**2. Lanthanides in algae**

The presence of lanthanides (Pr, Nd, and Sm) was recorded for the first time in the red alga *Phymatolithon calcareum*, originally *Lithotamnium calcareum*, near the coast of Roscoff in France [7].

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 [8–11]. 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].

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, 17–19], 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 [22–24]. 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, 26–29]. Algae can serve as bioindicators because they can accumulate

**Treea Teab Mossc Potatod Red algae Brown algaf Green algag**

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The data correspond to mean values established in μg/g dry weight. In bold, the highest values of the series are

**Table 1.** Examples of lanthanides and their concentrations in different plants and locations (according to Goecke et al. [3]).

**Organism Yao et al. [20] Shi et al. [21]** Crustacea 0.15 0.15–0.81 Fish 0.07-0.23 nd Macroalgae **1.30–1.40 0.78–49.10** Mollusks 3.32 0.37–21.60 Zooplankton 0.17 nd

**Table 2.** Lanthanide content in coexisting environmental samples from two studies in China.

Yb 0.008 0.044 0.011 0.001 0.008 **0.290** 0.007 Lu 0.019 0.007 0.001 0.000 0.001 **0.020** 0.001 **Total 1.034 2.945 1.489 0.117 1.704 22.460 0.239**

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

these elements in their cells (**Table 1**).

highlighted.

Samples of *Pinus silvestris* (pine needles), Germany [12].

Macroalgae in bold and values in μg/g dry weight [20, 21].

*Hylocomium splendens*, Sweden [14]. <sup>d</sup>*Solanum* sp. from a food market, China [15].

Red alga *Grateloupia filicina*, Japan [10].

Brown alga *Padina* sp., Malaysia [11].

Green alga *Codium fragile*, Japan [9].

Certified reference material GBW07605 tea leaves, China [13].

a

b

c

e

f

g

**3. Beneficial effects of lanthanides**



The data correspond to mean values established in μg/g dry weight. In bold, the highest values of the series are highlighted.

a Samples of *Pinus silvestris* (pine needles), Germany [12].

b Certified reference material GBW07605 tea leaves, China [13].

c *Hylocomium splendens*, Sweden [14].

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.

The presence of lanthanides (Pr, Nd, and Sm) was recorded for the first time in the red alga *Phymatolithon calcareum*, originally *Lithotamnium calcareum*, near the coast of Roscoff in France [7]. 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 [8–11]. These analyses show that seaweed lanthanide concentrations may be 10–20 times higher than those in terrestrial plants

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, 17–19],

**Treea Teab Mossc Potatod Red algae Brown algaf Green algag**

([8], see **Table 1**) and more than 100 times higher than in sea water [10, 16].

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 **3.990** 0.032 Ce 0.370 1.000 0.493 0.038 0.943 **9.080** 0.076 Pr 0.091 0.120 0.056 0.007 0.049 **0.910** 0.008 Nd 0.155 0.440 0.402 0.015 0.191 **4.910** 0.039 Sm 0.031 0.085 0.036 0.008 0.034 **0.900** 0.009 Eu 0.004 0.018 0.009 0.001 0.008 **0.090** 0.028 Gd 0.024 0.093 0.037 0.007 0.044 **1.020** 0.012 Tb 0.017 nd 0.005 0.001 0.006 **0.090** 0.001 Dy 0.021 0.074 0.024 0.002 0.030 **0.710** 0.012 Ho 0.004 0.019 0.004 0.000 0.006 **0.090** 0.002 Er 0.006 — 0.013 0.002 0.015 **0.350** 0.008 Tm 0.001 — 0.001 0.000 0.002 **0.020** 0.001

**2. Lanthanides in algae**

88 Lanthanides

and links therein).

<sup>d</sup>*Solanum* sp. from a food market, China [15].

e Red alga *Grateloupia filicina*, Japan [10].

f Brown alga *Padina* sp., Malaysia [11].

g Green alga *Codium fragile*, Japan [9].

**Table 1.** Examples of lanthanides and their concentrations in different plants and locations (according to Goecke et al. [3]).


**Table 2.** Lanthanide content in coexisting environmental samples from two studies in China.

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 [22–24].

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, 26–29]. 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.

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, 39–42]. 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, 54–56], 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

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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 *Chara corallina*, thereby enabling cytoplasmic streaming. Lanthanides can also induce a stimulating effect on the green microalga *Desmodesmus quadricauda* [2]. Five additions of different lanthanides, added at low concentrations, partially compensated the adverse effect of a Ca2+ deficiency (probably by substitution), but were not able to alleviate a Mn2+ deficiency. To specifically measure physiological stress caused by nutrient limitation, a decline in cellular growth and cell division was followed and a pulse amplitude modulation (PAM) fluorimeter was used to detect changes in photosynthetic parameters (**Figure 1**).

**Figure 1.** Photosynthetic parameters expressed as maximum relative electron transport rates (rETRmax), and the maximal quantum yield (*Fv/Fm*), in cultures of the alga *Desmodesmus quadricauda,* grown either in complete mineral medium (Ctrl, *red* symbols, *dashed* curve) or in calcium-deficient mineral medium (Def, *blue* symbols, *dashed* curves). To calcium-deficient cultures, either complete mineral medium (Rec, *black* symbols, *solid* line) or different lanthanides (Ce, Eu, Gd, La, Nd) were added, as marked in individual panels. Complete photosynthetic parameters are displayed in the

original publication (modified from Goecke et al. [2]).

their ability to neutralize inhibitory effects of heavy metals [37].

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, 33–35]. 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


Algal divisions are characterized as Chlorophyta (C), Haptophyta (H), and Ochrophyta (O); Cyanobacteria (B) and Euglenophyta (E). If the algal species has a new name, it is referred to using the actual name and an asterisk (\*); for names according to Algaebase, see Guiry et al. [53].

**Table 3.** Examples of studies testing the effect of lanthanides on growth, physiology, and survival of microalgae, specifying the concentrations at which positive, neutral, and negative effects were observed (values in μmol/L).

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, 39–42].

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 mem-

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, 33–35]. 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

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

**Algae Lanthanide Positive effect Negative effect Reference** *Arthrospira platensis* (B) La3+ 38.53–53 >53.94 [43] \**Arthrospira platensis* (B) LaCl<sup>3</sup> 30–40 >40 [44] *Chlamydomonas reinhardtii* (C) Ce<sup>3</sup> 5–20 — [45]

*Chlorella vulgaris* (C) Ce3+ 1.8 2.1 [46] \**Ch. vulgaris* v. *autotrophica* (C) 12 different Ln — 29.14 [47] \**Desmodesmus quadricauda* (C) La3+ <7.2 >72 [48] *Euglena gracilis* (E) Dy3+ 50–100 180–1000 [49] *Isochrysis galbana* (H) La 7.28–87.4 — [50, 51]

*Microcystis aeruginosa* (B) La3+ <7.2 >72 [48] *Skeletonema costatum* (O) 13 different Ln — 28–30 [52]

Algal divisions are characterized as Chlorophyta (C), Haptophyta (H), and Ochrophyta (O); Cyanobacteria (B) and Euglenophyta (E). If the algal species has a new name, it is referred to using the actual name and an asterisk (\*); for names

**Table 3.** Examples of studies testing the effect of lanthanides on growth, physiology, and survival of microalgae, specifying the concentrations at which positive, neutral, and negative effects were observed (values in μmol/L).

La3+ 5–20 — [45]

Gd 6.36–57.23 — [50, 51] Yb 5.78–17.34 — [50, 51]

Sc — 21.88 [52] Y — 43.21 [52]

brane permeability and the cellular ion ratio.

algae remain unclear [38].

90 Lanthanides

according to Algaebase, see Guiry et al. [53].

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, 54–56], 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].

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 *Chara corallina*, thereby enabling cytoplasmic streaming. Lanthanides can also induce a stimulating effect on the green microalga *Desmodesmus quadricauda* [2]. Five additions of different lanthanides, added at low concentrations, partially compensated the adverse effect of a Ca2+ deficiency (probably by substitution), but were not able to alleviate a Mn2+ deficiency. To specifically measure physiological stress caused by nutrient limitation, a decline in cellular growth and cell division was followed and a pulse amplitude modulation (PAM) fluorimeter was used to detect changes in photosynthetic parameters (**Figure 1**).

**Figure 1.** Photosynthetic parameters expressed as maximum relative electron transport rates (rETRmax), and the maximal quantum yield (*Fv/Fm*), in cultures of the alga *Desmodesmus quadricauda,* grown either in complete mineral medium (Ctrl, *red* symbols, *dashed* curve) or in calcium-deficient mineral medium (Def, *blue* symbols, *dashed* curves). To calcium-deficient cultures, either complete mineral medium (Rec, *black* symbols, *solid* line) or different lanthanides (Ce, Eu, Gd, La, Nd) were added, as marked in individual panels. Complete photosynthetic parameters are displayed in the original publication (modified from Goecke et al. [2]).

The effects of single lanthanides and monazite on growth rate, lipid profile, and pigments in two biotechnologically interesting algae (*Parachlorella kessleri* and *Trachydiscus minutus*) were evaluated. The impact of lanthanides depended on the combination of species, element, and light intensity. For example, the presence of Ce, La, and Sc caused the growth rate of *T. minutus* to rapidly rise at low light intensity. The saturated fatty acid content increased at the expense of polyunsaturated fatty acids in both species. The effect on pigments was variable [60].

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

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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,"

Algal divisions Chlorophyta (C), Ochrophyta (O), and Rhodophyta (R), and Cyanobacteria (B), and the protist classes Dinophyceae (D) and Euglenophyceae (E) are specified. If microalgae were utilized, they are annotated with an (m). If an algal species has a new name, it is referred to with the actual name and an asterisk (\*); names are according to Algaebase,

**Table 4.** Studies on algal accumulation, biosorption and/or desorption of lanthanides.

**Algae Lanthanide Reference** \**Amphidinium carterae* (D)m Ce [90] *Aphanothece sacrum* (C)m 14 different Ln, Y [91] *Carteria* sp. (C)m Ce [90] *Chaetoceros muelleri* (O)m Ce, La [19] *Chlorella vulgaris* (C)m La [92] \**Cylindrotheca closterium* (O)m Ce [90] \**Diacronema lutheri* (C)m Ce, La [19] *Euglena gracilis* (E)m Nd [93] *Euglena gracilis* (E)m Ce, Nd [94] *Microcystis aeruginosa* (B)m Ce, La [90] *Nannochloropsis gaditana* (C)m Ce, La [90] *Platymonas* sp. (C)m Ce [90] \**Porphyridium purpureum* (R)m Ce [90] *Sargassum polycystum* (O) Eu, La, Yb [95] *Sargassum polycystum* (O) Eu, La [96] *Sargassum* sp. (O) Eu, Gd, La, Nd, Pr, Sm [1, 97] *Tetraselmis chui* (C)m Ce, La [19] *Thalassiosira* sp. (O)m Ce [90] *Turbinaria conoides* (O) Ce, Eu, La, Yb [98] *Ulva lactuca* (C) 14 different Ln, Y [99]

on the environment.

see Guiry et al. [53].

**5. Bioaccumulation of metals in 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 *Haematococcus pluvialis*, cellular growth and production of astaxanthin increased after the addition of Ce3+ at a concentration of 1 mg/L. However, this effect was dose-dependent and growth at higher concentrations of Ce3+ was inhibited [61].
