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Review

Extremely Acidic Eukaryotic (Micro) Organisms: Life in Acid Mine Drainage Polluted Environments—Mini-Review

by
Ana Teresa Luís
1,2,*,
Francisco Córdoba
3,
Catarina Antunes
1,
Raul Loayza-Muro
4,
José Antonio Grande
2,5,
Bruna Silva
1,
Jesus Diaz-Curiel
6 and
Eduardo Ferreira da Silva
1
1
GeoBioTec Research Unit, Department of Geosciences, University of Aveiro, 3810-193 Aveiro, Portugal
2
Department of Water, Mining and Environment, Scientific and Technological Center of Huelva, University of Huelva, 21007 Huelva, Spain
3
Department of Integrated Sciences, Faculty of Experimental Sciences, University of Huelva, 21007 Huelva, Spain
4
Laboratório de Ecotoxicología, Facultad de Ciencias y Filosofiia, Universidad Peruana Cayetano Heredia, Av. Honorio Delgado 430, Lima 15102, Peru
5
Sustainable Mining Engineering Research Group, Department of Mining, Mechanic, Energetic and Construction Engineering, Higher Technical School of Engineering, University of Huelva, 21007 Huelva, Spain
6
Escuela Técnica Superior Ingenieros de Minas, Rios Rosas 21, 28003 Madrid, Spain
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2022, 19(1), 376; https://doi.org/10.3390/ijerph19010376
Submission received: 7 November 2021 / Revised: 20 December 2021 / Accepted: 28 December 2021 / Published: 30 December 2021

Abstract

:
Acid Mine Drainage (AMD) results from sulfide oxidation, which incorporates hydrogen ions, sulfate, and metals/metalloids into the aquatic environment, allowing fixation, bioaccumulation and biomagnification of pollutants in the aquatic food chain. Acidic leachates from waste rock dams from pyritic and (to a lesser extent) coal mining are the main foci of Acid Mine Drainage (AMD) production. When AMD is incorporated into rivers, notable changes in water hydro-geochemistry and biota are observed. There is a high interest in the biodiversity of this type of extreme environments for several reasons. Studies indicate that extreme acid environments may reflect early Earth conditions, and are thus, suitable for astrobiological experiments as acidophilic microorganisms survive on the sulfates and iron oxides in AMD-contaminated waters/sediments, an analogous environment to Mars; other reasons are related to the biotechnological potential of extremophiles. In addition, AMD is responsible for decreasing the diversity and abundance of different taxa, as well as for selecting the most well-adapted species to these toxic conditions. Acidophilic and acidotolerant eukaryotic microorganisms are mostly composed by algae (diatoms and unicellular and filamentous algae), protozoa, fungi and fungi-like protists, and unsegmented pseudocoelomata animals such as Rotifera and micro-macroinvertebrates. In this work, a literature review summarizing the most recent studies on eukaryotic organisms and micro-organisms in Acid Mine Drainage-affected environments is elaborated.

1. Introduction

Acid Mine Drainage (AMD) is one of the main hydrological and geochemical problems derived from anthropogenic influence on the geosphere, which affects many countries with intense mining activities [1,2].
AMD is produced when sulfide-bearing materials suffer direct oxidation, which is then spread by the indirect oxidation of ferric ions. Chemical oxidation processes can be biologically “catalyzed” by some bacteria [3]. Along with pyrite reactions [4], many other associated reactions can be produced by the remaining metals which, in the form of sulfur, appear along with pyrite. As a result of these reactions and due to the very acidic waters, numerous soluble contaminating elements, are stored on pyrite surfaces and transported by inland streams. This process is affected by numerous factors including the type, abundance and distribution of sulfides and minerals with neutralizing capacity as well as oxygen concentration, humidity, temperature, exposed pyrite surface area, types of bacteria, etc. [5]. When transported to inland streams, AMD can contaminate surfaces, ground sediments and soils, as a consequence of its very low pH as well as by a high content of sulfates and heavy metals in water and a high metallic content in sediments [6,7].
Both active and abandoned mines are major sources of AMD [8], which is not only generated in sulfide mines, e.g., the Iberian Pyrite Belt, but also to a lesser extent in coal mines, e.g., the Northern Appalachian Coalfield. In the nearest streams, this could result in species loss and significant structural changes to freshwater organisms [9] and loss of species richness [10] and macroinvertebrate abundance [11].
AMD is responsible for the disappearance of several species of algae and diatoms, such as the Cyclotella and Fragilaria genera [12], and for loss of diatomic diversity in impacted sites [13] dominated by typical species of acidic waters [14,15], for example Pinnularia acoricola and Eunotia exigua. At the community level, the highest metal concentrations (along with pH < 3 and high Eh potential) implicate the lowest diversity [16], while at the individual level changes in frustule morphology are observed [15,17]. With respect to filamentous green algae, acidophilic species of the Mougeotia and Klebsormidium genus are abundant in AMD streams [18,19], as are other unicellular algae such as Chlamydomonas or Euglena, which may be very abundant in such environment, along with Protozoa and some multicellular protists. In relation to the impact of AMD on macroinvertebrates, there is evidence of a high impact on density and taxa richness [20] as well as a change in the shape of the food pyramid [21]. In places affected by AMD, species of macroinvertebrates can be found, which are tolerant to these environments, for example, chironomids; on the other hand, the most sensitive species, for example, flies, are excluded as a result of the low pH and high concentrations of metals [22].
Therefore, the main objective of this review is to summarize the scientific literature related to AMD production and its effects on eukaryotic organisms thriving in the water or sediments of streams and rivers, focusing on the following subjects: Acid Mine Drainage and the impact of AMD on algae, Protozoa, fungi and yeast as well as on micro- and macroinvertebrates.

2. Acid Mine Drainage

Around the world, there are mines that have been abandoned and pose a long-term threat to aquatic ecosystems due to the continuous or intermittent flow of acidic drainage water containing high concentrations of various heavy metals [23]. AMD is predominantly caused when sulfide minerals present in metallic ores, coal beds, or the strata overlying and underlying the coal are exposed to weathering causing oxidation [24,25], which later on is propagated through indirect oxidation by ferric ions produced mainly by chemolithotrophic bacteria [26,27]. Chemical reactions such as hydrolysis and oxidation can transform sulfide minerals into sulfuric acid, decreasing the pH of water at active or abandoned mine sites [28]. Mine facilities, tailings and waste rocks left in these sites are major contamination sources of AMD (Okabayashi et al., 2005). Metal-bearing minerals are abundant in finely-ground mine tailings or fine particles of by-product from mining activities [28]. Tailings with 5% pyrite and arsenopyrite are high enough to produce AMD [29].
In mine waste materials containing sulfide minerals (pyrite, galena, sphalerite and arsenopyrite), AMD is produced due to natural oxidation reactions involving the exposed sulfides, air, water, and soil microorganisms [30]. An AMD with high potential of reactivity promotes the dissolution of the bedrock, mobilising heavy metals that will change the stream water quality and the groundwater system [30]. The Iberian Pyrite Belt (IPB) has one of the world’s largest concentrations of sulfide deposits, running from Lousal, Portugal to Aznalcóllar, Spain [31]. In Andalusia, southwestern Spain), thousands of years of mining in the IPB have resulted in enormous metal wastes [32] that severely degrade the environment [4,33]. The IPB zone has massive sulfide reserves of around 1700 Mt that are distributed across more than 50 massive sulfide deposits [34]. The Spanish side of the IPB has 88 mines [4,35], most generating AMD, in an area with more than 4000 ha of waste rock and tailings [31]. The Odiel River Basin is a well-known fluvial system in a catastrophic ecological situation due to AMD affecting 37% of its drainage network length [33]. The Odiel River is affected from its upper section to the Huelva estuary. In fact, the Ria de Huelva is one of the most heavily metal-contaminated estuaries in the world as a result of AMD from the IPB mines [36].
Coal originates in the burial of organic matter in swamps, and pyrite is also formed in these environments. One of the major sources of water pollution in and around both active and abandoned coal mines is AMD [37]. This becomes even more severe with marine influence in coal deposits, due to the presence of additional framboidal pyrite [38]. Pyrite in coal oxidizes when exposed to air and water, producing Fe (III) and H2SO4 [39]. Fe (II) ions are oxidized, forming Fe oxide and producing H+ ions, lowering the pH of the water and making it corrosive [39]. The Northern Appalachian Coalfield in the eastern US has a historical legacy of coal mining [40] and represents one third of the abandoned mine-related problems in the country [41]. The Witbank Coalfield, located in the headwaters of the Olifants River in Mpumalanga Province, South Africa is dominated by past and present coal mining, and AMD from these mines results in both a low pH and high total dissolved solids in this river, which then flows through areas of intensive agriculture [42].
Small-scale gradients of pH and metals within such systems can be useful as field model systems to study the biological effects of acid and metal pollution [23]. The information gained is very important because it might be useful to develop bioassessment methods. The mitigation of not only the physical, chemical and biological, but also the socioeconomic impacts of AMD is one of the major challenges faced by the mining industry worldwide, and many countries have been investing in the development of efficient treatment methods for wastewater from mining.

3. Eukaryotic Organisms in AMD-Polluted Extreme Environments

3.1. Diatoms

The diatoms are one of the most effective ecological indicators [14,15,16,17,20,31,43] in AMD-contaminated environments, due to their ubiquity in aquatic habitats [44] and high effectiveness for assessing aquatic health [45]. Thus, they are good indicators of pH changes and very abundant in environments impacted by low pH [46]. Diatoms respond to chemical stress at community and individual levels. At a community level, the highest metal concentrations (i.e., Fe: 6 g/L, Zn 1.7 g/L, Cu 347 mg/L, Cd 3.5 mg/L, Ni 3 mg/L, Mn 0.3 mg/L) and low pH (i.e., 2.0-4.5) result in low diatom diversity (Shannon–Winer diversity index < 2.2 on a 5-point scale) [14,15,16], and the species change to more acidophilic or acidobiontic varieties better-prepared to endure these harsh conditions. This decrease in species richness has been observed in many works [13,15,16,20,31,43,47,48], and is more prominent for diatoms than for macroinvertebrates [23].
The dominant and typical species in acidic waters are Pinnularia acoricola, Pinnularia acidophila, Pinnularia aljustrelica, Eunotia exigua (Figure 1) and Nitzschia hantzschiana [13,14,15,31]. The three Pinnularia species found in the impacted sites; P. aljustrelica is the most abundant due to its capacity to survive a very low pH, i.e., 1.9–4.2 [15,49]. Achnanthidium minutissimum is a difficult species, able to tolerate different environmental conditions and usually the only Achnanthidium species reported in AMD polluted streams [50], being abundant in a wide variety of habitats and environmental conditions [51]. However, A. minutissimum can also appear in unimpacted sites, being the dominant species in less-impacted sites [14]. It is considered to generally be the first taxon to colonize different habitats (e.g., rocks, sediments) [52], and has the ability to invade open areas following changes in environmental conditions [53].
Some of the other ‘true inhabitants of highly acidic waters’ [20] include Nitzschia capitellata, Nitzschia subcapitellata and Pinnularia subcapitata [54]. In sites with pH below 4.5, Eunotia exigua, Nitzschia cf. thermalis, Pinnularia acidophila, Pinnularia acoricola, Pinnularia subcapitata and Pinnularia aljustrelica can appear [31]. This fact is supported by other authors who have found these species under similar environmental conditions [16,46,49,55].The Pinnularia and Achnanthes genera (especially Pinnularia) are often the most frequent in impaired sites [56], implying that these genera are tolerant to AMD [22,57] and making them particularly useful as bioindicators of low pH [58].
In the Lousal and Aljustrel mining areas located in the Portuguese part of the IPB, the species found (in descending order of dominance) include Brachysira vitrea, Eunotia exigua and Pinnularia c.f. acidophila (Figure 1). In the Aljustrel mining area, with sulfated high to extreme metal/metalloid concentrations and low pH waters, P. aljustrelica, E. exigua (Figure 1) and Nitzschia aff. hantzschiana are the dominant species [15]. However, E. exigua is an acidobiontic taxon, and is the most widespread species in AMD-contaminated streams such as the Río Tinto [16,31,59,60,61] and the Aljustrel streams [14,15,17,55] (Table 1).
Metals lower biodiversity in several important ways. Diatoms have developed mechanisms such as biotransformation, biomineralization, bioaccumulation and biosorption to cope with heavy metal toxicity [62]; nevertheless, pollution-tolerant and pollution-sensitive diatoms have different responses to metal pollution [63]. When exposed to metals, community size can be impaired through reduction of cell number, selection for smaller species, and decrease in cell size within a given species [17,64,65,66]; diatom growth can be delayed or inhibited, therefore reducing diatom biomass [67] and decreasing the rates of survival and growth. Diatoms are able to sequestrate large quantities of metals from waters [68]. The most common taxa presenting abnormal valves due to metals/pH or metal-pH combination are Fragilaria capucina [69], Fragilaria rumpens and A. minutissimum [69] and Eunotia exigua [15].
Thus, the observed differences in diatom community structure result from the combined action of low pH and highly soluble heavy metals [54,70]. Diatoms can also be susceptible at the individual level showing changes in frustule morphology [17]. The resistance of A. minutissimum to metals is still under discussion, with contradictory results in the literature. It is usually considered an indicator of metal pollution [71], although it could also indicate good general water quality [72].

3.2. Unicellular and Filamentous Green Algae

Although AMD environments are not appetizing to many species, some genera of unicellular and filamentous green algae can adapt and survive; among these are species from the unicellular genera Chlamydomonas, Chlorella, Cyanidium, Dunaliella, Euglena [73,74] and from the filamentous genera Klesormidium, Microspora, Mougeotia, Ulothrix, Stigeoclomium, Zygnema and Microthammion. The genera Mougeotia, Ulothrix, Chlamydomonas, Chara and Nitella are typical of these environments; however, they may not be as abundant as diatoms [75,76,77].
Cyanidium is a red algae genus, or rhodophite. It has been observed at pH 1.2–1.8 in waters close to the Rio Tinto mines. Dunaliella, Chlamydomonas and Chlorella are unicellular green algae from the Chlorophyceae family. Both Chlamydomonas and Dunaliella may be motile, with the presence of flagella. Curiously, Dunaliella has no cell wall. Chlamydomonas acidophila is the most abundant species in acid waters, showing a high tolerance to copper and other heavy metals [78,79] Euglena mutabilis is abundant in shallow waters and easily forms large tufts that can look like filamentous algae. Oxygen bubbles are frequently observed in some places where Euglena thrives. All microalgae contribute to enhanced oxygen production (up to 200% saturation) and organic carbon, which reduces the oligotrophic conditions of AMD-polluted waters and increases the oxidative activity of aerobic chemoautolithotrophic bacteria and heterotrophic bacteria [80].
The acidophilic species of the Mougeotia genus can survive in the AMD environment, in waters with a pH of 2.9–4.1 [18]. The abundance and distribution of Klebsormidium sp. in AMD affected waters makes this species a good ecological indicator of this type of contamination, and Klebsormidium-dominated algal mats are particularly good indicators of high iron concentrations in water [81]. Additionally, Mougeotia, can be abundant in AMD streams [19,81], possibly because of strong competition for low DIC (dissolved inorganic carbon) in acidic environments [82]. The genus Klebsormidium is known to be metal resistant, and is been related with metal-rich polluted waters. K. subtile, K. rivulare, K. flaccidium and K. acidophilum are other species related with AMD-contaminated environments [19,51,77]. Chlamydomonas sp. shows tolerance in a wide range of physical and chemical conditions in a lake contaminated by AMD, being consistently present [83].
The Microspora genus is very abundant in mines with high levels of metal pollution, and is considered by [84] as a good bioindicator. The Ulothrix genus, on the other hand, is predominant in biofilms from AMD-contaminated sites, having a great capacity to recover Cu and As.
Several of the microorganisms described above are represented in Figure 2.

3.3. Protozoa, Fungi and Yeasts in AMD-Polluted Waters

In AMD-polluted waters, several groups of heterotrophic protists may be observed. The main groups include protozoa: ciliates such as Urotricha and Oxytricha, flagellates such as Bodo and Ochromonas, amoebas such as Actinophyrs and Naegleria, etc., and heliozoa. In acidic waters, these genera play an essential role in nutrient recycling in spite of their oligotrophic characteristics [85].
Fungi are more acidotolerant than acidophilic, although some filamentous fungi, such as as Acontium, Cephalosporium and the yeast Trichosporon, are able to growth up to pH 0 [85]. In [86], a wide variety of filamentous fungi are described, including Scytalidium, Bahusakala, Phoma, Heteroconium, and even Penicillium and diverse ascomycetes and zygomycetes. In addition to their role as components of an acidic river ecosystem, fungi play an important role in the biomineralization of iron and the accumulation of intracellular deposits of toxic metals [87,88]; see examples below (Figure 3).

3.4. The Impact of AMD on Micro-Macroinvertebrates

AMD represents an extremely stressful and long-term source of pollution due to the anthropogenic disturbance of geological layers. Characteristic low pH and high metal concentrations have been highlighted as the main drivers of micro- (<500 µm length) and macroinvertebrate (>500 µm, length) diversity and community composition in streams affected by AMD [11,20,90], while acidification may induce an increase in the bioaccumulation of metals in insect larvae with consequences for the food chain and aquatic fauna [91]. The main microinvertebrates observed in these waters are from phylum Rotifera, considered pseudocoelomate “animals” [89,92,93].
Variation in macroinvertebrate assemblages and densities has also shown a strong relationship with other water chemistry variables in addition to metals, such as dissolved oxygen and conductivity, inducing a clear shift from metal-sensitive (e.g., Ephemeroptera, Plecoptera and Trichoptera) to metal-tolerant (Diptera, Coleoptera and Collembolla) taxa [94,95,96,97,98]. The order Ephemeroptera is a group highly sensitive to metals; however, some species, such as Baetis rhodani and Caenis cf. luctuosa, exhibit tolerance to these contaminants [99,100].
Among metal-tolerant taxa, Chironomidae (Diptera) assemblages often represent a significant portion of the sediment-dwelling fauna at deteriorated sites, and are hence especially useful as bioindicators and for sediment quality assessment [101,102,103]. Chironomid species have been found in acidified metal-polluted temperate [103,104], tropical and high-altitude streams [96,105] as well as unpolluted glacier-elevated water streams [106]. Species of Chironomus may have physiological adaptations responsible for such tolerance, as those species coming from contaminated points are able to adjust their body metals concentration when compared to other species [97]. Chironomids from elevated altitudes and metal-contaminated sites contain more melanin than species from reference sites at lower altitudes [107]. This fact highlights the importance of melanin in chironomids as a UV-B radiation protector and metal chelator. In addition, genetic adaptation has been found to be a metal tolerance tool in Chironomus species from highly contaminated environments [108,109,110]. In [97], it was found that only one tolerant strain of chironomids was able to survive in the most metal-rich points in the Andes, which indicates that tolerance could have been developed as an answer to naturally existing acid and metal-rich environments, and thus may have preceded human-influenced alterations due to mining activity. The adaptation of this unique chironomid species to very large metal values may have come with direct costs, as represented by smaller specimens in comparison to those from species in similar reference streams, in the form of reallocation of energy towards resistance tools such as metal-binding metallothioneins. Melanin production or cuticle sclerotization in chironomids [107] may convey a trade-off evidenced as reduced growth [111].
Chironomids are used as potential biomonitors at different organizational levels in order to indicate the biological effects of metal pollution. At the cytological level, genotoxic damage produces micronuclei in the structure of salivary gland chromosomes of larvae of Chironomus acidophilus in a river with high concentrations of Cu, Fe, Mn and Zn [112]. At the organism level, cause–effect relationships between morphological abnormalities such as deformities of the mouthparts and metal-rich stream sediments have been demonstrated in both, laboratory [113,114] and field [115,116,117,118]. This was the case for Chironomus tentans larvae, where fused, split, missing, extra and abnormally-shaped teeth on the mandible were associated with different metal levels [119].
Most taxa within the Chironomidae (Figure 4) are collector-filterers and collector-gatherers while a few (e.g., Cryptochironomus sp., Endochironomus spp., Glyptotendipes spp., Polypedilum spp. and Chironomus spp.) are predatory on oligochaetes in AMD-contaminated sites [100], which indicates that these group show different ecological response patterns to AMD [103]. Moreover, shredder-climbers can be the dominant group at impacted sites and could be more adaptive in AMD affected streams than other groups, as Fe-loving bacteria growing on leaves coated with Fe hydroxide become an option as a food resource [120].
In general, stress conditions may benefit the increase of secondary consumers, changing, considerably, the food chain shape [103]. This phenomenon has been described for macroinvertebrates from AMD impacted streams [100] and implies major shifts in resource utilisation, possibly reducing the number of trophic levels and consequently simplifying the food web. While these ecological processes still need further analysis in AMD environments, they can explain the use of Tanypodinae as bioindicators. This is because AMD leads to a significant change in the community structure of chironomid larvae. On the other hand, the taxonomic richness within the Chironomidae remains stable in acid mine drainage because the loss of sensitive species is compensated for by tolerant species [100]. Sites with severe AMD have a significant decrease in abundance of stationary collector-filterer prey (primarily Hydropsychidae, caddisflies that occur in high densities), showing that both the diversity and abundance of macroinvertebrate prey decreases as AMD impact increases [121]. Thus, AMD contamination sites can have high biodiversity because of high tolerant species richness, as well as considerable variability in metal tolerance among macroinvertebrate taxa and species (Byrne et al., 2012). When compared to reference sites, the functional diversity of macroinvertebrates is lessened, and their functional structure is much simpler [122].

4. Conclusions

This research study sought to put in evidence the importance of extremophile organisms in AMD-affected environments. This mini-review summarizes the eukaryotic groups inhabiting these environments. AMD affects the organisms inhabiting the water and sediment substrates, which are subjected to high concentrations of metals and sulfates along with low pH. AMD-provoked changes in the ecological environment at both the community level and the individual level are responsible for species disappearance and the loss of diversity and abundance. Only those organisms capable of developing adaptation mechanisms to these extreme conditions survive and succeed [123].
Further research in this area is crucial in order to minimize the evident environmental consequences of mining exploration through the centuries, with bio- and eco-friendly solutions having particular appeal.
New applications using these extreme organisms in biotechnology and astrobiology studies are the main reason for their study at present. An example is a recent study of the Tintillo River [124], contaminated by Río Tinto in Huelva, Spain, where bacterial filaments and diatoms are capable of forming iron stromatolites as laminated sedimentar structures. Furthermore, the active biosorption and bioleaching of sulfur are suggested by the black and white coloration of microbial filaments inside these stromatolites. AMD systems are hazardous to physical, chemical, and biological agents; however, they also provide valuable biogeochemical information which can aid in inferring past geochemical conditions on Earth, and perhaps even other planets such as Mars.

Author Contributions

Conceptualization, A.T.L.; Investigation, A.T.L., C.A., F.C., R.L.-M.; supervision, E.F.d.S.; resources, J.D.-C.; writing—original draft preparation, A.T.L., C.A.; writing—review and editing, B.S., F.C., J.A.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

The authors are grateful to the Department of Geosciences of the University of Aveiro, Portugal, where this work was developed. We also thank the Lic. Karen Velásquez Rodríguez and Fiorella La Matta Romero for the macroinvertebrate microphotographs. All the other photos are original and never published before. AT Luís is funded by national funds (OE) through FCT—Fundação para a Ciência e a Tecnologia, I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of 29 August, changed by Law 57/2017, of 19 July.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kleinmann, R.L.P.; Crerar, D.A.; Pacelli, R.R. Biogeochemistry of acid mine drainage and a method to control acid formation. Miner. Eng. 1981, 33, 300–305. [Google Scholar]
  2. Gray, N.F. Environmental impact and remediation of acid-mine drainage: A management problem. Environ. Geol. 1997, 30, 62–71. [Google Scholar] [CrossRef]
  3. Nicholson, R.V. Iron-sulfide oxidation mechanism. In Chemical Weathering Rates of Silicate Minerals; White, A.F., Brantley, R.J., Eds.; Mineralogical Society of America: Chantilly, VA, USA, 1994; Volume 31, pp. 173–225. [Google Scholar]
  4. Grande, J.A. Drenaje Ácido de Mina en la Faja Pirítica Ibérica: Técnicas de estudio e inventario de explotaciones. Serv. Publ. 2016, 1, 345. [Google Scholar]
  5. Dogan, P.A. Characterization of mine waste for prediction of acid mine drainage. In Environmental Impacts of Mining Activities; Azcue, J.M., Ed.; Springer: Berlin, Germany, 1999; pp. 19–38. [Google Scholar]
  6. USEPA. Technical Document: Acid Mine Drainage Prediction; USEPA: Washington, DC, USA, 1994; p. 52. [Google Scholar]
  7. Grande, J.A.; Beltrán, R.; Santos, J.C.; de la Torre, M.L.; Borrego, J. Acid mine drainage and acid rock drainage in the environment of Herrerías Mine (Iberian Pyrite Belt, Huelva-Spain) and impact on the Andévalo dam. Environ. Geol. 2005, 47, 185–196. [Google Scholar] [CrossRef]
  8. Okabayashi, A.; Wakai, S.; Kanao, T.; Sugio, T.; Kamimura, K. Diversity of 16S ribosomal DNA-defined bacterial population in acid rock drainage from Japanese pyrite mine. J. Biosci. Bioeng. 2005, 100, 644–652. [Google Scholar] [CrossRef]
  9. DeNicola, D.M.; Stapleton, M.G. Benthic diatoms as indicators of long-term changes in a watershed receiving passive treatment for acid mine drainage. Hydrobiologia 2014, 732, 29–48. [Google Scholar] [CrossRef]
  10. Gray, N.F.; Delaney, E. Comparison of benthic macroinvertebrate indices for the assessment of the impact of acid mine drainage on an Irish river below an abandoned Cu-S mine. Environ. Pollut. 2007, 155, 31–40. [Google Scholar] [CrossRef]
  11. Clapcott, J.E.; Goodwin, E.O.; Harding, J.S. Identifying catchment-scale predictors of coal mining impacts on New Zealand stream communities. Environ. Manag. 2016, 57, 711–721. [Google Scholar] [CrossRef]
  12. Ruggiu, D.; Luglié, A.; Cattaneo, A.; Panzani, P. Paleoecological evidence for diatom response to metal pollution in Lake Orta (N. Italy). J. Paleolimnol. 1998, 20, 333–345. [Google Scholar] [CrossRef]
  13. Luís, A.T.; Coelho, H.; Almeida, S.F.P.; Ferreira da Silva, E.A.; Serôdio, J. Photosynthetic activity and ecology of benthic diatom communities from streams affected by Acid Mine Drainage (AMD) in pyritic mines. Fundam. Appl. Limnol. 2013, 182, 47–59. [Google Scholar] [CrossRef]
  14. Luís, A.T.; Teixeira, P.; Almeida, S.F.P.; Ector, L.; Matos, J.X.; Ferreira da Silva, E.A. Impact of acid mine drainage (AMD) on water quality, stream sediments and periphytic diatom communities in the surrounding streams of Aljustrel mining area (Portugal). Water Air Soil Pollut. 2009, 200, 147–167. [Google Scholar] [CrossRef]
  15. Luís, A.T.; Durães, N.; Almeida, S.F.P.; Ferreira da Silva, E.A. Integrating geochemical (surface waters, stream sediments) and biological (diatoms) approaches to assess AMD environmental impact in a pyritic mining area: Aljustrel (Alentejo, Portugal. J. Environ. Sci. 2016, 42, 215–226. [Google Scholar] [CrossRef]
  16. Valente, T.; Rivera, M.J.; Almeida, S.F.P.; Delgado, C.; Gomes, P.; Grande, J.A.; de la Torre, M.L. Characterization of water reservoirs affected by acid mine drainage: Geochemical, mineralogical and biological (diatoms) properties of the water. Environ. Sci. Pollut. Res. Int. 2016, 23, 6002–6011. [Google Scholar] [CrossRef]
  17. Luís, A.T.; Teixeira, P.; Almeida, S.F.P.; Matos, J.X.; Ferreira da Silva, E. Environmental impact of mining activities in the Lousal area (Portugal): Chemical and diatom characterization of metal-contaminated stream sediments and surface water of Corona stream. Sci. Total Environ. 2011, 409, 4312–4325. [Google Scholar] [CrossRef] [PubMed]
  18. Freitas, A.P.P.; Schneider, I.A.H.; Schwartzbold, A. Biosorption of heavy metals by algal communities in water streams affected by the acid mine drainage in the coal-mining region of Santa Catarina state. Brazil Miner. Eng. 2011, 24, 1215–1218. [Google Scholar] [CrossRef]
  19. Sabater, S.; Buchaca, T.; Cambra, J.; Catalan, J.; Guasch, H.; Ivorra, N.; Munoz, I.; Navarro, E.; Real, M.; Romaní, A. Structure and function of benthic algal communities in an extremely acid river. J. Phycol. 2003, 39, 481–489. [Google Scholar] [CrossRef] [Green Version]
  20. DeNicola, D.M. A review of diatoms found in highly acidic environments. Hydrobiologia 2000, 433, 111–122. [Google Scholar] [CrossRef]
  21. Bisthoven, L.J.; Nuyts, P.; Goddeeris, B.; Ollevier, F. Sublethal parameters in deformed Chironomus larvae: Clues to understanding their biomarker value. Freshw. Biol. 1998, 39, 179–191. [Google Scholar] [CrossRef]
  22. Hogsden, K.L.; Harding, J.S. Consequences of acid mine drainage for the structure and function of benthic stream communities: A, review. Freshw. Sci. 2012, 31, 108–120. [Google Scholar] [CrossRef]
  23. Bisthoven, J.L.; Gerhardt, A.; Soares, A.M.V.M. Chironomidae as bioindicators of an acid mine drainage in S. Portugal. Hydrobiologia 2005, 532, 181–191. [Google Scholar] [CrossRef]
  24. Montero, I.C.; Brimhall, G.H.; Alpers, C.N.; Swayze, G.A. Characterization of waste rock associated with acid drainage at the Penn Mine, California, by ground-based visible to short-wave infrared reflectance spectroscopy assisted by digital mapping. Chem. Geol. 2005, 215, 452–472. [Google Scholar] [CrossRef] [Green Version]
  25. Lottermoser, B. Mine Wastes Characterization, Treatment and Environmental Impacts, 2nd ed.; Springer Publisher: Heidelberg, Germany, 2007; p. 400. [Google Scholar]
  26. Pearce, J.; Weber, P.; Pearce, S.; Scott, P. Acid and metalliferous drainage contaminant load prediction for operational or legacy mines at closure. In Mine Closure; Fourie, A.B., Tibbett, M., Eds.; Australian Centre for Geomechanics: Perth, Australia, 2016; pp. 663–676. [Google Scholar]
  27. Quatrini, R.; Johnson, D.B. Microbiomes in extremely acidic environments: Functionalities and interactions that allow survival and growth of prokaryotes at low pH. Curr. Opin. Microbiol. 2018, 43, 139–147. [Google Scholar] [CrossRef] [PubMed]
  28. Yaacob, W.Z.W.; Pauzi, N.S.M.; Mutalib, H.A. Acid mine drainage and heavy metals contamination at abandoned and active mine sites in Pahang. Bull. Geol. Soc. Malays. 2009, 55, 15–20. [Google Scholar] [CrossRef] [Green Version]
  29. Bodenan, F.; Baranger, P.; Piantone, P.; Lassin, A.; Azaroual, M. Arsenic behaviour in gold-ore mill tailings, Massif Central, France: Hydrogeochemical study and investigation of in situ redox signatures. Appl. Geochem. 2004, 19, 1785–1800. [Google Scholar] [CrossRef]
  30. Kang, J.-K.; Song, Y.; Moon, J.-W.; Moon, H.-S. Water quality impact of mining in the Wolmyoung area of Korea, and its short-term changes. Water Air Soil Pollut. 2001, 129, 349–367. [Google Scholar] [CrossRef]
  31. Rivera, M.J.; Luís, A.T.; Grande, J.A.; Sarmiento, A.M.; Dávila, J.M.; Fortes, J.C.; Córdoba, F.; Diaz-Curiel, J.; Santisteban, M. Physico-Chemical Influence of Surface Water Contaminated by Acid Mine Drainage on the Populations of Diatoms in Dams (Iberian Pyrite Belt, SW Spain). Int. J. Environ. Res. Public Health 2019, 16, 4516. [Google Scholar] [CrossRef] [Green Version]
  32. Nocete, F.; Sáez, R.; Nieto, J.M.; Cruz-Aunon, R.; Cabrero, R.; Alex, E.; Bayona, M.R. Circulation of silicified oolitic limestone blades in South-Iberia (Spain and Portugal) during the third millennium B.C.: An expression of a core/periphery framework. J. Anthropol. Archaeol. 2005, 24, 62–81. [Google Scholar] [CrossRef]
  33. Sarmiento, A.M.; Nieto, J.M.; Olías, M.; Cánovas, C.R. Hydrochemical characteristics and seasonal influence on the pollution by acid mine drainage in the Odiel river Basin (SW Spain). Appl. Geochem. 2009, 24, 697–714. [Google Scholar] [CrossRef]
  34. Sarmiento, A.M.; DelValls, A.; Nieto, J.M.; Salamanca, M.J.; Caraballo, M.A. Toxicity and potential risk assessment of a river polluted by acid mine drainage in the Iberian Pyrite Belt (SW Spain). Sci. Total Environ. 2011, 409, 4763–4771. [Google Scholar] [CrossRef] [PubMed]
  35. Grande, J.A.; Valente, T.; de la Torre, M.; Santisteban, M.; Cerón, J.C.; Pérez-Ostalé, E. Characterization of acid mine drainage sources in the Iberian Pyrite Belt: Base methodology for quantifying affected areas and for environmental management. Environ. Earth. Sci. 2014, 71, 2729–2738. [Google Scholar] [CrossRef]
  36. Sáinz, A.; Grande, J.A.; de la Torre, L. Characterization of heavy metal discharge into the Ria of Huelva. Environ. Int. 2004, 30, 557–566. [Google Scholar] [CrossRef]
  37. Younger, P.L. Hydrogeochemistry of minewaters flowing from abandoned coal workings in the Durham coalfield. Q. J. Eng. Geol. Hydrogeol. 1995, 28, 101–113. [Google Scholar] [CrossRef]
  38. Caruccio, F.T.; Ferm, J.C. Paleoenvironment—predictor of Acid Mine Drainage Problems. In Proceedings of the 5th Coal Mine Drainage Research Symposium, National Coal Association (USA), Louisville, KY, USA; 1974; pp. 5–9. [Google Scholar]
  39. Kim, J.-Y.; Chon, H.-T. Pollution of a water course impacted by acid mine drainage in the Imgok creek of the Gangreung coal field, Korea. Appl. Geochem. 2001, 16, 1387–1396. [Google Scholar] [CrossRef]
  40. Herlihy, A.T.; Kaufmann, P.R.; Mitch, M.E.; Brown, D.D. Regional estimates of acid mine drainage impact on streams in the mid-Atlantic and southeastern United States. Water Air Soil Pollut. 1990, 50, 91–107. [Google Scholar] [CrossRef]
  41. Pennsylvania Department of Environmental Protection. Pennsylvania Water Quality Assessment 305(b) Report: Harrisburg, P.A., Pennsylvania Department of Environmental Protection, 3800-BK-DEP2530 5/2/2002. Available online: www.dep.pa.gov (accessed on 7 November 2021).
  42. Bell, F.G.; Halbich, T.F.J.; Bullock, S.E.T. The effects of acid mine drainage from an old mine in the Witbank Coalfield, South Africa. Q. J. Eng. Geol. Hydrogeol. 2002, 35, 265–278. [Google Scholar] [CrossRef]
  43. Luís, A.T.; Teixeira, M.; Durães, N.; Pinto, R.; Almeida, S.F.P.; Ferreira da Silva, E.A.; Figueira, E. Extremely acidic environment: Biogeochemical effects on algal biofilms. Ecotoxicol. Environ. Saf. 2019, 177, 124–132. [Google Scholar] [CrossRef] [PubMed]
  44. Gray, J.B.; Vis, M.L. Reference diatom assemblage response to restoration of an acid mine drainage stream. Ecol. Indic. 2013, 29, 234–245. [Google Scholar] [CrossRef]
  45. Hill, B.H.; Herlihy, A.T.; Kaufmann, P.R.; Stevenson, R.J.; McCormick, F.H.; Johnson, C.B. Use of periphyton assemblage data as an index of biotic integrity. J. N. Am. Benthol. Soc. 2000, 19, 50–67. [Google Scholar] [CrossRef]
  46. Zalack, J.T.; Smucker, N.J.; Vis, M.L. Development of a Diatom Index of biotic integrity for acid mine drainage impacted streams. Ecol. Indic. 2010, 10, 287–295. [Google Scholar] [CrossRef]
  47. Smucker, N.J.; Vis, M.L. Use of diatoms to assess agricultural and coal mining impacts on streams and a multiassemblage case study. J. N. Am. Benthol. Soc. 2009, 28, 659–675. [Google Scholar] [CrossRef] [Green Version]
  48. Van Dam, H.; Merten, A.; Sinkeldam, J. A coded checklist and ecological indicator values of freshwater diatoms from The Netherlands. Netherland J. Aquat. Ecol. 1994, 28, 117–133. [Google Scholar]
  49. Luís, A.T.; Novais, M.H.; Van de Vijver, B.; Almeida, S.F.P.; Ferreira da Silva, E.A.; Hoffmann, L.; Ector, L. Pinnularia aljustrelica sp. nov. (Bacillariophyceae), a new diatom species found in acidic waters in the Aljustrel mining area (Portugal), and further observations on the taxonomy, morphology and ecology of P. acidophila HOFMANN et KRAMMER and P. acoricola HUSTEDT. Fottea 2012, 12, 27–40. [Google Scholar]
  50. Ponader, K.C.; Potapova, M.G. Diatoms from the genus Achnanthidium in flowing waters of the Appalachian Mountains (North America): Ecology, distribution and taxonomic notes. Limnologica 2007, 37, 227–241. [Google Scholar] [CrossRef] [Green Version]
  51. Verb, R.G.; Vis, M.L. Comparison of benthic diatom assemblages from streams draining abandoned and reclaimed coal mines and nonimpacted sites. J. N. Am. Benthol. Soc. 2000, 19, 274–288. [Google Scholar] [CrossRef]
  52. Sabater, S. Diatom communities as indicators of environmental stress in the Guadiamar River, S.-W. Spain, following a major mine tailings spill. J. Appl. Phycol. 2000, 12, 113–124. [Google Scholar] [CrossRef]
  53. Peterson, C.G.; Stevenson, R.J. Resistance and resilience of lotic algal communities: Importance of disturbance timing and current. Ecology 1992, 73, 1445–1461. [Google Scholar] [CrossRef]
  54. Gerhardt, A.; Bisthoven, L.J.; Guhr, K.; Soares, A.M.V.M.; Pereira, M.J. Phytoassessment of acid mine drainage: Lemna gibba bioassay and diatom community structure. Ecotoxicology 2008, 17, 47–58. [Google Scholar] [CrossRef]
  55. Luís, A.T.; Grande, J.A.; Dávila, J.M.; Aroba, J.; Durães, N.; Almeida, S.F.P.; de la Torre, M.L.; Sarmiento, A.M.; Fortes, J.C.; Ferreira da Silva, E.; et al. Application of fuzzy logic tools for the biogeochemical characterisation of (un)contaminated waters from Aljustrel mining area (South Portugal). Chemosphere 2018, 211, 736–744. [Google Scholar] [CrossRef]
  56. Dong, X.; Jian, X.; Jiang, W.; Wu, N.; Tang, T.; Cai, Q. Development and testing of a diatom-based index of biotic integrity for river ecosystems impacted by acid mine drainage in Gaolan river, China. Fresen. Environ. Bull. 2015, 24, 4114–4124. [Google Scholar]
  57. Bray, J.P.; Broady, P.A.; Niyogi, D.K.; Harding, J.S. Periphyton communities in New Zealand streams impacted by acid mine drainage. Mar. Freshw. Res. 2008, 59, 1084–1091. [Google Scholar] [CrossRef]
  58. Jia, X.; Jiang, W.; Li, F.; Tang, T.; Duan, S.; Cai, Q. The response of benthic algae to the impact of acid mine drainage. Acta Ecol. Sin. 2009, 29, 4620–4629. [Google Scholar]
  59. Urrea-Clos, G.; Sabater, S. Comparative study of algal communities in acid and alkaline waters from Tinto, Odiel and Piedras river basins (SW Spain). Limnetica 2009, 28, 261–272. [Google Scholar]
  60. Aguilera, A. Eukaryotic organisms in extreme acid environments. Life 2013, 3, 363–374. [Google Scholar] [CrossRef] [Green Version]
  61. Rivera, M.J.; Santisteban, M.; Aroba, J.; Grande, J.A.; Dávila, J.M.; Sarmiento, A.M.; Fortes, J.C.; Diaz-Curiel, J.; Luís, A.T. Application of Fuzzy Logic Techniques for Biogeochemical Characterization of Dams Affected by Acid Mine Drainage (AMD) Processes in the Iberian Pyrite Belt (IPB), Spain. Water Air Soil Pollut. 2020, 231, 142. [Google Scholar] [CrossRef]
  62. Tiwari, A.; Marella, T.K. Potential and application of diatoms for industry-specific wastewater treatment. In Application of Microalgae in Wastewater Treatment; Gupta, S., Bux, F., Eds.; Springer: Cham, Germany, 2019; pp. 321–339. [Google Scholar]
  63. Marella, T.K.; Saxena, A.; Tiwari, A. Diatom mediated heavy metal remediation: A review. Bioresour. Technol. 2020, 305, 123068. [Google Scholar] [CrossRef] [PubMed]
  64. Morin, S.; Vivas-Nogues, M.; Duong, T.T.; Boudou, A.; Coste, M.; Delmas, F. Dynamics of benthic diatom colonization in a cadmium/zinc-polluted river (Riou-Mort, France). Fundam. Appl. Limnol. 2007, 168, 179–187. [Google Scholar] [CrossRef]
  65. Morin, S.; Cordonier, A.; Lavoie, I.; Arini, A.; Blanco, S.; Duong, T.T.; Tornés, E.; Bonet, B.; Corcoll, N.; Faggiano, L.; et al. Consistency in diatom response to metal-contaminated environments. In Handbook of Environmental Chemistry, Emerging and Priority Pollutants in Rivers; Guasch, H., Ginebreda, A., Geiszinger, A., Eds.; Springer: Heidelberg, Germany, 2012; pp. 117–146. [Google Scholar]
  66. Falasco, E.; Bona, F.; Badino, G.; Hoffmann, L.; Ector, L. Diatom teratological forms and environmental alterations: A review. Hydrobiologia 2009, 623, 1–35. [Google Scholar] [CrossRef]
  67. Gold, C.; Feurtet-Mazel, A.; Coste, M.; Boudou, A. Effects of cadmium stress on periphytic diatom communities in indoor artificial streams. Freshw. Biol. 2003, 48, 316–328. [Google Scholar] [CrossRef]
  68. Hernández-Ávila, J.; Salinas-Rodríguez, E.; Cerecedo-Sáenz, E.; Reyes-Valderrama, I.; Arenas-Flores, A.; Román-Gutiérrez, A.D.; Rodríguez-Lugo, V. Diatoms and their capability for heavy metal removal by cationic exchange. Metals 2017, 7, 169. [Google Scholar] [CrossRef]
  69. Ferreira da Silva, E.F.; Almeida, S.F.P.; Nunes, M.L.; Luís, A.T.; Borg, F.; Hedlund, M.; Marques de Sá, C.; Patinha, C.; Teixeira, P. Heavy metal pollution downstream the abandoned Coval da Mó mine (Portugal) and associated effects on epilithic diatom communities. Sci. Total Environ. 2009, 407, 5620–5636. [Google Scholar] [CrossRef]
  70. Stewart, P.M.; Smith, E.P.; Cairns-Jr, J. Relationship of the physicochemical environment to diatom and protozoan communities: A multivariate approach. Arch. Für Protistenkd. 1987, 134, 331–341. [Google Scholar] [CrossRef]
  71. Cattaneo, A.; Couillard, Y.; Wunsam, S.; Courcelles, M. Diatom taxonomic and morphological changes as indicators of metal pollution and recovery in Lac Dufault (Québec, Canada). J. Paleolimnol. 2004, 32, 163–175. [Google Scholar] [CrossRef]
  72. Coste, M.; Boutry, S.; Tison-Rosebery, J.; Delmas, F. Improvements of the Biological Diatom Index (BDI): Description and efficiency of the new version (BDI-2006). Ecol. Indic. 2009, 9, 621–650. [Google Scholar] [CrossRef]
  73. Amaral-Zettler, L.A.; Gomez, F.; Zettler, E.; Keenan, B.G.; Amils, R.; Sogin, M.L. Eukaryotic diversity in Spain’s River of Fire. Nature 2002, 417, 137. [Google Scholar] [CrossRef]
  74. Aguilera, A.; Souza-Egipsy, V.; Gonzalez-Toril, E. La vida en Río Tinto; Centro de Astrobiología-CSIC-INTA, Ministerio de Defensa: Madrid, Spain, 2000; p. 100. [Google Scholar]
  75. Verb, R.G.; Vis, M.L. Macroalgal communities from an acid mine drainage impacted watershed. Aquat. Bot. 2001, 71, 93–107. [Google Scholar] [CrossRef]
  76. Niyogi, D.K.; Lewis, W.M., Jr.; McKnight, D.M. Effects of stress from mine drainage on diversity, biomass, and function of primary producers in mountain streams. Ecosystems 2002, 5, 554–567. [Google Scholar]
  77. Novis, P.M. Taxonomy of Klebsormidium (Klebsormidiales, Charophyceae) in New Zealand streams and the significance of low-pH habitats. Phycologia 2006, 45, 293–301. [Google Scholar] [CrossRef]
  78. Dean, A.P.; Hartley, A.; McIntosh, O.A.; Smith, A.; Feord, H.K.; Holmberg, N.H.; King, T.; Yardley, E.; White, K.N.; Pittman, J.K. Metabolic adaptation of a Chlamydomonas acidophila strain isolated from acid mine drainage ponds with low eukaryotic diversity. Sci. Total Environ. 2019, 647, 75–87. [Google Scholar] [CrossRef]
  79. Díaz, S.; de Francisco, P.; Olsson, S.; Aguilera, A.; González-Toril, E.; Martín, A.M. Toxicity, physiological, and ultrastructural effects of Arsenic and Cadmium on the extremophilic microalga Chlamydomonas acidophila. Int. J. Environ. Res. Public Health 2020, 17, 1650. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  80. Aguilera, A.; Suominen, S.; Pétursdóttir, S.; Olgudóttir, E.; Guðmundsdóttir, E.E.; Altamirano, M.; González-Toril, E.; Hreggviðsson, G.O. Physiological plasticity of high-temperature intertidal cyanobacterial microbial mats to temperature and salinity: Daily and seasonal in situ photosynthetic performance. Eur. J. Phycol. 2020, 55, 223–233. [Google Scholar] [CrossRef]
  81. Stevens, A.E.; McCathy, B.C.; Vis, M.L. Metal content of Klebsormidium-dominated (Chlorophyta) algal mats from acid mine drainage waters in southeastern. J. Torrey Bot. Soc. 2001, 128, 226–233. [Google Scholar] [CrossRef]
  82. Vinebrooke, R.D. Abiotic and biotic regulation of periphyton in recovering acidified lakes. J. N. Am. Benthol. Soc. 1996, 15, 318–331. [Google Scholar] [CrossRef]
  83. Kalin, M.; Wheeler, W.N.; Olaveson, M.M. Response of phytoplankton to ecological engineering remediation of a Canadian Shield Lake affected by acid mine drainage. Ecol. Eng. 2006, 28, 296–310. [Google Scholar] [CrossRef]
  84. Novis, P.M. A taxonomic survey of microspora (Chlorophyceae, Chlorophyta) in New Zealand. N. Z. J. Bot. 2004, 42, 153–165. [Google Scholar] [CrossRef]
  85. Aguilera, A.; González-Toril, E. Eukaryotic life in extreme environments: Acidophilic fungi. In Fungi in Extreme Environments: Ecological Role and Biotechnological Significance; Tiquia-Arashiro, S.M., Grube, M., Eds.; Springer: NY city, NY, USA, 2019; pp. 21–38. [Google Scholar]
  86. López-Archilla, A.; González, A.E.; Terrón, M.C.; Amils, R. Ecological study of the fungal populations of the acidic Tinto River in Southwestern Spain. Can. J. Microbiol. 2004, 50, 923–934. [Google Scholar] [CrossRef] [PubMed]
  87. Duran, C.; Marin, I.; Amils, R. Specific metal sequestering acidophilic fungi. In Biohydrometallurgy and the Environment; Amils, R., Ballester, A., Eds.; Towards the Mining of the 21st Century, Proc. Int. Biohydrometal Symp; Elsevier: Amsterdam, The Netherlands, 1999; pp. 521–530. [Google Scholar]
  88. Oggerin, M.; Tornos, F.; Rodríguez, N.; del Moral, C.; Sánchez-Román, M.; Amils, R. Specific jarosite biomineralization by Purpureocillium lilacinum, an acidophilic fungus isolated from Río Tinto. Environ. Microbiol. 2013, 15, 2228–2237. [Google Scholar] [CrossRef] [PubMed]
  89. López-Archilla, A.I. Rio Tinto: Un universo de mundos microbianos. Ecosistemas 2005, 14, 52–65. [Google Scholar]
  90. Wright, I.A.; Paciuszkiewicz, K.; Belmer, N. Increased Water Pollution After Closure of Australia’s Longest Operating Underground Coal Mine: A 13-Month Study of Mine Drainage, Water Chemistry and River Ecology. Water Air Soil Pollut. 2018, 229, 55. [Google Scholar] [CrossRef]
  91. St. Louiss, V.L. Element concentrations in chironomids and their abundance in the littoral zone of acidified lakes in Northwestern Ontario. J. Fish. Aquat. Sci. 1993, 50, 953–963. [Google Scholar] [CrossRef]
  92. Deneke, R. Review of rotifers and crustaceans in highly acidic environments of pH values < 3. Hydrobiologia 2000, 433, 167–172. [Google Scholar]
  93. Amaral-Zettler, L.A. Eukaryotic diversity at pH extremes. Front. Microbiol. 2013, 3, 1–17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Gower, A.M.; Myers, G.; Kent, M.; Foulkes, M.E. Relationships between macroinvertebrate communities and environmental variables in metal-contaminated streams in south-West England. Freshw. Biol 1994, 32, 199–221. [Google Scholar] [CrossRef]
  95. de Jonge, M.; de Vijuer, B.V.; Blust, R.; Bervoets, L. Responses of aquatic organisms to metal pollution in a lowland river in Flanders: A comparison of diatoms and macroinvertebrates. Sci. Total Environ. 2008, 407, 615–629. [Google Scholar] [CrossRef] [PubMed]
  96. Loayza-Muro, R.A.; Elias-Letts, R.; Marticorena-Ruiz, J.K.; Palomino, E.J.; Duivenvoorden, J.F.; Kraak, M.H.S.; Admiraal, W. Metal-induced shifts in benthic macroinvertebrate community composition in Andean high altitude streams. Environ. Toxicol. Chem. 2010, 29, 2761–2768. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  97. Loayza-Muro, R.A.; de Baat, M.L.; Palomino, E.J.; Kuperus, P.; Kraak, M.H.S.; Admiraal, W.; Breeuwer, J.A.J. Metals and altitude drive genetic diversity of chironomids in Andean streams. Freshw. Biol. 2014, 59, 56–63. [Google Scholar] [CrossRef]
  98. Loayza-Muro, R.A.; Duivenvoorden, J.F.; Kraak, M.H.S.; Admiraal, W. 2014b Metal leaching, acidity, and altitude confine benthic macroinvertebrate community composition in Andean streams. Environ. Toxicol. Chem. 2014, 33, 404–411. [Google Scholar] [CrossRef]
  99. Beltman, D.J.; Clements, W.H.; Lipton, J.; Cacela, D. Benthic invertebrate metals exposure, accumulation and community-level effects downstream from a hard rock mine site. Environ. Toxicol. Chem. 1999, 18, 299–307. [Google Scholar] [CrossRef]
  100. Gerhardt, A.L.; Bisthoven, J.; Soares, A.M.V.M. Macroinvertebrate response to acid mine drainage: Community metrics and on-line behavioural toxicity bioassay. Environ. Pollut. 2004, 130, 263–274. [Google Scholar] [CrossRef]
  101. Canfield, T.J.; Kemble, N.E.; Brumbaugh, W.G.; Dwyer, F.J.; Ingersoll, C.G.; Fairchild, J.F. Use of benthic invertebrate community structure and the sediment quality triad to evaluate metal-contaminated sediment in the upper Clark Fork River, Montana. Environ. Toxicol. Chem. 1994, 13, 1999–2012. [Google Scholar] [CrossRef]
  102. Bisthoven, L.J.; Gerhardt, A. Chironomidae (Diptera, Nematocera) fauna in three small streams of Skania, Sweden. Environ. Monit. Assess. 2003, 83, 89–102. [Google Scholar] [CrossRef]
  103. Bisthoven, J.L.; Gerhardt, A.; Soares, A.M.V.M. Effects of Acid Mine Drainage on larval Chironomus (Diptera, Chironomidae) measured with the Multispecies Freshwater Biomonitor. Environ. Toxicol. Chem. 2004, 23, 1123–1128. [Google Scholar] [CrossRef]
  104. De Haas, E.M.; van Haaren, R.; Koelmans, A.A.; Kraak, M.H.S.; Admiraal, W. Analyzing the causes for the persistence of chironomids in floodplain lake sediments. Arch. Hydrobiol. 2005, 162, 211–228. [Google Scholar] [CrossRef]
  105. Löhr, A.J.; Sluik, R.; Olaveson, M.M.; Ivorra, N.; van Gestel, C.A.M.; van Straalen, N.M. Macroinvertebrate and algal communities in an extremely acidic river and the Kawah Ijen crater lake (pH < 0.3), Indonesia. Arch. Hydrobiol. 2006, 165, 1–21. [Google Scholar]
  106. Hamerlík, L.; Jacobsen, D. Chironomid (Diptera) distribution and diversity in Tibetan streams with different glacial influence. Insect Conserv. Divers. 2011, 5, 319–326. [Google Scholar] [CrossRef]
  107. Loayza-Muro, R.A.; Marticorena-Ruiz, J.K.; Palomino, E.J.; Merritt, C.; De Baat, M.L.; van Gemert, M.; Verweij, R.A.; Kraak, M.H.S.; Admiraal, W. Persistence of chironomids in metal polluted Andean high altitude streams: Does melanin play a role? Environ. Sci. Technol. 2013, 47, 601–607. [Google Scholar] [CrossRef] [PubMed]
  108. Groenendijk, D.; Lücker, S.M.G.; Plans, M.; Kraak, M.H.S.; Admiraal, W. Dynamics of metal adaptation in riverine chironomids. Environ. Pollut. 2002, 117, 101–109. [Google Scholar] [CrossRef]
  109. Van Straalen, N.M.; Donker, M.H.; Vijver, M.G.; van Gestel, C.A.M. Bioavailability of contaminants estimated from uptake rates into soil invertebrates. Environ. Pollut. 2005, 136, 409–417. [Google Scholar] [CrossRef] [PubMed]
  110. Buchwalter, D.B.; Cain, D.J.; Martin, C.A.; Xie, L.; Luoma, S.N.; Garland, T. Aquatic insect ecophysiological traits reveal phylogenetically based differences in dissolved cadmium susceptibility. Proc. Natl. Acad. Sci. USA 2008, 105, 8321–8326. [Google Scholar] [CrossRef] [Green Version]
  111. Sibly, R.M.; Calow, P. A life-cycle theory of responses to stress. Biol. J. Linn. Soc. 1989, 37, 101–116. [Google Scholar] [CrossRef]
  112. Michailova, P.; Ilkova, J.; Kerr, R.; White, K. Chromosome variability in Chironomus acidophilus Keyl, 1960 from the Afon Goch, UK—A river subject to long-term trace metal pollution. Aquat. Insects 2009, 31, 213–225. [Google Scholar] [CrossRef]
  113. Martinez, E.A.; Moore, B.C.; Schaumloffel, J.; Dasgupta, N. Morphological abnormalities in Chironomus tentans exposed to cadmium and copper-spiked sediments. Ecotoxicol. Environ. Saf. 2003, 55, 204–212. [Google Scholar] [CrossRef]
  114. di Veroli, A.; Goretti, E.; Paumen, M.L.; Kraak, M.H.S.; Admiraal, W. Induction of mouthpart deformities in chironomid larvae exposed to contaminated sediments. Environ. Pollut. 2012, 166, 212–217. [Google Scholar] [CrossRef] [PubMed]
  115. Warwick, W.F. Morphological deformities in Chironomidae (Diptera) larvae as biological indicators of toxic stress. In Toxic Contaminants and Ecosystem Health: A Great Lakes Focus; Evans, M.S., Ed.; Wiley: New York, NY, USA, 1988; pp. 281–320. [Google Scholar]
  116. Warwick, W.F. Indexing deformities in ligulae and antennae of Procladius larvae (Diptera: Chironomidae): Application to contaminant-stressed environments. J. Fish. Aquat. Sci. 1991, 48, 1151–1166. [Google Scholar] [CrossRef]
  117. Beghelli, F.G.D.; Lopez-Doval, J.C.; Rosa, A.H.; Pompeo, M.; Carlos, V.M. Lethal and sublethal effects of metal-polluted sediments on Chironomus sancticaroli Strixino and Strixino, 1981. Ecotoxicology 2018, 27, 286–299. [Google Scholar] [CrossRef] [PubMed]
  118. di Veroli, A.; Santoro, F.; Pallottini, M.; Selvaggi, R.; Scardazza, F.; Cappelletti, D.; Goretti, E. Deformities of chironomid larvae and heavy metal pollution: From laboratory to field studies. Chemosphere 2014, 112, 9–17. [Google Scholar] [CrossRef]
  119. Martinez, E.A.; Moore, B.C.; Schaumloffel, J.; Dasgupta, N. Effects of exposure to a combination of zinc- and lead-spiked sediments on mouthpart development and growth in Chironomus tentans. Environ. Toxicol. Chem. 2004, 23, 662–667. [Google Scholar] [CrossRef] [PubMed]
  120. Schlief, J.; Mutz, M. Palatability of leaves conditioned in streams affected by mine drainage: A feeding experiment with Gammarus pulex (L.). Hydrobiologia 2006, 563, 445–452. [Google Scholar] [CrossRef]
  121. Aluma, E.; Johnson, K.S.; Hassett, P. Mercury Bioaccumulation in Crayfish in Acid Mine-Impaired Appalachian Streams. Water Air Soil Pollut. 2017, 228, 200. [Google Scholar] [CrossRef]
  122. He, F.; Jiang, W.; Tang, T.; Cai, Q. Assessing impact of acid mine drainage on benthic macroinvertebrates: Can functional diversity metrics be used as indicators? J. Freshw. Ecol. 2015, 30, 513–524. [Google Scholar] [CrossRef] [Green Version]
  123. Luís, A.T.; Grande, J.A.; Durães, N.; Dávila, J.M.; Santisteban, M.; Almeida, S.F.P.; Sarmiento, A.M.; de la Torre, M.L.; Fortes, J.C.; Ferreira da Silva, E. Biogeochemical characterization of surface waters in the Aljustrel mining area (South Portugal). Environ. Geochem. Health 2019, 211, 736–744. [Google Scholar] [CrossRef] [PubMed]
  124. Chacon-Baca, E.; Santos, A.; Sarmiento, A.M.; Luís, A.T.; Santisteban, M.; Fortes, J.C.; Dávila, J.M.; Curiel, J.; Grande, J.A. Acid Mine Drainage as energizing microbial niches for the formation of clastic iron stromatolites: The Tintillo river in SW Spain. Astrobiology 2021, 21, 443–463. [Google Scholar] [CrossRef] [PubMed]
Figure 1. (A) Pinnularia acidophila, (B) Pinnularia acoricola, (C) Pinnularia aljustrelica, (D) Pinnularia subcapitata and (E) Eunotia exigua.
Figure 1. (A) Pinnularia acidophila, (B) Pinnularia acoricola, (C) Pinnularia aljustrelica, (D) Pinnularia subcapitata and (E) Eunotia exigua.
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Figure 2. (A) Unicellular algae (Chlamydomonas acidophila), (B) Filamentous algae (Klebsormidium sp.), (C) Euglena mutabilis, (D) Protozoo Heliozoa, (E) Protozoo Ciliata, (F) Amoeba, (G) Rotífer.
Figure 2. (A) Unicellular algae (Chlamydomonas acidophila), (B) Filamentous algae (Klebsormidium sp.), (C) Euglena mutabilis, (D) Protozoo Heliozoa, (E) Protozoo Ciliata, (F) Amoeba, (G) Rotífer.
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Figure 3. (A) Scytalidium thermophilum, (B) Possible Acremonium sp., (C) Scytalidium acidophilum, (D) Lecythophora hoffmannii. Photos from [89]. Photos adapted from ref. [89].
Figure 3. (A) Scytalidium thermophilum, (B) Possible Acremonium sp., (C) Scytalidium acidophilum, (D) Lecythophora hoffmannii. Photos from [89]. Photos adapted from ref. [89].
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Figure 4. Microphotographs of individuals from family Chironomidae: (A) Cricotopus sp., (B) subfamily Orthocladinae.
Figure 4. Microphotographs of individuals from family Chironomidae: (A) Cricotopus sp., (B) subfamily Orthocladinae.
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Table 1. Diatom species with pH and metal concentrations (mg/L), pH tolerance range and optimum pH.
Table 1. Diatom species with pH and metal concentrations (mg/L), pH tolerance range and optimum pH.
Species NamepH Tolerance RangeOptimum pHMetal Concentrations
Pinnularia aljustrelica2.0–5.02.0–3.0Fe 1300 to 6000
Cu 230–350
Zn 118–170
Pinnularia acidophila2.0–4.52.0–2.2
Pinnularia acoricola2.0–6.02.0–3.0
Nitzschia thermalis2.0–7.03.0
Nitzschia hantzschiana2.0–6.82.0–2.2
Eunotia exigua3.0–5.03.0Similar metal concentrations as above, but species valves are morphologically affected by metals (teratologies)
Brachysira vitrea4.5–7.54.8Fe 1100
Zn 0.30
Cu 0.64
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Luís, A.T.; Córdoba, F.; Antunes, C.; Loayza-Muro, R.; Grande, J.A.; Silva, B.; Diaz-Curiel, J.; Ferreira da Silva, E. Extremely Acidic Eukaryotic (Micro) Organisms: Life in Acid Mine Drainage Polluted Environments—Mini-Review. Int. J. Environ. Res. Public Health 2022, 19, 376. https://doi.org/10.3390/ijerph19010376

AMA Style

Luís AT, Córdoba F, Antunes C, Loayza-Muro R, Grande JA, Silva B, Diaz-Curiel J, Ferreira da Silva E. Extremely Acidic Eukaryotic (Micro) Organisms: Life in Acid Mine Drainage Polluted Environments—Mini-Review. International Journal of Environmental Research and Public Health. 2022; 19(1):376. https://doi.org/10.3390/ijerph19010376

Chicago/Turabian Style

Luís, Ana Teresa, Francisco Córdoba, Catarina Antunes, Raul Loayza-Muro, José Antonio Grande, Bruna Silva, Jesus Diaz-Curiel, and Eduardo Ferreira da Silva. 2022. "Extremely Acidic Eukaryotic (Micro) Organisms: Life in Acid Mine Drainage Polluted Environments—Mini-Review" International Journal of Environmental Research and Public Health 19, no. 1: 376. https://doi.org/10.3390/ijerph19010376

APA Style

Luís, A. T., Córdoba, F., Antunes, C., Loayza-Muro, R., Grande, J. A., Silva, B., Diaz-Curiel, J., & Ferreira da Silva, E. (2022). Extremely Acidic Eukaryotic (Micro) Organisms: Life in Acid Mine Drainage Polluted Environments—Mini-Review. International Journal of Environmental Research and Public Health, 19(1), 376. https://doi.org/10.3390/ijerph19010376

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