Effects of manufactured nanomaterials on algae: Implications and applications

Abstract

● Summary of positive and negative effects of MNMs on algae.

● MNMs adversely affect algal gene expression, metabolite, and growth.

● MNMs induce oxidative stress, mechanical damage and light-shielding effects on algae.

● MNMs can promote production of bioactive substances and environmental remediation.

The wide application of manufactured nanomaterials (MNMs) has resulted in the inevitable release of MNMs into the aquatic environment along their life cycle. As the primary producer in aquatic ecosystems, algae play a critical role in maintaining the balance of ecosystems’ energy flow, material circulation and information transmission. Thus, thoroughly understanding the biological effects of MNMs on algae as well as the underlying mechanisms is of vital importance. We conducted a comprehensive review on both positive and negative effects of MNMs on algae and thoroughly discussed the underlying mechanisms. In general, exposure to MNMs may adversely affect algae’s gene expression, metabolites, photosynthesis, nitrogen fixation and growth rate. The major mechanisms of MNMs-induced inhibition are attributed to oxidative stress, mechanical damages, released metal ions and light-shielding effects. Meanwhile, the rational application of MNMs-algae interactions would promote valuable bioactive substances production as well as control biological and chemical pollutants. Our review could provide a better understanding of the biological effects of MNMs on algae and narrow the knowledge gaps on the underlying mechanisms. It would shed light on the investigation of environmental implications and applications of MNMs-algae interactions and meet the increasing demand for sustainable nanotechnology development.

Graphical abstract

Keywords

Manufactured nanomaterials / Algae / Mechanisms / Effects / Implications / Applications

1 Introduction

Manufactured nanomaterials (MNMs) refer to materials with a critical dimension of less than 100 nm on at least one geometric surface and high homogeneity, particularly manufactured products for application purposes, which are different from natural nanomaterials (e.g., protein molecules, viral particles, raw magnetite and ultrafine particles) (Lopez-Alonso et al., 2020). Based on the composition, MNMs can be divided into carbonaceous MNMs, metal/metal oxide MNMs, quantum dots and organic polymers (Haque and Ward, 2018). MNMs display unique physical and chemical properties at the nanoscale, such as high surface area, nanoscale size effects and quantum effects, etc. Given these unique properties, nanomaterials have been widely used in diverse applications, including agriculture, electronics, aerogels, aerospace, automotive, medicine, cosmetics and textiles (Zhang et al., 2020; Jiang et al., 2022). MNMs are estimated to be components of more than 2,000 commercial products, and this number is expected to grow significantly in the forthcoming years (Wang et al., 2021a). However, during the production, transportation, use and disposal of these products, MNMs are inevitably released into the environment (Keller et al., 2013).

The aquatic environment is the ultimate destination of almost all pollutants, including MNMs (Zhang et al., 2018a). MNMs can enter the aquatic environment through industrial wastewater, domestic sewage, and coastal recreation actives (e.g., swimming, diving) (Cedervall et al., 2012; Yue et al., 2017; Huang et al., 2021). In addition, MNMs are widely used to treat groundwater and other water bodies, which would be inevitably left in the water environment (Zhang and Elliott, 2006; Yang et al., 2021). Taking the global production of about 309000 tons of MNMs in 2010 as an example, it is estimated that 0.4%–7% of the nano-products eventually enter the water environment (Keller et al., 2013). The risk of MNMs to the aquatic ecosystem has been an increasing concern (Haque and Ward, 2018).

Algae is the primary producer in aquatic ecosystems, as it could produce oxygen for aquatic organisms via photosynthesis. In addition, algae are the key fundamental part of the food chain as they would generate organic carbon and biomass to supply as food sources for the aquatic ecosystems. Thus, the change of algal species composition and community structure would directly affect the aquatic ecosystems’ energy flow, material circulation and information transmission, which plays an essential role in maintaining the balance of aquatic ecosystems (Rai et al., 2016; Li et al., 2020b; Grigoriev et al., 2021). Numerous studies have demonstrated that the exposure of MNMs induces adverse biological effects onto algae, which may further affect algae’s gene expression, metabolism, photosynthesis, nitrogen fixation, and growth (Chen et al., 2019). Hence, investigations into the MNMs’ effects on algae as well as the underlying mechanisms are critical in the ecological risk evaluation of MNMs. On the other hand, the biological interaction between MNMs and algae as well as the consequential effects may exhibit beneficial applications (e.g., hazard remediation (Guleri et al., 2020; Mohsenpour et al., 2021)), biomass production (Kartik et al., 2021), which has been overlooked in the previous reviews. Therefore, the current review aims to provide a full picture of the biological effects of MNMs on algae, including both negative implications and positive applications, which would provide a better understanding of mechanisms of MNMs’ biological effects and help to meet the increasing demand in the sustainable development of nanotechnology.

2 Effects of MNMs on algae

MNMs would induce adverse biological effects onto algae, affecting algae’s gene expression, metabolism, photosynthesis, nitrogen fixation, and growth.

2.1 MNMs affect algae’s gene expression

MNMs induce biological effects onto algae’s gene expression, particularly, the gene expression related to antioxidant synthesis, lipid synthesis, cell division and photosynthesis (Fig. 1). Middepogu et al. reported that nano-TiO₂ disrupted material and energy metabolisms in algal photosynthesis at the molecular level (Middepogu et al., 2018). The expression of genes related to lipid synthesis (gdat), carbohydrate synthesis (cah2) and cell division (tdsH) were all down-regulated, indicating that nano-TiO₂ suppressed the lipid and carbohydrate biosynthesis and cell division at the gene expression level. Similar results were reported in the Chlorella pyrenoidosa’s gene expression change to oxidized multi-walled carbon nanotubes (o-MWCNTs), as remarkable down-regulated were observed on the algal carbon fixation and photosynthesis-related genes (e.g., CAH2 and rbcL) (Zhang et al., 2018b).

Furthermore, advances in “omics” technologies (e.g., transcriptomics, proteomics and metabolomics) facilitate the comprehensive analysis of stressor effects at subcellular levels (Lauritano et al., 2019; Balbi et al., 2021). Particularly, transcriptomics and proteomics could provide a better understanding of the stress effects and mechanisms of toxic action by analyzing the expression of genes and proteins within an organism. Pillai et al. investigated the effects of nano-Ag onto Chlamydomonas reinhardtii at the transcriptome and proteome levels, revealing an oxidative stress response at subcellular levels, even though no lipid peroxidation was observed at the biochemical level (Pillai et al., 2014).

2.2 MNMs affect algae’s metabolism

As shown in Fig. 1, MNMs would affect the metabolic processes of algal cells by causing oxidative stress in algae, affecting the activity of enzymes involved in metabolic processes, or affecting the expression of related genes, which would further induce the changes in levels or concentrations of macromolecules and metabolites (e.g., lipids, fatty acids, carotenoids, amino acids, polysaccharides) as well as the ratio of carbon, nitrogen and phosphorous in algal cells (Manier et al., 2013; Cherchi et al., 2015; Li et al., 2015a; Praveenkumar et al., 2015; Rhiem et al., 2015; Li et al., 2016; Zhang et al., 2016b). Cherchi et al. reported changes in Cyanobacteria Anabaena’s intracellular C:N, C:P and N:P stoichiometries after exposure to nano-TiO₂ at varying dose concentrations (0–1 mg/L) and exposure duration (96 h–21 d) (Cherchi et al., 2015). Notably, the relative ratio of amide II, lipids, nucleic acids and carbohydrates to the cellular protein content (quantified as amide I stretch) changed significantly within the initial 96 h exposure.

Similar to transcriptome and proteomics, metabolomics is also helpful to evaluate the effects of nanomaterials on algae at the molecular level, and has been gradually applied in the field of ecotoxicology (Huang et al., 2018; Huang et al., 2019; Grigoriev et al., 2021). Taylor et al. investigated the potential toxicity of tightly constrained nano-CeO₂ to the unicellular green algae by using the metabolomics approach (Taylor et al., 2016). According to principal components analysis (PCA) of the mass spectrometry-based metabolomics data, there was a significant perturbation of metabolic function within the algal cells when exposed to nano-CeO₂ at supra-environmental concentrations.

2.3 MNMs affect algae’s photosynthesis and nitrogen fixation

Photosynthesis activity is an important indicator for evaluating the MNMs’ effects on algae. Chlorophyll content, the maximal electron transport rate (ETR_max) and primary light energy conversion efficiency of photosystem II (PSII) have been widely used as indicators of the external stressor’s effects on the algal photosystem (Pillai et al., 2014; Masojidek et al., 2021). Several studies have shown that a higher concentration of MNMs ( > 10 mg/L) can inhibit photosynthesis of algae by reducing chlorophyll content or affecting photoelectron transfer (Saison et al., 2010; Wei et al., 2010a; Sadiq et al., 2011a; Oukarroum et al., 2012; Pillai et al., 2014). Saison et al. investigated the change of Chlamydomonas reinhardtii’s PSII after exposure to nano-CuO, and reported that both the content of chlorophyll and PSII electron transport rate significantly decreased, indicating strong inhibition of the PSII photochemistry (Saison et al., 2010). Likewise, it was reported that contents of chlorophyll decreased in Haematococcus pluvialis after the exposure to nano-Cu (Babazadeh et al., 2021).

Though most studies have demonstrated that MNMs could inhibit the photosynthesis of algae, there are exceptions. Some studies have found that MNMs can enhance photosynthetic performance of microalgae (Rodea-Palomares et al., 2012; Serag et al., 2013; Giraldo et al., 2014; Xu et al., 2018). Rodea-Palomares et al. reported that low concentrations (0.01–0.1 mg/L) of nano-CeO₂ increased the photosynthetic electron transport and chlorophyll a content in the freshwater alga Pseudokirchneriella subcapitata (Rodea-Palomares et al., 2012). Similarly, carbon nanotubes (CNTs) exhibited high efficiency in light energy capture, owing to the broader absorption spectrum than the chloroplast antenna pigments (Hagen and Hertel, 2003). It has been reported that CNTs could promote photosynthetic electron transport both ex vivo and in vivo (Lambreva et al., 2015) and increase photosynthetic activity (Giraldo et al., 2014). The underlying mechanisms of MNMs’ positive effects on the photosynthetic activity might attribute to their widened spectral region for energy capturing (Lambreva et al., 2015) and higher chlorophyll content under the MNMs-induced stress (Chen and Smith, 2012). However, the presence of MNMs even at low concentrations ( < 0.1 mg/L) would induce oxidative stress to algal organisms (Rodea-Palomares et al., 2012), which would further cause lipid peroxidation and cell death. In addition, to long-term effect of algae exposed to MNMs should be thoroughly studied to maximize the positive contribution of MNMs to algal photosynthetic performance and biomass accumulation (Giraldo et al., 2014).

In addition to affecting photosynthesis, MNMs would affect the algal nitrogen fixation ability (Cherchi and Gu, 2010; Kumar et al., 2016). After exposure to nano-TiO₂, both the occurrence and intracellular levels of the nitrogen-rich cyanophycin grana proteins (CGPs) in cyanobacteria Anabaena variabilis increased with the increasing concentration and time of nano-TiO₂ exposure, indicating inhabitation in nitrogen fixation activity (Cherchi and Gu, 2010). Likewise, it was reported that nano-hexaconazole, a nanoscale polymer carrier for pesticides, caused inhibition in blue-green algae’s activity of nitrogen assimilating enzymes (Kumar et al., 2016). On the other hand, the biological effects of MNMs to algae also vary under different nitrogen conditions. For example, the exposure to nano-TiO₂ under replete nitrogen conditions would decrease the growth and biomass of Chlorella vulgaris, while the exposure to nano-TiO₂ under limited nitrogen would lead to a more severe drop of the algal growth and biomass (Dauda et al., 2017). MNMs would induce negative effects on algal nutrient cycling and nitrogen fixation, which deserves more in-depth investigation.

2.4 MNMs affect algae’s growth

As discussed above, the exposure to MNMs would affect algae’s gene expression, metabolism, photosynthesis, and nitrogen fixation, which would eventually affect the growth of algal cells (Wang et al., 2011; Hazani et al., 2013; Nogueira et al., 2015; Sohn et al., 2015). We have summarized the adverse effects and mechanisms of MNMs on algae in Table 1. Generally, the inhibition of algae growth by MNMs is usually evaluated by the median effective concentration (EC₅₀), which may vary significantly with the MNMs type, exposure time or concentration, testing organisms, and algae age. For instance, the EC₅₀ of metal quantum dots (QDs) was significantly higher than that of carbon QDs on Chlorella pyrenoidosa (Xiao et al., 2016). Besides, EC₅₀ of MNMs on “mid-age” algae is usually lower than that of “young” and “old” algae (Metzler et al., 2011). Metzler et al. studied the effect of nano-TiO₂ on Pseudokirchneriella subcapitata and reported that as the algal age increased, there was an increase in EC₅₀ from that in 3–5 d algae to 8-d algae, but a decrease of EC₅₀ in 12–14 d algae (Metzler et al., 2011). Moreover, EC₅₀ usually increases with exposure time. For example, EC₅₀ of nano-TiO₂ inhibiting Chlamydomonas reinhardtii growth was 10 and 100 mg/L for 3-d and 10-d exposure, respectively (Gunawan et al., 2013).

In general, the higher exposure concentration of MNMs would induce stronger inhibition of algae growth (Schwab et al., 2011; Sohn et al., 2015). Wei (Wei et al., 2014) et al. reported that the growth inhibition of Scenedesmus obliquus were 6.27%, 11.2%, and 20.7% after 96-h exposure of 50, 100, 200 mg/L nano-SiO₂. Meanwhile, low-dosage MNMs exposure may also suppress algae growth, for example, the growth of Chlorella kessleri was hindered by up to 91.9% after the exposure to 26.7 mg/L C₆₀ fullerene, which was only 70.2% when exposed to 40 mg/L C₆₀ fullerene (Kubatova et al., 2013).

On the other hand, the exposure to low concentrations of MNMs may promote the growth of algae (Sohn et al., 2015; Tyne et al., 2015; Chen et al., 2019; Vargas-Estrada et al., 2020). For instance, Sohn et al. reported that the biomass of Raphidocelis subcapitata was elevated 1.47 times after 72-hour exposure of 12 mg/L single-walled carbon nanotubes (SWCNTs), which was attributed to hormesis (Sohn et al., 2015).

3 Mechanisms of MNMs’ effect on algae

MNMs affect algae mainly by inducing mechanical damage and light-shielding effects in algae as well as releasing metal ions in water, and which could directly or indirectly induce oxidative stress in algae.

3.1 Mechanical damage

Owing to MNMs’ high surface/interface potential, strong interaction between MNMs and algal cells (e.g., MNMs being adsorbed on the surface of algal cells, encapsulated algal cells) would induce mechanical damages (e.g., MNMs penetrate algal cells with a sharp edge and corner) (Chen et al., 2015; Zhang et al., 2016a; Zhao et al., 2017; Middepogu et al., 2018). Two-dimension MNMs, for example, reduced graphene oxide (rGO) and multi-layer graphene (MG) were reported to destroy membrane integrity of Chlorella pyrenoidosa, due to the direct contact of the edges of rGO and MG with algal cells (Zhao et al., 2017).

Moreover, MNMs were reported to enter the algal cells and destroy the subcellular structure (Dalai et al., 2013; Manier et al., 2013; Li et al., 2015a; Zhang et al., 2016a; Wang et al., 2021b). Iswarya et al. assessed the damage of anatase and rutile nano-TiO₂ to the membrane and subcellular structures of Chlorella vulgaris, and suggested that anatase nano-TiO₂ would damage algal cells’ nucleus and cell membrane while rutile nano-TiO₂ would cause chloroplast and internal organelle damages (Iswarya et al., 2015). However, it is not always the case that MNMs would enter the algal cells, for instance, QDs were observed adsorbed on the surface of Phaeodactylum tricornutum and Dunaliella salinaonly, while no QDs were observed inside the algal cells (Morelli et al., 2013).

3.2 MNMs induced light-shielding effect

The interactions between MNMs and algal cells (e.g., heteroaggregation) may result in the attachment to the surface of the algal cells to absorb or block part of the light, inducing a light-shielding effect. The light-shielding effect of MNMs would further affect the photosynthesis of algae, which directly or indirectly affects the growth and reproduction of algae (Schwab et al., 2011; Hazeem et al., 2020; Thiagarajan et al., 2021; Wang et al., 2021b). Sadiq et al. reported that the existence of nano-Al₂O₃ had a certain light-shielding effect on Scenedesmus sp. and Chlorella sp., inhibiting the synthesis of photosynthetic pigments and thus suppressing algae growth (Sadiq et al., 2011b). Similarly, graphene oxide (GO) was reported to exhibit a light-shielding effect onto Chlorella vulgaris (Zhao et al., 2016), while CNT was also demonstrated to inhibit the growth of Chlorella vulgaris due to the light-shielding effect (Schwab et al., 2011).

However, there have been debates on the role of the light-shielding effect in MNMs induced toxicity (Saison et al., 2010; Wang et al., 2011). Aruoja et al. found no significant growth inhibition when using nano-TiO₂ to block the light source (Aruoja et al., 2009). Likewise, the light-shielding effect was not observed in the toxicity study of nano-TiO₂ on Scenedesmus obliquus (Li et al., 2020a). The MNMs induced shading effects may depend on the properties of MNMs, for example, the black flake-like MNMs (e.g., GO) may have a stronger light-shielding effect.

3.3 MNMs released metal ions

Metal-containing MNMs, especially nano-Ag, nano-ZnO, nano-PbS, nano-Cu₂O, etc., would gradually release metal ions along the environmental process (Gunasekaran et al., 2020; Ahmed et al., 2021; Kong et al., 2021; Xiong et al., 2021b), which may also induce biological effects to algae. Particularly, some researchers suggested that the toxicity of MNMs to algae is dominated by MNMs-induce dissolved metal ions (Franklin et al., 2007; Wong et al., 2010). Franklin et al. reported that the toxicity of nano-ZnO to Pseudokirchneriella subcapitata was statistically similar to that of ZnCl₂, suggesting Zn²⁺ released by the dissolution of nano-ZnO lead to the major toxic effect (Franklin et al., 2007). Likewise, Li et al. reported less toxicity on alga Euglena gracilis exposed to nano-Ag, compared to AgNO₃ (Li et al., 2015b). The proteinaceous pellicle of algae could effectively inhibit the uptake of MNMs, while the dissolved ions could mitigate into algal cells and induce biological effects (e.g., suppress the photosynthetic yield).

On the contrary, compared to the released metal ions, some researchers considered the role of MNMs is more critical in causing the biological effects onto algae (Navarro et al., 2008; Manzo et al., 2013). Manzo et al. reported that nano-ZnO induced significantly higher than that of bulk ZnO, though similar amount of Zn²⁺ was detected in both exposures, demonstrating the critical role of MNMs in the toxicity effect on algae (Manzo et al., 2013). Similarly, it’s reported that nano-ZnO exhibited higher toxicity to green algae Chlorella sp compared to the bulk-ZnO and Zn²⁺, which was attributed to the fact that nano-ZnO entrapped and wrapped the algal cells and may contribute to the algal growth inhibition (Ji et al., 2011). Thus, the MNMs released metal ions should not be considered as the sole reason for MNMs’ negative effects to algae, while the “nano-effect” of MNMs (e.g., light-shielding effect, mechanical damage) might be dominant contributors (Chen et al., 2019).

3.4 MNMs induced ROS generation

Oxidative stress has been widely considered as one of the dominant mechanisms in the toxic effect of MNMs on algae (Xiao et al., 2016; Santschi et al., 2017; Chen et al., 2019). MNMs have unique physicochemical properties (e.g., photocatalytic, oxidative capability), which may trigger reactive oxygen species (ROS) formation in algal cells via direct and indirect chemical reactions (Ouabadi et al., 2013; von Moos and Slaveykova, 2014).

Generally, the intracellular ROS could be generated via directly contact-mediated approach, or indirectly through dissolved ions. The direct MNMs-mitochondria contacts could compromise the organelle membrane integrity, which would release of Ca²⁺ ions from interior stores and further activate the ROS-generating Ca²⁺/calmodulin-dependent enzymes (Santschi et al., 2017). Additional direct pathways may associate with the interactions between MNMs and membrane-bound enzymes to trigger ROS formation (Navarro et al., 2008). Meanwhile, the indirect pathways are involved in the interactions between algae and leached MNM constituents such as metals and organics, which further engage in redox cycling that yield ROS (e.g., H₂O₂, O²⁻·, OH·) production (Ouabadi et al., 2013). Studies have revealed that the amount of MNMs generated ROS exhibited linear correlations with their toxicity to biological organisms (Li et al., 2012). For example, the exposure of nano-Ag had increased the ROS generation in Chlorella vulgaris, and resulted in stronger toxic effects (Hazeem et al., 2019). The exceeded intracellular ROS would engage in unrestricted oxidation of biological molecules and cellular components (e.g., lipid peroxidation), and eventually result in losing cell function and apoptosis (Rocha et al., 2015; Glomstad et al., 2016; Liu et al., 2018).

4 Implications and applications of MNMs’ on algae

The effects of MNMs on algae could be either positive or negative, as posing ecological risks (e.g., intracellular biochemical composition change, metabolism alteration, nitrogen-fixation inhibition, photosynthesis suppression, growth reduction) and potential applications (e.g., enhanced production of valuable bioactive substances, control of biological and chemical pollutants).

4.1 Implications of MNMs on algae

As discussed above, MNMs would induce manifold biological effects on algae, including intracellular biochemical composition change, metabolism alteration, nitrogen-fixation inhibition, photosynthesis suppression, and growth reduction. Due to the long-term exposure of MNMs at environmentally relevant concentrations, the alteration of algae’s photosynthesis, nitrogen fixation and the ratio of C, N, P may further influence the general biogeochemical processes (e.g., carbon and nitrogen cycling) (Cherchi and Gu, 2010; Cherchi et al., 2015). Furthermore, MNMs-engaged biomass change of algae would break the balance of interspecies equilibriums and community dynamics in aquatic ecosystems (Oukarroum et al., 2012; Cherchi et al., 2015).

On the other hand, as the major primary producers in aquatic ecosystems, algae may promote the bioaccumulation of MNMs via the food chain due to the algae-MNMs interaction (e.g., adsorption, internalization) (Rhiem et al., 2015; Xin et al., 2021). It has been proved that MNMs can be transferred from low to high trophic levels along the food chain, and further accumulated in high trophic organisms (Zhao and Wang, 2010; Campos et al., 2013; Bhuvaneshwari et al., 2018). For example, Bouldin et al. fed Ceriodaphnia dubia with CdSe QDs exposed Pseudokirchneriella subcapitata, and found the existence of CdSe QDs in the Ceriodaphnia dubia (Bouldin et al., 2008). In addition, studies have shown that the bio-enrichment of MNMs via the food web is significantly greater than that through water (Zhao and Wang, 2010; Campos et al., 2013). It’s reported that more than 70% of nano-Ag accumulated in the Daphnia magna was through ingestion of algae (Zhao and Wang, 2010). The trophic transfer, bioaccumulation and bio-enrichment of MNMs via the food web would eventually pose a great threat to the ecosystem and public health.

4.2 Applications of MNMs’ effect on algae

4.2.1 Enhance the production of valuable bioactive substances

As shown in Fig. 2, algae could produce a variety of bioactive substances (e.g., fatty acids, steroids, carotenoids, polysaccharides, lectins, mycoplasma-like amino acids, halogenated compounds) through different metabolic pathways (Almendinger et al., 2021), which also serves as the adaption to the environmental change. As discussed above, the exposure of MNMs would alter the metabolism of algae, which may tune certain metabolic pathways to enhance the production of valuable bioactive substances. As a high-value antioxidant, astaxanthin (AXT) has been widely used in cosmetics, health care products, medical and other industries (Du et al., 2021). AXT could be produced by Haematococcus pluvialis, however, the yield is very limited. Recently, nano-Au was innovatively used to stimulate Haematococcus pluvialis to produce AXT at a single cell level, providing a successful MNMs-enhanced biorefinery process (Praveenkumar et al., 2015).

On the other hand, algae is considered as a unique feedstock to produce biofuel (Saber et al., 2016; Yap et al., 2021), while the efficiency and cost-reduction of the cultivation and harvesting steps remain key obstacles (Jones and Mayfieldt, 2012; Kim et al., 2013; Fazal et al., 2021). Due to the MNMs-algae interactions, the biofuel production could be promoted via the induction of intracellular lipid accumulation by nutrient competition and/or stress environments (Farooq et al., 2016; Kim et al., 2016; Liu et al., 2016; He et al., 2017), enhancement of cell growth and/or pigment by light scattering (Torkamani et al., 2010; Pattarkine and Pattarkine, 2012; Eroglu et al., 2013), increased cell separation efficiency and processing time in culture media (Borlido et al., 2013; Hu et al., 2013), and integrated one-pot harvest/cell division (Lee et al., 2014).

4.2.2 Control of biological pollutants

Though algae are an important part of the ecosystem, however, they would also generate biological pollutants (e.g., eutrophication and biofouling). Since MNMs could inhibit the growth of algal cells, which would be beneficial to control eutrophication or inhibit biofouling (Fig. 2).

Due to the excellent aggregation and sedimentation properties in aqueous suspension (Hartmann et al., 2010; Campos et al., 2013; Chowdhury et al., 2013) as well as photocatalytic potential (Metzler et al., 2012), MNMs have been increasingly used to eliminate the bloom algae via surface-mediated reactions and adsorption (Wang et al., 2015; da Silva et al., 2016). Particularly, nano-TiO₂ and iron-containing MNMs are considered the most effective MNMs for the control of red tide algae (Wang et al., 2015; da Silva et al., 2016; Fan et al., 2018; Song et al., 2021). However, MNMs may also adversely affect other species in the ecosystem when treating algae bloom. Da Silva et al. investigated the performance of nano-TiO₂ on remediating eutrophic waters under a microcosm experiment, and had eliminated the algal blooms (da Silva et al., 2016). Meanwhile, Silva et al. also reported that Daphnia magna, Lemna minor and Chironomus riparius exhibited significant inhibition, suggesting more attention should be paid to assessing the potential impact of MNMs on the entire ecosystem.

Moreover, studies have revealed that the engagement of MNMs (e.g., nano-TiO₂, nano-CuO, nano-Ag) could effectively control the biofouling induced by algae (Fonseca et al., 2010; Graziani et al., 2013; Verma et al., 2014). Biofilms would form along with the algal colonization, causing the biofouling on the surface of marine vessels and infrastructure (e.g., bridge), which may further induce decay and damage to materials (Scheerer et al., 2009).

4.2.3 Enhanced remediation of chemical pollutants

Algal photolysis has been proved as a promising alternative way to remove aquatic environmental contaminants (Wang et al., 2017; Samara Sanchez-Sandoval et al., 2021; Xiong et al., 2021a), which can produce photogenerated reactive radicals to accelerate the degradation of pollutants (Sun et al., 2020; Premnath et al., 2021; Wei et al., 2021). Similarly, photocatalytic MNMs have been widely applied for environmental remediation (Tan et al., 2020; Chen et al., 2021; Ding et al., 2021). Thus, the remediation efficiency could be significantly enhanced via the synergistic effect by combining MNMs and algae (Cai et al., 2017; Wang et al., 2017; Chen et al., 2018; Jing et al., 2018; Chang and Wu, 2019).

Researchers have fixed the MNMs together with algal cells on engineered templates (e.g., fibers mat) to promote the degradation of pollutants. For example, algae-TiO₂/Ag bio-nano hybrid material was developed by loading algal cells on the ultrafine TiO₂/Ag chitosan hybrid nanofiber mat, which has significantly improved the photo-removal of Cr(VI) under visible light irradiation (Wang et al., 2017). The organic substances released by algae could consume photo-excited holes and ·OH efficiently, which attenuated the electron-hole recombination and enhanced the photocatalytic reduction of Cr(VI) on TiO₂. Meanwhile, the release of intracellular substances (chlorophylls, carboxylate acids) could be served as photosensitizers to improve the generation of ROS, which enhanced the photoreduction of Cr(VI) in the system.

Likewise, algae could act as carriers to have MNMs fixed onto the algae biological templates (Tu et al., 2012). Cai et al. immobilized nano-TiO₂ on Chlorella vulgaris cells via the hydrothermal method, and sensitization of the photosynthesis pigment boosted nano-TiO₂’s photodegradation efficiency under the visible light (Cai et al., 2017).

5 Conclusion and perspectives

Being widely applied in multiple fields, MNMs could be released into the aquatic environments along the life cycle, inducing critical effects on algae. We conducted a comprehensive review on both positive and negative impacts of MNMs on algae and thoroughly discussed the underlying mechanisms. In general, exposure to MNMs may adversely affect algae’s gene expression, metabolism, photosynthesis, nitrogen fixation and growth rate. The major mechanisms of MNMs-induced inhibition are attributed to oxidative stress, mechanical damages, released metal ions and light-shielding effects.

On the other hand, rational utilization of the MNMs-induced effects would promote the production of valuable bioactive substances as well as control biological and chemical pollutants. MNMs could be used to stimulate algae to produce useful bioactive substances (e.g., antioxidants, biofuel), while the MNMs-algae interaction could effectively enhance the efficiency of environmental remediation process (e.g., degradation of contaminants, control of eutrophication and biofouling.

However, there are still knowledge gaps that need to be addressed to gain a comprehensive understanding of the effect of MNMs on algae as well as the associated implications and applications. The risks of MNMs on algae in the natural ecosystem should be thoroughly assessed prior to the applications. Particularly, MNMs would be involved in environmental processes, which may induce weathering and aging effects on MNMs, further changing the physicochemical properties and effective concentration of MNMs. More in-depth investigations should be conducted to address the migration, transformation, and aging of MNMs under realistic environmental conditions. It also poses huge demand on the quantitative information of the environmental background concentration of MNMs in aquatic ecosystems, which is still missing. It is an urgent need to advance analytical instruments and protocols to quantitatively analyze the actual environmental concentrations and size distributions of MNMs.

Meanwhile, the toxicity assessment of MNMs on algae should be evaluated under environmentally relevant conditions, which should fully consider the heterogeneous joint toxicity effect of MNMs and other environmental factors, including hypoxia, acidification, temperature, heavy metal, persistent organic pollutants and micro-plastics (Liu and Wang, 2020; Liu et al., 2022). In addition, the biological effects of MNMs on algae should be carried out in real or simulated ecosystems with certain complexity and biodiversity, which is essential to improve the rationality and effectiveness of the data to obtain the whole picture of MNMs’ ecological risks.

References

[1] Ahmed I , Zhang B , Muneeb-Ur-Rehman M , Fan W . Effect of different shapes of Nano-Cu₂O and humic acid on two-generations of Daphnia Magna. Ecotoxicology and Environmental Safety, 2021, 207 : 111274–

[2] Angela I , Imbi K , Kaja K , Irina B , Villem A , Sandra S , Heiki V , Aleksandr K , Tiina T , Margit H . Size-dependent toxicity of silver nanoparticles to bacteria, yeast, algae, rrustaceans and mammalian cells in vitro. PLoS One, 2014, 9( 7): e102108–

[3] Aruoja V , Dubourguier H C , Kasemets K , Kahru A . Toxicity of nanoparticles of CuO, ZnO and TiO₂ to microalgae Pseudokirchneriella subcapitata. , 2009, 4( 207): 1461– 1468

[4] Bhuvaneshwari M , Iswarya V , Vishnu S , Chandrasekaran N , Mukherjee A . Dietary transfer of zinc oxide particles from algae (Scenedesmus obliquus) to daphnia (Ceriodaphnia dubia). Environmental Research, 2018, 164 : 395– 404

[5] Borlido L , Azevedo A M , Roque A C A , Aires-Barros M R . Magnetic separations in biotechnology. Biotechnology Advances, 2013, 31( 8): 1374– 1385

[6] Bouldin J L , Ingle T M , Sengupta A , Alexander R , Hannigan R E , Buchanan R A . Aqueous toxicity and food chain transfer of quantum dots in freshwater algae and Ceriodaphnia dubia. Environmental Toxicology and Chemistry, 2008, 27( 9): 1958– 1963

[7] Burchardt A D , Carvalho R N , Valence A , Nativo P , Gilliland D , Garcia C P , Passarella R , Pedroni V , Rossi F , Lettieri T . Effects of silver nanoparticles in diatom Thalassiosira pseudonana and Cyanobacterium Synechococcus sp. Environmental Science & Technology, 2012, 46( 20): 11336– 11344

[8] Cai A , Guo A , Ma Z . Immobilization of TiO₂ nanoparticles on Chlorella pyrenoidosa cells for enhanced visible-light-driven photocatalysis. Materials (Basel), 2017, 10( 5): 541–

[9] Campos B , Rivetti C , Rosenkranz P , Navas J M , Barata C . Effects of nanoparticles of TiO₂ on food depletion and life-history responses of Daphnia magna.. Aquatic Toxicology (Amsterdam, Netherlands), 2013, ( 130–131): 174– 183

[10] Cedervall T , Hansson L A , Lard M , Frohm B , Linse S . Food chain transport of nanoparticles affects behaviour and fat metabolism in fish. PLoS One, 2012, 7( 2): e32254–

[11] Chang Y H , Wu M C . Enhanced photocatalytic reduction of Cr(VI) by combined magnetic TiO₂-based NFs and ammonium oxalate hole scavengers. Catalysts, 2019, 9( 1): 72– 84

[12] Chen C , Zhu K , Chen K , Alsaedi A , Hayat T . Synthesis of Ag nanoparticles decoration on magnetic carbonized polydopamine nanospheres for effective catalytic reduction of Cr(VI). Journal of Colloid and Interface Science, 2018, 526 : 1– 8

[13] Chen F R , Xiao Z G , Yue L , Wang J , Feng Y , Zhu X S , Wang Z Y , Xing B S . Algae response to engineered nanoparticles: Current understanding, mechanisms and implications. Environmental Science. Nano, 2019, 6( 4): 1026– 1042

[14] Chen G , Wang H , Dong W , Huang Y , Zhao Z , Zeng Y . Graphene dispersed and surface plasmon resonance-enhanced Ag₃PO₄ (DSPR-Ag₃PO₄) for visible light driven high-rate photodegradation of carbamazepine. Chemical Engineering Journal, 2021, 405 : 126850–

[15] Chen J , Qian Y , Li H , Cheng Y , Zhao M . The reduced bioavailability of copper by nano-TiO₂ attenuates the toxicity to Microcystis aeruginosa. Environmental Science and Pollution Research International, 2015, 22( 16): 12407– 12414

[16] Chen J E , Smith A G . A look at diacylglycerol acyltransferases (DGATs) in algae. Journal of Biotechnology, 2012, 162( 1): 28– 39

[17] Cherchi C , Gu A Z . Impact of titanium dioxide nanomaterials on nitrogen fixation rate and intracellular nitrogen storage in Anabaena variabilis. Environmental Science & Technology, 2010, 44( 21): 8302– 8307

[18] Cherchi C , Miljkovic M , Diem M , Gu A Z . nTiO₂ induced changes in intracellular composition and nutrient stoichiometry in primary producer —cyanobacteria. Science of the Total Environment, 2015, ( 512–513): 345– 352

[19] Chowdhury I , Walker S L , Mylon S E . Aggregate morphology of nano-TiO₂: Role of primary particle size, solution chemistry, and organic matter. Environmental Science. Processes & Impacts, 2013, 15( 1): 275– 282

[20] Dalai S , Pakrashi S , Joyce Nirmala M , Chaudhri A , Chandrasekaran N , Mandal A B , Mukherjee A . Cytotoxicity of TiO₂ nanoparticles and their detoxification in a freshwater system. Aquatic Toxicology (Amsterdam, Netherlands), 2013, ( 138–139): 1– 11

[21] da Silva M B , Abrantes N , Nogueira V , Gonçalves F . TiO2 nanoparticles for the remediation of eutrophic shallow freshwater systems: Efficiency and impacts on aquatic biota under a microcosm experiment. Aquatic Toxicology, 2016, 178 : 58– 71

[22] Dauda S , Chia M A , Bako S P . Toxicity of titanium dioxide nanoparticles to Chlorella vulgaris Beyerinck (Beijerinck) 1890 (Trebouxiophyceae, Chlorophyta) under changing nitrogen conditions. Aquatic Toxicology (Amsterdam, Netherlands), 2017, ( 187): 108– 114

[23] Dědková K , Bureš Z , Palarčík J , Vlček M , Kukutschová J . Acute aquatic toxicity of gold nanoparticles to freshwater green algae. Procceedings of NanoCon, 2014, 2014 : 5– 7

[24] Ding W , Tan X , Chen G , Xu J , Yu K , Huang Y . Molecular-level insights on the facet-dependent degradation of perfluorooctanoic acid. ACS Applied Materials & Interfaces, 2021, 13( 35): 41584– 41592

[25] Du F , Hu C , Sun X , Zhang L , Xu N . Transcriptome analysis reveals the promoting effect of trisodium citrate on astaxanthin accumulation in Haematococcus pluvialis under high light condition. Aquaculture (Amsterdam, Netherlands), 2021, ( 543): 736978–

[26] Eroglu E , Eggers P K , Winslade M , Smith S M , Raston C L . Enhanced accumulation of microalgal pigments using metal nanoparticle solutions as light filtering devices. Green Chemistry, 2013, 15( 11): 3155– 3159

[27] Fan J , Hu Y B , Li X Y . Nanoscale zero-valent iron coated with magnesium hydroxide for effective removal of Cyanobacteria from water. ACS Sustainable Chemistry & Engineering, 2018, 6( 11): 15135– 15142

[28] Farooq W , Lee H U , Huh Y S , Lee Y C . Chlorella vulgaris cultivation with an additive of magnesium-aminoclay. ALGAL RESEARCH-BIOMASS BIOFUELS AND BIOPRODUCTS, 2016, 17 : 211– 216

[29] Fazal T , Rehman M S U , Javed F , Akhtar M , Mushtaq A , Hafeez A , Alaud Din A , Iqbal J , Rashid N , Rehman F . Integrating bioremediation of textile wastewater with biodiesel production using microalgae (Chlorella vulgaris). Chemosphere, 2021, 281 : 130758–

[30] Fonseca A J , Pina F , Macedo M F , Leal N , Romanowska-Deskins A , Laiz L , Gomez-Bolea A , Saiz-Jimenez C . Anatase as an alternative application for preventing biodeterioration of mortars: Evaluation and comparison with other biocides. International Biodeterioration & Biodegradation, 2010, 64( 5): 388– 396

[31] Franklin N M , Rogers N J , Apte S C , Batley G E , Gadd G E , Casey P S . Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl₂ to a freshwater microalga (Pseudokirchneriella subcapitata): The importance of particle solubility. Environmental Science & Technology, 2007, 41( 24): 8484– 8490

[32] Giraldo J P , Landry M P , Faltermeier S M , McNicholas T P , Iverson N M , Boghossian A A , Reuel N F , Hilmer A J , Sen F , Brew J A , Strano M S . Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nature Materials, 2014, 13( 4): 400– 408

[33] Glomstad B , Altin D , Sørensen L , Liu J , Jenssen B M , Booth A M . Carbon nanotube properties influence adsorption of phenanthrene and subsequent bioavailability and toxicity to Pseudokirchneriella subcapitata. Environmental Science & Technology, 2016, 50( 5): 2660– 2668

[34] Graziani L , Quagliarini E , Osimani A , Aquilanti L , Clementi F , Yepremian C , Lariccia V , Amoroso S , D’orazio M . Evaluation of inhibitory effect of TiO₂ nanocoatings against microalgal growth on clay brick facades under weak UV exposure conditions. Building and Environment, 2013, 64 : 38– 45

[35] Grigoriev I V , Hayes R D , Calhoun S , Kamel B , Wang A , Ahrendt S , Dusheyko S , Nikitin R , Mondo S J , Salamov A , Shabalov I , Kuo A . PhycoCosm, a comparative algal genomics resource. Nucleic Acids Research, 2021, 49( D1): D1004– D1011

[36] Guleri S , Singh K , Kaushik R , Dhankar R , Tiwari A . Phycoremediation: A novel and synergistic approach in wastewater remediation. Journal of Microbiology, Biotechnology and Food Sciences, 2020, 10( 1): 98– 106

[37] Gunasekaran D , Chandrasekaran N , Jenkins D , Mukherjee A . Plain polystyrene microplastics reduce the toxic effects of ZnO particles on marine microalgae Dunaliella salina. Journal of Environmental Chemical Engineering, 2020, 8( 5): 104250–

[38] Gunawan C , Sirimanoonphan A , Teoh W Y , Marquis C P , Amal R . Submicron and nano formulations of titanium dioxide and zinc oxide stimulate unique cellular toxicological responses in the green microalga Chlamydomonas reinhardtii. Journal of Hazardous Materials, 2013, 260 : 984– 992

[39] Hagen A , Hertel T . Quantitative analysis of optical spectra from individual single-wall carbon nanotubes. Nano Letters, 2003, 3( 3): 383– 388

[40] Haque E , Ward A C . Zebrafish as a model to evaluate nanoparticle toxicity. Nanomaterials, 2018, 8 : 561–

[41] Hartmann N B , Von der Kammer F , Hofmann T , Baalousha M , Ottofuelling S , Baun A . Algal testing of titanium dioxide nanoparticles: Testing considerations, inhibitory effects and modification of cadmium bioavailability. Toxicology, 2010, 269( 2–3): 190– 197

[42] Hazani A A , Ibrahim M M , Arif I A , Shehata A I , El-Gaaly G , Daoud M , Fouad D , Rizwana H , Moubayed N . Ecotoxicity of Ag-nanoparticles to microalgae. Journal of Pure & Applied Microbiology, 2013, 7 : 233– 241

[43] Hazeem L J , Kuku G , Dewailly E , Slomianny C , Barras A , Hamdi A , Boukherroub R , Culha M , Bououdina M . Toxicity effect of silver nanoparticles on photosynthetic pigment content, growth, ROS production and ultrastructural changes of microalgae Chlorella vulgaris.. Nanomaterials (Basel, Switzerland), 2019, 9( 7): 914–

[44] Hazeem L J , Yesilay G , Bououdina M , Perna S , Cetin D , Suludere Z , Barras A , Boukherroub R . Investigation of the toxic effects of different polystyrene micro-and nanoplastics on microalgae Chlorella vulgaris by analysis of cell viability, pigment content, oxidative stress and ultrastructural changes. Marine Pollution Bulletin, 2020, 156 : 111278–

[45] He M , Chen Y , Yan Y , Zhou S , Wang C . Influence of interaction between α-Fe₂O₃ nanoparticles and dissolved fulvic acid on the physiological responses in Synechococcus sp. PCC7942. Bulletin of Environmental Contamination and Toxicology, 2017, 99( 6): 719– 727

[46] Hu Y R , Wang F , Wang S K , Liu C Z , Guo C . Efficient harvesting of marine microalgae Nannochloropsis maritima using magnetic nanoparticles. Bioresource Technology, 2013, 138 : 387– 390

[47] Huang Y , Adeleye A S , Zhao L , Minakova A S , Anumol T , Keller A A . Antioxidant response of cucumber (Cucumis sativus) exposed to nano copper pesticide: Quantitative determination via LC-MS/MS. Food Chemistry, 2019, 270 : 47– 52

[48] Huang Y X , Keller A A , Cervantes-Aviles P , Nelson J . Fast multielement quantification of nanoparticles in wastewater and sludge using single-particle ICP-MS. ACS ES&T Water, 2021, 1( 1): 205– 213

[49] Huang Y X , Li W W , Minakova A S , Anumol T , Keller A A . Quantitative analysis of changes in amino acids levels for cucumber (Cucumis sativus) exposed to nano copper. NanoImpact, 2018, 12 : 9– 17

[50] Iswarya V , Bhuvaneshwari M , Alex S A , Iyer S , Chaudhuri G , Chandrasekaran P T , Bhalerao G M , Chakravarty S , Raichur A M , Chandrasekaran N , Mukherjee A . Combined toxicity of two crystalline phases (anatase and rutile) of Titania nanoparticles towards freshwater microalgae: Chlorella sp. Aquatic Toxicology (Amsterdam, Netherlands), 2015, ( 161): 154– 169

[51] Ji J , Long Z F , Lin D H . Toxicity of oxide nanoparticles to the green algae Chlorella sp. Chemical Engineering Journal, 2011, 170( 2-3): 525– 530

[52] Jiang Z , Tan X , Huang Y . Piezoelectric effect enhanced photocatalysis in environmental remediation: State-of-the-art techniques and future scenarios. Science of the Total Environment, 2022, 806( Pt 4): 150924–

[53] Jing L , Xu Y , Xie M , Liu J , Deng J , Huang L , Xu H , Li H . Three dimensional polyaniline/MgIn₂S₄ nanoflower photocatalysts accelerated interfacial charge transfer for the photoreduction of Cr(VI), photodegradation of organic pollution and photocatalytic H₂ production. Current Opinion in Biotechnology, 2018, 23( 3): 346– 351

[54] Jones C S , Mayfield S P . Algae biofuels: Versatility for the future of bioenergy. Current opinion in biotechnology, 2012, 23( 3): 346– 351

[55] Kartik A , Akhil D , Lakshmi D , Panchamoorthy Gopinath K , Arun J , Sivaramakrishnan R , Pugazhendhi A . A critical review on production of biopolymers from algae biomass and their applications. Bioresource Technology, 2021, 329 : 124868–

[56] Keller A A , Mcferran S , Lazareva A , Suh S . Global life cycle releases of engineered nanomaterials. Journal of Nanoparticle Research, 2013, 15( 6): 1692–

[57] Kim B , Praveenkumar R , Lee J , Nam B , Kim D M , Lee K , Lee Y C , Oh Y K . Magnesium aminoclay enhances lipid production of mixotrophic Chlorella sp. KR-1 while reducing bacterial populations. Bioresource Technology, 2016, 219 : 608– 613

[58] Kim J , Yoo G , Lee H , Lim J , Kim K , Kim C W , Park M S , Yang J W . Methods of downstream processing for the production of biodiesel from microalgae. Biotechnology Advances, 2013, 31( 6): 862– 876

[59] Kong Y , Sun H , Zhang S , Zhao B , Zhao Q , Zhang X , Li H . Oxidation process of lead sulfide nanoparticle in the atmosphere or natural water and influence on toxicity toward Chlorella vulgaris. Journal of Hazardous Materials, 2021, 417 : 126016–

[60] Kubatova H , Zemanová E , Klouda K , Bilek K , Kadukova J . Effects of C₆₀ fullerene and its derivatives on selected microorganisms. Journal of Microbiology Research (Rosemead, Calif.), 2013, ( 3): 152– 162

[61] Kumar R , Gopal M , Pabbi S , Paul S , Imteyaz Alam M , Yadav S , Nair K K , Chauhan N , Srivastava C , Gogoi R , Singh P K , Goswami A . Effect of nanohexaconazole on nitrogen fixing blue green algae and bacteria. Journal of Nanoscience and Nanotechnology, 2016, 16( 1): 643– 647

[62] Lambreva M D , Lavecchia T , Tyystjärvi E , Antal T K , Orlanducci S , Margonelli A , Rea G . Potential of carbon nanotubes in algal biotechnology. Photosynthesis Research, 2015, 125( 3): 451– 471

[63] Lauritano C , Ferrante M I , Rogato A . Marine natural products from microalgae: An omics overview. Marine Drugs, 2019, 17( 5): 269–

[64] Lee S , Kang Y I , Ha S J , Moon J H . Carbon-deposited TiO₂ nanoparticle balls for high-performance visible photocatalysis. RSC Advances, 2014, 4( 98): 55371– 55376

[65] Li F , Liang Z , Zheng X , Zhao W , Wu M , Wang Z . Toxicity of nano-TiO₂ on algae and the site of reactive oxygen species production. Aquatic Toxicology (Amsterdam, Netherlands), 2015a, ( 158): 1– 13

[66] Li X , Zhou S , Fan W . Effect of nano-Al₂O₃ on the toxicity and oxidative stress of copper towards Scenedesmus obliquus. International Journal of Environmental Research and Public Health, 2016, 13( 6): 575–

[67] Li X M , Schirmer K , Bernard L , Sigg L , Pillai S , Behra R . Silver nanoparticle toxicity and association with the alga Euglena gracilis. Environmental Science. Nano, 2015b, 2( 6): 594– 602

[68] Li Y , Zhang W , Niu J , Chen Y . Mechanism of photogenerated reactive oxygen species and correlation with the antibacterial properties of engineered metal-oxide nanoparticles. ACS Nano, 2012, 6( 6): 5164– 5173

[69] Li Z , Juneau P , Lian Y , Zhang W , Wang S , Wang C , Shu L , Yan Q , He Z , Xu K . Effects of titanium dioxide nanoparticles on photosynthetic and antioxidative processes of Scenedesmus obliquus. Plants (Basel, Switzerland), 2020a, 9( 12): 1748–

[70] Liu P , Corilo Y E , Marshall A G . Polar lipid composition of biodiesel algae candidates Nannochloropsis oculata and Haematococcus pluvialis from nano liquid chromatography coupled with negative electrospray ionization 14.5 T Fourier transform ion cyclotron resonance mass spectrometry. Energy & Fuels, 2016, 30( 10): 8270– 8276

[71] Liu X S , Wang J M . Algae (Raphidocelis subcapitata) mitigate combined toxicity of microplastic and lead on Ceriodaphnia dubia. Frontiers of Environmental Science & Engineering, 2020, 14( 6): 97–

[72] Liu X S , Wang J M , Huang Y W . Understanding the role of nano-TiO₂ on the toxicity of Pb on C. dubia through modeling—Is it additive or synergistic? Frontiers of Environmental Science & Engineering, 2022, 16( 5): 59–

[73] Liu Y , Wang S , Wang Z , Ye N , Fang H , Wang D . TiO₂, SiO₂ and ZrO₂ nanoparticles synergistically provoke cellular oxidative damage in freshwater microalgae. Nanomaterials (Basel, Switzerland), 2018, 8( 2): 95–

[74] López-Alonso M , Díaz-Soler B , Martínez-Rojas M , Fito-López C , Martínez-Aires M D . Management of occupational risk prevention of nanomaterials manufactured in construction sites in the EU. International Journal of Environmental Research and Public Health, 2020, 17( 24): 9211–

[75] Manier N , Bado-Nilles A , Delalain P , Aguerre-Chariol O , Pandard P . Ecotoxicity of non-aged and aged CeO₂ nanomaterials towards freshwater microalgae. Environmental Pollution (Barking, Essex: 1987), 2013, 180 : 63– 70

[76] Manzo S , Miglietta M L , Rametta G , Buono S , Di Francia G . Toxic effects of ZnO nanoparticles towards marine algae Dunaliella tertiolecta. Science of the Total Environment, 2013, 445–446 : 371– 376

[77] Masojidek J , Ranglova K , Lakatos G , Silva Benavides A M , Torzillo G . Variables governing photosynthesis and growth in microalgae mass cultures. Processes (Basel, Switzerland), 2021, 9( 5): 820–

[78] Metzler D M , Erdem A , Tseng Y H , Huang C P . Responses of algal cells to engineered nanoparticles measured as algal cell population, Chlorophyll a, and lipid peroxidation: Effect of particle size and type. Journal of Nanotechnology, 2012, 2012 : 237212– 237284

[79] Metzler D M , Li M , Erdem A , Huang C P . Responses of algae to photocatalytic nano-TiO₂ particles with an emphasis on the effect of particle size. Chemical Engineering Journal, 2011, 170( 2–3): 538– 546

[80] Middepogu A , Hou J , Gao X , Lin D . Effect and mechanism of TiO₂ nanoparticles on the photosynthesis of Chlorella pyrenoidosa. Ecotoxicology and Environmental Safety, 2018, 161 : 497– 506

[81] Mohsenpour S F , Hennige S , Willoughby N , Adeloye A , Gutierrez T . Integrating micro-algae into wastewater treatment: A review. Science of the Total Environment, 2021, 752 : 142168–

[82] Morelli E , Cioni P , Posarelli M , Gabellieri E . Chemical stability of CdSe quantum dots in seawater and their effects on a marine microalga. Aquatic Toxicology (Amsterdam, Netherlands), 2012, ( 122–123): 122– 123

[83] Nogueira P F M , Nakabayashi D , Zucolotto V . The effects of graphene oxide on green algae Raphidocelis subcapitata.. Aquatic Toxicology (Amsterdam, Netherlands), 2015, ( 166): 29– 35

[84] Ouabadi N , Gauthier-Brunet V , Cabioc’h T , Bei G P , Dubois S . Formation mechanisms of Ti3SnC2 nanolaminate carbide using Fe as additive. Journal of the American Ceramic Society, Oukarroum A, Bras S, Perreault F, Popovic R (2012). Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta.. Ecotoxicology and Environmental Safety, 2013, ( 78): 80– 85

[85] Oukarroum A , Bras S , Perreault F , Popovic R . Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicology and Environmental Safety, 2012, 78 : 80– 85

[86] PattarkineM V, PattarkineV M (2012). Nanotechnology for algal biofuels. New York: Springer

[87] Pillai S , Behra R , Nestler H , Suter J F , Schirmer K . Linking toxicity and adaptive responses across the transcriptome, proteome, and phenotype of Chlamydomonas reinhardtii exposed to silver. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111( 9): 3490– 3495

[88] Praveenkumar R , Gwak R , Kang M , Shim T S , Cho S , Lee J , Oh Y K , Lee K , Kim B . Regenerative astaxanthin extraction from a single microalgal (Haematococcus pluvialis) cell using a gold nano-scalpel. ACS Applied Materials & Interfaces, 2015, 7( 40): 22702– 22708

[89] Premnath N , Mohanrasu K , Guru Raj Rao R , Dinesh G H , Prakash G S , Ananthi V , Ponnuchamy K , Muthusamy G , Arun A . A crucial review on polycyclic aromatic hydrocarbons: Environmental occurrence and strategies for microbial degradation. Chemosphere, 2021, 280 : 130608–

[90] RaiV, KarthikaichamyA, DasD, NoronhaS, WangikarP P, SrivastavaS (2016). Multi-omics Frontiers in Algal Research: Techniques and Progress to Explore Biofuels in the Postgenomics World. Omics A Journal of Integrative Biology: omi.2016.0065

[91] Rhiem S , Riding M J , Baumgartner W , Martin F L , Semple K T , Jones K C , Schäffer A , Maes H M . Interactions of multiwalled carbon nanotubes with algal cells: Quantification of association, visualization of uptake, and measurement of alterations in the composition of cells. Environmental Pollution (Barking, Essex: 1987), 2015, ( 196): 431– 439

[92] Rocha T L , Gomes T , Sousa V S , Mestre N C , Bebianno M J . Ecotoxicological impact of engineered nanomaterials in bivalve molluscs: An overview. Marine Environmental Research, 2015, 111 : 74– 88

[93] Rodea-Palomares I , Gonzalo S , Santiago-Morales J , Leganés F , García-Calvo E , Rosal R , Fernández-Piñas F . An insight into the mechanisms of nanoceria toxicity in aquatic photosynthetic organisms. Aquatic Toxicology (Amsterdam, Netherlands), 2012, ( 122–123): 122– 123

[94] Saber M , Golzary A , Hosseinpour M , Takahashi F , Yoshikawa K . Catalytic hydrothermal liquefaction of microalgae using nanocatalyst. Applied Energy, 2016, 183( dec.1): 566– 576

[95] Sadiq I M , Dalai S , Chandrasekaran N , Mukherjee A . Ecotoxicity study of titania (TiO₂) NPs on two microalgae species: Scenedesmus sp. and Chlorella sp. Ecotoxicology and Environmental Safety, 2011a, 74( 5): 1180– 1187

[96] Sadiq I M , Pakrashi S , Chandrasekaran N , Mukherjee A . Studies on toxicity of aluminum oxide (Al₂O₃) nanoparticles to microalgae species: Scenedesmus sp. and Chlorella sp. Journal of Nanoparticle Research, 2011b, 13( 8): 3287– 3299

[97] Saison C , Perreault F , Daigle J C , Fortin C , Claverie J , Morin M , Popovic R . Effect of core-shell copper oxide nanoparticles on cell culture morphology and photosynthesis (photosystem II energy distribution) in the green alga, Chlamydomonas reinhardtii.. Aquatic Toxicology (Amsterdam, Netherlands), 2010, 96( 2): 109– 114

[98] Samara Sanchez-Sandoval D , Gonzalez-Ortega O , Fernanda Navarro-Martinez M , Marcos Castro-Tapia J , Garcia De La Cruz R F , Elena Soria-Guerra R . Photodegradation and removal of diclofenac by the green alga Nannochloropsis oculata. Phyton, 2021, 90( 5): 1519– 1533

[99] Santschi C , Von Moos N , Koman V B , Slaveykova V I , Bowen P , Martin O J F . Non-invasive continuous monitoring of pro-oxidant effects of engineered nanoparticles on aquatic microorganisms. Journal of Nanobiotechnology, 2017, 15( 1): 19–

[100] ScheererS, Ortega-MoralesO, GaylardeC (2009). Advances in Applied Microbiology, Vol 66. Laskin A L, Sariaslani S, Gadd G, eds. San Diego.: Academic Press, 97–139

[101] Schwab F , Bucheli T D , Lukhele L P , Magrez A , Nowack B , Sigg L , Knauer K . Are carbon nanotube effects on green algae caused by shading and agglomeration?. Environmental Science & Technology, 2011, 45( 14): 6136– 6144

[102] Serag M F , Kaji N , Habuchi S , Bianco A , Baba Y . Nanobiotechnology meets plant cell biology: Carbon nanotubes as organelle targeting nanocarriers. RSC Advances, 2013, 3( 15): 4856– 4862

[103] Sohn E K , Chung Y S , Johari S A , Kim T G , Kim J K , Lee J H , Lee Y H , Kang S W , Yu I J . Acute toxicity comparison of single-walled carbon nanotubes in various freshwater organisms. BioMed Research International, 2015, 2015 : 323090–

[104] Song J , Li C , Wang X , Zhi S , Wang X , Sun J . Visible-light-driven heterostructured g-C₃N₄/Bi-TiO₂ floating photocatalyst with enhanced charge carrier separation for photocatalytic inactivation of Microcystis aeruginosa. Frontiers of Environmental Science & Engineering, 2021, 15( 6): 129–

[105] Sun S , Deng H , Yang J , Zhou D , Wan X , Han F . Photodegradation of butyl 4-hydroxybenzoate in the presence of peroxides and mediated by dissolved organic matter. Environmental Engineering Science, 2020, 37( 7): 497– 508

[106] Tan X , Chen G , Xing D , Ding W , Liu H , Li T , Huang Y . Indium-modified Ga₂O₃ hierarchical nanosheets as efficient photocatalysts for the degradation of perfluorooctanoic acid. Environmental Science: Nano, 2020, 7( 8): 2229– 2239

[107] Taylor M P , Forbes M K , Opeskin B , Parr N , Lanphear B P . The relationship between atmospheric lead emissions and aggressive crime: An ecological study. Environmental Health, 2016, 15 : 23–

[108] Thiagarajan V , Alex S A , Seenivasan R , Chandrasekaran N , Mukherjee A . Toxicity evaluation of nano-TiO₂ in the presence of functionalized microplastics at two trophic levels: Algae and crustaceans. Science of the Total Environment, 2021, 784 : 147262–

[109] Torkamani S , Wani S N , Tang Y J , Sureshkumar R . Plasmon-enhanced microalgal growth in miniphotobioreactors. Applied Physics Letters, 2010, 97( 4): 043703–

[110] Tu Y D , Zhou Z , Yan R J , Gan Y P , Huang W Z , Weng X X , Huang H , Zhang W K , Tao X Y . Bio-template synthesis of spirulina/TiO₂ composite with enhanced photocatalytic performance. RSC Advances, 2012, 2( 28): 10585– 10591

[111] Tyne W , Little S , Spurgeon D J , Svendsen C . Hormesis depends upon the life-stage and duration of exposure: Examples for a pesticide and a nanomaterial. Ecotoxicology and Environmental Safety, 2015, 120 : 117– 123

[112] Vargas-Estrada L , Torres-Arellano S , Longoria A , Arias D M , Okoye P U , Sebastian P J . Role of nanoparticles on microalgal cultivation: A review. Fuel, 2020, 280 : 118598–

[113] Verma A , Prakash N T , Toor A P . An efficient TiO₂ coated immobilized system for the degradation studies of herbicide isoproturon: Durability studies. Chemosphere, 2014, 109 : 7– 13

[114] Verneuil L , Silvestre J , Randrianjatovo I , Marcato-Romain C E , Girbal-Neuhauser E , Mouchet F , Flahaut E , Gauthier L , Pinelli E . Double walled carbon nanotubes promote the overproduction of extracellular protein-like polymers in Nitzschia palea: An adhesive response for an adaptive issue. Carbon, 2015, 88 : 113– 125

[115] von Moos N , Slaveykova V I . Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic microalgae: State of the art and knowledge gaps. Nanotoxicology, 2014, 8( 6): 605– 630

[116] Wahid M H , Eroglu E , Chen X , Smith S M , Raston C L . Entrapment of Chlorella vulgaris cells within graphene oxide layers. RSC Advances, 2013, 3( 22): 8180– 8183

[117] Wang P , Zhao L , Huang Y , Qian W , Zhu X , Wang Z , Cai Z . Combined toxicity of nano-TiO₂ and Cd²⁺ to Scenedesmus obliquus: Effects at different concentration ratios. Journal of Hazardous Materials, 2021a, 418 : 126354–

[118] Wang S , Wang Z , Chen M , Fang H , Wang D . Co-exposure of freshwater microalgae to tetrabromobisphenol A and sulfadiazine: Oxidative stress biomarker responses and joint toxicity prediction. Bulletin of Environmental Contamination and Toxicology, 2017, 99( 4): 438– 444

[119] Wang X , Zhang J , Sun W , Yang W , Cao J , Li Q , Peng Y , Shang J K . Anti-algal activity of palladium oxide-modified nitrogen-doped titanium oxide photocatalyst on Anabaena sp. PCC 7120 and its photocatalytic degradation on Microcystin LR under visible light illumination. Chemical Engineering Journal, 2015, 264 : 437– 444

[120] Wang Z , Li J , Zhao J , Xing B . Toxicity and internalization of CuO nanoparticles to prokaryotic alga Microcystis aeruginosa as affected by dissolved organic matter. Environmental Science & Technology, 2011, 45( 14): 6032– 6040

[121] Wang Z , Zhang F , Vijver M G , Peijnenburg W J G M . Graphene nanoplatelets and reduced graphene oxide elevate the microalgal cytotoxicity of nano-zirconium oxide. Chemosphere, 2021b, 276 : 130015–

[122] Wei C , Zhang Y , Guo J , Han B , Yang X , Yuan J . Effects of silica nanoparticles on growth and photosynthetic pigment contents of Scenedesmus obliquus. Journal of Environmental Sciences (China), 2010a, 22( 1): 155– 160

[123] Wei L , Li H , Lu J . Algae-induced photodegradation of antibiotics: A review. Environmental Pollution, 2021, 272 : 115589–

[124] Wei L , Thakkar M , Chen Y , Ntim S A , Mitra S , Zhang X . Cytotoxicity effects of water dispersible oxidized multiwalled carbon nanotubes on marine alga, Dunaliella tertiolecta.. Aquatic Toxicology (Amsterdam, Netherlands), 2010, 100( 2): 194– 201

[125] Wong S W Y , Leung P T Y , Djurisić A B , Leung K M Y . Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility. Analytical and Bioanalytical Chemistry, 2010, 396( 2): 609– 618

[126] Xiao A , Wang C , Chen J , Guo R , Yan Z , Chen J . Carbon and metal quantum dots toxicity on the microalgae Chlorella pyrenoidosa. Ecotoxicology and Environmental Safety, 2016, 133 : 211– 217

[127] Xin X , Huang G , Zhang B , Zhou Y . Trophic transfer potential of nTiO₂, nZnO, and triclosan in an algae-algae eating fish food chain. Aquatic Toxicology (Amsterdam, Netherlands), 2021, 235 : 105824–

[128] Xiong Q , Hu L X , Liu Y S , Zhao J L , He L Y , Ying G G . Microalgae-based technology for antibiotics removal: From mechanisms to application of innovational hybrid systems. Environment International, 2021a, 155 : 106594–

[129] Xiong S , Cao X , Fang H , Guo H , Xing B . Formation of silver nanoparticles in aquatic environments facilitated by algal extracellular polymeric substances: Importance of chloride ions and light. Science of the Total Environment, 2021b, 775 : 145867–

[130] Xu J , Luo X , Wang Y , Feng Y . Evaluation of zinc oxide nanoparticles on lettuce (Lactuca sativa L). growth and soil bacterial community. Environmental Science and Pollution Research International, 2018, 25( 6): 6026– 6035

[131] Yan Z C J , Xiao A , Shu J , Chen J . Effects of representative quantum dots on microorganisms and phytoplankton: A comparative study. RSC Advances, 2015, 5( 129): 106406– 106412

[132] Yang X Y , He Q , Guo F C , Liu X B , Chen Y . Translocation and biotoxicity of metal (oxide) nanoparticles in the wetland-plant system. Frontiers of Environmental Science & Engineering, 2021, 15( 6): 138–

[133] Yap J K , Sankaran R , Chew K W , Halimatul Munawaroh H S , Ho S H , Rajesh Banu J , Show P L . Advancement of green technologies: A comprehensive review on the potential application of microalgae biomass. Chemosphere, 2021, 281 : 130886–

[134] Yue Y , Li X , Sigg L , Suter M J F , Pillai S , Behar R , Schirmer K . Interaction of silver nanoparticles with algae and fish cells: A side by side comparison. Journal of Nanobiotechnol, 2017, 15 : 16–

[135] Zhang C , Chen X , Tan L , Wang J . Combined toxicities of copper nanoparticles with carbon nanotubes on marine microalgae Skeletonema costatum. Environmental Science and Pollution Research International, 2018a, 25( 13): 13127– 13133

[136] Zhang C , Wang J , Tan L , Chen X . Toxic effects of nano-ZnO on marine microalgae Skeletonema costatum: Attention to the accumulation of intracellular Zn. Aquatic Toxicology (Amsterdam, Netherlands), 2016a, 158– 164

[137] Zhang L Q , Lei C , Yang K , White J C , Lin D H . Cellular response of Chlorella pyrenoidosa to oxidized multi-walled carbon nanotubes. Environmental Science. Nano, 2018b, 5( 10): 2415– 2425

[138] Zhang Q , Hu J , Lee D J . Biogas from anaerobic digestion processes: Research updates. Renewable Energy, 2016b, 98 : 108– 119

[139] Zhang W X , Elliott D W . Applications of iron nanoparticles for groundwater remediation. Hoboken: Wiley Subscription Services, Inc., 2006, 16( 2): 7– 21

[140] Zhang Y D , Liu N , Wang W , Sun J T , Zhu L Z . Photosynthesis and related metabolic mechanism of promoted rice (Oryza sativa L). growth by TiO₂ nanoparticles. Frontiers of Environmental Science & Engineering, 2020, 14( 6): 103–

[141] Zhao C M , Wang W X . Biokinetic uptake and efflux of silver nanoparticles in Daphnia magna. Environmental Science & Technology, 2010, 44( 19): 7699– 7704

[142] Zhao J , Cao X , Liu X , Wang Z , Zhang C , White J C , Xing B . Interactions of CuO nanoparticles with the algae Chlorella pyrenoidosa: Adhesion, uptake, and toxicity. Nanotoxicology, 2016, 10( 9): 1297– 1305

[143] Zhao J , Cao X , Wang Z , Dai Y , Xing B . Mechanistic understanding toward the toxicity of graphene-family materials to freshwater algae. Water Research, 2017, 111 : 18– 27

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