Examples of lanthanides and their concentrations in different plants and locations (according to Goecke et al. [3]).
Abstract
This chapter discusses the ecological and physiological impacts of lanthanides on algae as primary producers in aquatic environments. Although lanthanides are nonessential elements for living organisms, their bioaccumulation is a common phenomenon. Here, we critically review the ecological effects of increasing levels of lanthanides directly reaching water systems through mining, application of fertilizers, and the production of advanced technologies. We describe interactions between lanthanides and algae, with a particular focus on various applications including fertilizers, tracers, bioindicators, bioremediation, and recycling. We examine the stimulatory effects of low levels of lanthanides versus their toxicity at higher levels and discuss mechanisms by which they may affect the algal cell. This chapter highlights the importance of a better understanding of the biological roles of lanthanides.
Keywords
- algae
- microalgae
- lanthanides
- bioaccumulation
- environmental pollution
- toxicity
- fertilizers
- metals
- recycling
- remediation
1. Introduction
Lanthanides play many roles in a number of different fields including chemistry, biology, and medicine [1]. They have also become indispensable in many modern technologies but the growing demand for these metals has also increased their release into the surrounding biosphere. Therefore, it is important to consider and address the impacts of increased lanthanides on the environment. The affinity of algae for these elements can pose a serious environmental threat or be a unique opportunity for the treatment of contaminated areas.
Lanthanides are considered nonessential elements that can induce both positive and negative physiological responses in the living organism. They are not essential for any known metabolic process, but under certain conditions, they may have a positive effect [2, 3]. Unlike heavy metals, whose toxicity has been extensively investigated, the effects of lanthanides have been neglected [4], particularly, their impacts on aquatic environments that are associated with the exploitation of lanthanides [5]. Water contamination by metals is a global problem, and metal recovery from wastewaters and industrial wastes is significant not only from an ecological point of view but also because of the sustainable availability of these materials [6].
This review aims to summarize our knowledge of positive and toxic effects of lanthanides on algae in order to better elucidate their biological roles. Various applications and methods of use, including the possibility of remediation and lanthanide recycling, are also summarized.
2. Lanthanides in algae
The presence of lanthanides (Pr, Nd, and Sm) was recorded for the first time in the red alga
Algae contain a diverse spectrum of lanthanides, regardless of size (micro or macroalgae), structural arrangements (unicellular, fibrous, and crustaceous), algal type (e.g., Chlorophyta, Rhodophyta, and Charophyta) as well as Cyanobacteria [8, 9, 10, 11]. These analyses show that seaweed lanthanide concentrations may be 10–20 times higher than those in terrestrial plants ([8], see Table 1) and more than 100 times higher than in sea water [10, 16].
Treea | Teab | Mossc | Potatod | Red algae | Brown algaf | Green algag | |
---|---|---|---|---|---|---|---|
Sc | nd | 0.085 | nd | nd | nd | nd | nd |
Y | nd | 0.360 | 0.127 | 0.011 | nd | nd | nd |
La | 0.280 | 0.600 | 0.266 | 0.017 | 0.362 | 0.032 | |
Ce | 0.370 | 1.000 | 0.493 | 0.038 | 0.943 | 0.076 | |
Pr | 0.091 | 0.120 | 0.056 | 0.007 | 0.049 | 0.008 | |
Nd | 0.155 | 0.440 | 0.402 | 0.015 | 0.191 | 0.039 | |
Sm | 0.031 | 0.085 | 0.036 | 0.008 | 0.034 | 0.009 | |
Eu | 0.004 | 0.018 | 0.009 | 0.001 | 0.008 | 0.028 | |
Gd | 0.024 | 0.093 | 0.037 | 0.007 | 0.044 | 0.012 | |
Tb | 0.017 | nd | 0.005 | 0.001 | 0.006 | 0.001 | |
Dy | 0.021 | 0.074 | 0.024 | 0.002 | 0.030 | 0.012 | |
Ho | 0.004 | 0.019 | 0.004 | 0.000 | 0.006 | 0.002 | |
Er | 0.006 | — | 0.013 | 0.002 | 0.015 | 0.008 | |
Tm | 0.001 | — | 0.001 | 0.000 | 0.002 | 0.001 | |
Yb | 0.008 | 0.044 | 0.011 | 0.001 | 0.008 | 0.007 | |
Lu | 0.019 | 0.007 | 0.001 | 0.000 | 0.001 | 0.001 | |
Total lanthanides can range from 1 to 1.3 μg/g of algal biomass under laboratory conditions, and can be achieved easily, whereas under natural conditions (freshwater and sea water), the total amount of lanthanides ranges between 10−3 and 10−1 μg/g of algal biomass ([4, 17, 18, 19], and links therein).
There are only a few studies comparing lanthanides in different coexisting organisms, including algae. These studies indicate the relevance of lanthanides, particularly in microorganisms, and clear differences between coexisting groups of organisms (Table 2). Such a wide range of biotic concentrations of lanthanides can be generated by: (i) relative concentrations of elements in water; (ii) physical and metabolic processes specific to each type of algae (cell wall components, enzymes, proteins, etc.); and (iii) environmental factors specific to each area, e.g., temperature, light, pH, and nitrogen availability that can affect the two previous factors [22, 23, 24].
The concentration of lanthanides in the environment increases with changes in climatic conditions, groundwater action, and volcanic activity [25], but there are also significant anthropogenic sources of lanthanides in phosphoric mineral fertilizers, industrial waste waters, and mine extractions [4, 18, 26, 27, 28, 29]. Algae can serve as bioindicators because they can accumulate these elements in their cells (Table 1).
3. Beneficial effects of lanthanides
The probable biological effect of lanthanides is related to similarities between their ionic radii and coordination numbers with elements such as Ca, Mn, Mg, Fe, or Zn. Another aspect is their ability to form stable complexes with organic molecules [30]. Substitution of essential metal ions involves, for example, changes in enzyme activity, protein conformation, or polymerization. Also, changes in the use or allocation of ion channels affects specific membrane permeability and the cellular ion ratio.
Although lanthanides have been used for decades, particularly in China, as fertilizer in agriculture, their specific effects on plants and less so on algae, are not understood. Beneficial effects of lanthanides on growth and quality have been studied, mostly on crops [14, 31, 32] and domestic animals [14, 33, 34, 35]. Absorption, transmission, and metabolic conversion of nutrients were stimulated; metal deficiencies were overcome; and increases in metabolism via enzymatic activities were observed. Likewise, effects of lanthanides on photosynthesis or resistance to stress caused by drought, acid rain, and/or toxic metals (reviewed by [14, 32, 36, 37]) have been described. However, a specific cellular or molecular model for these observations has not been proposed and therefore mechanisms of action of lanthanide in plants or algae remain unclear [38].
One of the positive effects of lanthanides is connected with their ability to alleviate calcium deficiency because of Ln2+ and Ca2+ ions with high chemical similarities. These similarities, as well as the fact that lanthanides have higher valence values compared to calcium, resulted in Ln ions easily replacing Ca2+ and being able to bind with a higher affinity to multiple receptors, thus having various effects on metabolism depending on the effect of the replaced metal [31, 39, 40, 41, 42].
In the majority of experiments carried out with algae and lanthanides, attention was focused on algal (eventually cyanobacterial) growth properties without any effort to understand mechanism(s) of beneficial effects (Table 3). Thus, it is not clear whether the beneficial effects of lanthanides are due to the mitigation of nutrient deficiencies (such as Ca2+, Mg2+, or Mn2+), as previously found in plants [2, 48, 54, 55, 56], or to the fact that lanthanides are involved in some physiological reactions such as scavenging of oxygen-free radicals [30, 57, 58] or due to their ability to neutralize inhibitory effects of heavy metals [37].
Algae | Lanthanide | Positive effect | Negative effect | Reference |
---|---|---|---|---|
La3+ | 38.53–53 | >53.94 | [43] | |
* | LaCl3 | 30–40 | >40 | [44] |
Ce3 | 5–20 | — | [45] | |
La3+ | 5–20 | — | [45] | |
Ce3+ | 1.8 | 2.1 | [46] | |
* | 12 different Ln | — | 29.14 | [47] |
* | La3+ | <7.2 | >72 | [48] |
Dy3+ | 50–100 | 180–1000 | [49] | |
La | 7.28–87.4 | — | [50, 51] | |
Gd | 6.36–57.23 | — | [50, 51] | |
Yb | 5.78–17.34 | — | [50, 51] | |
La3+ | <7.2 | >72 | [48] | |
13 different Ln | — | 28–30 | [52] | |
Sc | — | 21.88 | [52] | |
Y | — | 43.21 | [52] |
In a study on the effect of lanthanides in alleviating metal deficiency in algae, Li et al. [59] showed that La3+ at low concentrations were able to partly substitute for a Ca2+ deficiency in the green macroalga
The effects of single lanthanides and monazite on growth rate, lipid profile, and pigments in two biotechnologically interesting algae (
The use of lanthanides in agriculture and in aquatic cultures is gradually increasing although their impact on the environment has not been sufficiently verified. Lanthanides are not yet commercially available to increase the production of algal biomass despite the fact that their effects on economically interesting pigments and lipids are known. In the alga
4. Toxicity of lanthanides
The toxicity of lanthanides has been reported as low, but is dependent on their chemical form and processing, as reported by Hodge-Sterner’s classification system [62]. In soil and water, however, a surplus of lanthanides has a negative to toxic effect on human beings and animals [63]. Human exposure to lanthanides and effects on health are discussed by Pagano et al. [64]. The best studied effects on health are for Ce, La, and Gd, and the rest remain unclear [64]. The toxicity of lanthanides to various organisms is described in several reports [31, 42, 65], but maximum admissible concentrations, thresholds, and toxicity levels are poorly defined [66]. For each organism or species, the toxicity of different lanthanides differs, but the exact effects remain unknown [67, 68] (Table 3).
The ability of lanthanides to be involved in the metabolism of several basic elements has been considered as a possible cause of their toxicity [36]. Due to this phenomenon, differences in normal functions of several enzymes have been found, as demonstrated by work describing ATPase and pectate lyase [69, 70], ion channel blocking [71], or mineral transport [42, 72].
Although toxic effects of lanthanides have been reported for various microorganisms (Table 3), there is little evidence to generalize their effect on algae. Only a few orders of Charophyta [73], Chlorophyta [46, 48, 74], Dinophyta [75], Euglenophyta [49], Bacillariophyceae [76, 77] and Haptophyta [50], and Cyanobacteria [78, 79] have been studied. Most other algal studies, however, contained little or no data on the bioavailability of lanthanides. The relationship between lanthanide concentrations and stimulatory or inhibitory effects on the same algal species are therefore inconsistent. Moreover, many algal groups or species have not yet been tested for toxicity and no tests for macroalgae have been developed. The database on bioassays for algal toxicity is summarized in Guida et al. [80].
The transfer of lanthanides is expected through the food chain, as algae are primary producers [66, 81]. The toxicity of lanthanide on algae therefore needs to be addressed because any harmful effects may result in the transfer of negative effects to organisms at higher trophic levels [67, 82, 83].
Recent studies on the toxicity of lanthanides to algae describe the depletion of nutrients rather than toxicity itself [83, 84], see Section 7. In these works, it was suggested that lanthanides could capture some essential nutrients such as phosphates, resulting in an effect on growth (death by hunger). The relationship between lanthanides and phosphate was analyzed in detail in [85]. This important property should be examined in more detail because it could affect the bioavailability of these metals (EC50), changing the evaluation of their impact on the environment.
5. Bioaccumulation of metals in algae
In recent decades, metal uptake by algal biomass has been studied with great interest. Uptake can be by passive binding, so-called “biosorption,” or an active process of “bioaccumulation,” where uptake or removal of elements is metabolically controlled [86, 87]. Some metals belong to the group of essential micronutrients, being important for growth and development of plant cells, and are involved in active metabolism [88]. Bioaccumulation of chemical compounds depends on rates of uptake and metabolism, and on the ability of the organism to degrade or store compounds. In essence, the process of accumulation of elements in algal cells is very complicated and depends on the properties of the species (type, size, form, and state of development), the element (charge, chemical form, and concentration), and the medium (pH, type, and concentration of metal salts or presence of complexing agents) [89]. As can be seen in Table 4, accumulation, biosorption, and desorption of lanthanides occurs in micro- and macroalgae, including brown, green, and red algae, algal flagellates, and also cyanobacteria. The potential for biosorption of cerium ions by cyanobacteria
Algae | Lanthanide | Reference |
---|---|---|
* | Ce | [90] |
14 different Ln, Y | [91] | |
Ce | [90] | |
Ce, La | [19] | |
La | [92] | |
* | Ce | [90] |
* | Ce, La | [19] |
Nd | [93] | |
Ce, Nd | [94] | |
Ce, La | [90] | |
Ce, La | [90] | |
Ce | [90] | |
* | Ce | [90] |
Eu, La, Yb | [95] | |
Eu, La | [96] | |
Eu, Gd, La, Nd, Pr, Sm | [1, 97] | |
Ce, La | [19] | |
Ce | [90] | |
Ce, Eu, La, Yb | [98] | |
14 different Ln, Y | [99] |
Precise data about mechanisms of entry for lanthanides into algae and their accumulation are sparse. Even in higher plants, which are much more researched, cell processes responsible for lanthanide intake have only recently been described [38]. Several studies have shown that lanthanides concentrate in chloroplasts [93, 94, 106, 107, 108]. It was demonstrated that selective deposition of individual lanthanides in chloroplasts or the cytoplasm occurs in the green alga
However, many questions regarding the transfer and accumulation of lanthanides remain unanswered. For example, mechanisms of transport through the complex cell wall of algae or cyanobacteria, and whether they are stored in some specific structures or just loosely in the cytoplasm are unclear. Research into resistant strains or natural hyper-accumulators might bring some answers.
6. Biological applications of lanthanides
In biological systems, lanthanides are applied for different purposes such as growth promoters, fertilizers, water bloom killers, or as detection tools (bioindicators, tracers, and markers). Lanthanides have been proposed as growth stimulators for various animals such as pigs and other livestock [110]. Algae were also used as a feed additive to improve the condition of domestic animals [111]. Lanthanide-rich algae are a potential alternative to food supplements or functional foods. However, only one study on young abalones was performed to demonstrate that lanthanide-enriched algal biomass was an effective growth promoter [82]. Therefore, it would be important to increase the number of studies, to obtain relevant data on the effects of lanthanide transmission and to assess the risk of human exposure through food derived from animals [35].
Many microorganisms, including blue-green algae (e.g.,
The unique chemical features of lanthanides make them ideal tracers for geochemical processes in nature [9]. They represent alternative, nonradioactive, highly detectable labels. They were used, for example, to confirm the impact of cyanobacterial mats on deep waters outside French Polynesia, providing evidence for an end-ascending flow [114]. They enable scientists to follow oceanic cycles, petrogenesis, the chemical evolution of the Earth [16, 29], or palaeo-environmental conditions [115, 116, 117, 118]. Lanthanides can also serve as anthropogenic activity indicators [27]. Because of their particular affinity to algae, the lanthanide profile may be a useful indicator for exploring the ecology of marine environments [10] and can also be used to monitor sources of pollution from natural events such as volcanic activity [25]. In combination with macroalgal sampling, the lanthanide profile may help to characterize coastal water quality and pollution [22, 23, 27].
Lanthanides have been used for their inert nature as detection agents in various experiments, for example, in studies of the rate of passage and digestibility of nutrients in humans and animals [119, 120, 121]. Lanthanide oxides have been used as markers in sea cucumber (
In the development of new, sensitive detection methods, active chelates of lanthanides have been obtained and tested. They are used in sensitive immunoassays to suppress the background [122] or as very sensitive fluorescence probes [123]. An example of their use is the labeling of the cyanotoxin microcystin [124, 125].
7. Remediation of lanthanide waste and their recovery
In countries with sufficient sources of lanthanides (mainly China), these elements are used as fertilizers to increase agricultural production. With increasing consumption, waste with varying contents of different lanthanides has increased significantly and rapidly. The most important of these are magnets (neodymium), metal alloys (europium and yttrium), batteries, glass, and catalysts (cerium and lanthanum) [126]. Other important sources of lanthanide waste are phosphate mineral fertilizers, industrial wastewater, sewage sludge, mining processes, or wastes from industrial aluminum production [4, 18, 26, 27, 28, 29]. Lanthanides present in ecosystems from agricultural production can thus penetrate into the groundwater and migrate to rivers and lakes [58] or to the sea [127]. Some studies on ecological effects and potential threats due to the bioaccumulation of lanthanides have been described, but they are not long-term enough to draw any general conclusions [128, 129]. Relevant regulations or standards concerning doses and threshold values for the presence of lanthanides in the environment have also not been established [38]. In China, lanthanides are cited as the main source of environmental contamination [130]. They are also considered to be emerging pollutants outside of China, requiring the specification of threshold values for concentrations and emissions of lanthanides in the environment [64, 131]. Removing these lanthanide contaminants is therefore a very important requirement in order to reduce the ever-increasing environmental burden on the aquatic environment.
In addition to this very important requirement for remediation, the need for recycling of lanthanides from any (not only liquid) industrial production waste becomes even more acute. One reason is the risk of reduced availability of resources (China owns more than 95% of natural sources) or their relatively rapid depletion from other sources. Replacement of lanthanides with alternate substances in industrial applications is currently not possible [132, 133]. Due to their unique chemical and physical properties and their extensive applications in industrial products, the importance and demand for these elements is constantly increasing [131, 134]. The economic impact of an emerging lanthanide shortage increases the urgency for efficiently using renewable energy sources from the ever increasing number of different types of waste products worldwide. At present, research is focused on the progressive and cost-efficient recycling of lanthanides for industrial processes [4, 95, 102, 135, 136], which would reduce risks associated with inaccessibility or depletion of natural resources while minimizing environmental problems associated with their extraction and processing [137].
One of the most widespread lanthanide-containing wastes is electrical and electronic equipment, including lighting equipment, computers, or photovoltaic panels. This waste is a growing threat to the world’s environment, and lanthanide recovery is therefore becoming economically attractive. The main sources for recycling are luminophores, powder mixtures obtained from electronic waste and containing high concentrations of lanthanides. Luminophores are obtained from television screens or monitors, as well as energy-saving bulbs and lamps, where they are used to convert cathodic tube radiation or ultraviolet electric discharge into mercury vapor and visible light. These luminophores occur as a powder attached to the inner surfaces of mesh or tubes. The glass parts of these waste networks, monitors, screens, and light bulbs can be easily recycled, but luminophore layers must be removed because the luminescent compounds would reduce the quality of recycled glass. The luminophores as waste represent a toxicity problem but, on the other hand, are a concentrated source of various lanthanides, either in the form of dry powder or wet mud [138].
7.1. Chemical recycling
Lanthanides from waste sources can be recycled by chemical separation from solutions (e.g., chemical precipitation, electrochemically, membrane division, reverse osmosis, etc.). These methods are comparatively costly and, moreover, are often a source of other nonorganic wastes [139]. Methods such as pyrometry and hydrometallurgy for the extraction of lanthanides from ores have significant negative impacts on the environment and involve high costs [126]. The other serious disadvantage is the dependence on a single and limited source and possibly the depletion of other natural resources [126, 140, 141]. These traditional physicochemical processes are expensive or even inefficient for the treatment of sewage containing low concentrations of metal ions [142]. A by-product of conventional methods is the associated large volume of contaminated water, high temperatures and a high consumption of chemical compounds [143, 144]. Researchers are therefore looking for low-cost approaches and at the same time environmentally friendly technologies.
7.2. Biosorption
As a biotechnological approach, biosorption is considered to be a more efficient and cheaper alternative to conventional chemical methods of recycling lanthanides [133, 145, 146]. Various different organic residues of animal or plant origin, including resin, activated charcoal, or biomass of various organisms (algae, fungi, and bacteria), have been shown to adsorb different lanthanides and have been tested as biosorbents [95, 98, 132, 147]. The development of effective biological methods for lanthanide regeneration from these materials was proven in the aerobic, genetically modified bacterium,
7.3. Accumulation in living cells
Methods for the recycling of lanthanides via living cells offer an alternative, which does not have the disadvantages of chemical and adsorption approaches. Accumulation of lanthanides from the environment is cost-effective and does not produce any substantial secondary waste. In addition, it is a great advantage that it can also be effective in water containing very low lanthanide concentrations, which is problematic in other approaches.
Waste solutions containing lanthanides often have high acidity. Thus, the discovery that the sulfothermophilic red alga
Up to now, only one paper has been published demonstrating the high potential of seaweed (in this case, brown algae
8. Conclusions
Algae are very important organisms in terms of ecology, being at the very beginning of the food chain. Their relationships with metals therefore affects other living organisms. Their ability to accumulate lanthanides may have an impact on the surrounding environment, representing both a threat and an opportunity, with the potential for further study and use. As bioaccumulation abilities and beneficial or toxic effects of lanthanides differ in individual algal strains, it is difficult to predict specific ecological hazards. Algae in combination with lanthanides offer a wide variety of applications. They can be used as bioindicators, fertilizers, toxin detectors, or for phytoremediation and recycling. Therefore, understanding the relationships between algae and lanthanides is very important. Once we understand the molecular mechanisms of their effects, we will have greater opportunities for their use.
Acknowledgments
We thank Prof. John Brooker for critical reading and language corrections of the manuscript. This work was supported by the National Program of Sustainability I, ID: LO1416.
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