermo                   Hot springs (microbial mats),        [56]
desulfobacterium                    Iceland
hveragerdense

Thermo desulfobium       Hot springs (microbial mats),        [57]
narugense                            Japan

Desulfotomaculum spp.    Subsurface environments, rice      [58-62]
(30 species)               fields, mines, oil spills

Desulfosporosinus        Groundwater contaminated with        [63]
meridiei                      polycyclic aromatic
                         hydrocarbons, in Swan Coastal
                                Plain, Australia

Desulfosporosinus        Artificial wetland (sediment)        [64]
youngii

Desulfosporosinus                      nd                     [65]
orientis

Desulfosporomusa         Oligotrophic lake (sediment),        [66]
polytropa                            German

Thermo desulfovibrio    Hot springs (water, sediment and      [67]
yellowstonii            mats) Yellowstone National Park,
                                      USA

Thermo desulfovibrio     Bioreactor inoculated with hot       [56]
islandicus              springs (microbial mats) sample,
                                    Iceland

Desulfohalobium spp.        hypersaline environments        [68, 69]
(6 species)

Desulfocaldus              Sea oil facilities, Alaksa         [70]
terraneus

Desulfomicrobium spp.   Anaerobic sediments (Freshwater,    [54, 69]
(4 species)               brackish, marine), anaerobic
                         strata or overlying water, and
                        in saturated mineral or organic
                                   deposits.

Desulfonatronovibrio    Alkaline soda lakes (anaerobic)       [71]
hydrogenovorans

Desulfonatronum spp.    Alkaline soda lakes (anaerobic)       [72]
(3 species)

Desulfovibrio spp.                     nd                     [73]
(47 species)

Desulfomonile spp.                   Sludge                   [74]
(2 species)

Syntrophobacteraceae       Sewage sludge, freshwater,       [73, 75]
(8 genera)                 brackish, marine sediment,
                         marine hydrothermal vents, hot
                                spring sediments

Desulfobacterium          Freshwater, Brackish water,         [76]
anilini                     Marine, and Haloalkaline
                                    habitats

Desulfarculus baarsii     Freshwater, Brackish water,         [76]
                            Marine, and Haloalkaline
                                    habitats

Desulfobacteraceae        Freshwater, Brackish water,         [77]
(12 genera)                 Marine, and Haloalkaline
                                    habitats

Desulfosporosinus        Sediment from an acid effluent       [26]
acidophilus                           pond

Desulfosporosinus        White river draining from the        [78]
acididurans             Soufriere hills in Monserrat (pH
                                      3.2)

aValues closed by parenthesis are considered optimal pH;
nd: not informed by consulted reference.
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Author:Nancucheo, Ivan; Bitencourt, Jose A.P.; Sahoo, Prafulla K.; Alves, Joner Oliveira; Siqueira, Jose O.
Publication:BioMed Research International
Article Type:Report
Geographic Code:3BRAZ
Date:Jan 1, 2017
Words:8618
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