Journal of Environmental Management 357 (2024) 120723

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Journal of Environmental Management

journal homepage: www.elsevier.com/locate/jenvman

Review

Harnessing the potential of microalgae-based systems for mitigating

pesticide pollution and its impact on their metabolism
Tufail Fayaz a, Soujanya S. Rana a, Esha Goyal a, Sachitra Kumar Ratha b, Nirmal Renuka a, *
a
Algal Biotechnology Laboratory, Department of Botany, Central University of Punjab, Bathinda, 151401, India
b
Algology Laboratory, CSIR-National Botanical Research Institute, Lucknow, 226001, India

A R T I C L E I N F O A B S T R A C T

Handling editor: Raf Dewil Due to increased pesticide usage in agriculture, a significant concentration of pesticides is reported in the
environment that can directly impact humans, aquatic flora, and fauna. Utilizing microalgae-based systems for
Keywords: pesticide removal is becoming more popular because of their environmentally friendly nature, ability to degrade
Micropollutants pesticide molecules into simpler, nontoxic molecules, and cost-effectiveness of the technology. Thus, this review
Microalgae
focused on the efficiency, mechanisms, and factors governing pesticide removal using microalgae-based systems
Pesticide removal
and their effect on microalgal metabolism. A wide range of pesticides, like atrazine, cypermethrin, malathion,
Bioremediation
Gene expression trichlorfon, thiacloprid, etc., can be effectively removed by different microalgal strains. Some species of Chlorella,
Biochemical composition Chlamydomonas, Scenedesmus, Nostoc, etc., are documented for >90% removal of different pesticides, mainly
through the biodegradation mechanism. The antioxidant enzymes such as ascorbate peroxidase, superoxide
dismutase, and catalase, as well as the complex structure of microalgae cell walls, are mainly involved in
eliminating pesticides and are also crucial for the defense mechanism of microalgae against reactive oxygen
species. However, higher pesticide concentrations may alter the biochemical composition and gene expression
associated with microalgal growth and metabolism, which may vary depending on the type of strain, the
pesticide type, and the concentration. The final section of this review discussed the challenges and prospects of
how microalgae can become a successful tool to remediate pesticides.

1. Introduction legal requirements to minimize possible repercussions. Because pesti­

cides are so extensively accumulative and persistent in the environment,
Global use of pesticides is estimated at 2 million tons, with China, the frequent use of them can result in many health issues that adversely
United States, and Argentina contributing most of this usage (Sharma affect non-target organisms over time, especially aquatic species, lead­
et al., 2019). Due to industrial waste and overflow from crop fields, ing to a significant ecological concern (Carazo-Rojas et al., 2018; Lee
pesticides are often detected in aquatic ecosystems such as wastewater, and Choi, 2020; Zaka et al., 2019). Longer half-life, significant bio­
surface water, and groundwater (Supplementary Fig. S1). The world­ accumulation potential, and toxicity are characteristics of several pes­
wide occurrence of pesticides (including organophosphates, alkyl ticides that are usually prevalent in food, vegetables, milk, and various
phosphates, pyrethroids, triazines, etc.) in municipal wastewater, sur­ food products (Khan and Pathak, 2020).
face water, and groundwater has been reported in several studies (Fir­ Conventional methods for removing pesticides from wastewater are
ouzsalari et al., 2019; Rousis et al., 2020; Zhou et al., 2020; mainly ineffective; consequently, pesticides are still prevalent (Khan and
Montiel-León et al., 2019; Nag et al., 2020). Water-soluble pesticides are Pathak, 2020; Sutton et al., 2019). In the recent decade, various inno­
flushed away from the environment during precipitation by percolating vative technologies have emerged to efficiently remove micropollutants,
through the soil layers and finally reaching the surface and groundwater including pesticides. The advantages and drawbacks of these technolo­
(Syafrudin et al., 2021). Pesticide pollution in groundwater has been gies have been discussed in Table 1. These approaches and procedures
evidenced by the occurrence of pesticide residues in groundwater (Berni for treating pesticides have significant disadvantages in practicality,
et al., 2021; Chaza et al., 2018). Thus, careful use of pesticides is of economic viability, and effectiveness; thus, biological treatment has
utmost importance, and one should follow all labeled directions and evolved as a substitute technique for pesticide removal (Shrikant and

* Corresponding author.
E-mail addresses: [email protected], [email protected] (N. Renuka).

https://doi.org/10.1016/j.jenvman.2024.120723
Received 30 December 2023; Received in revised form 28 February 2024; Accepted 19 March 2024
Available online 1 April 2024
0301-4797/© 2024 Elsevier Ltd. All rights reserved.
T. Fayaz et al. Journal of Environmental Management 357 (2024) 120723

Table 1 Table 1 (continued )

Advantages and limitations of different emerging technologies for pesticide Approaches for Advantages Limitations Reference
removal from the aquatic environment. pesticide removal
Approaches for Advantages Limitations Reference from wastewater
pesticide removal nature, and high periodically, the 2015; Biswas and
from wastewater efficiency in oxide film can Goel, 2022; Das
Chlorination Cheap and easy to Oxidation of (Li et al., 2023; dealing with passivate the et al., 2023;
implement. micro- Saleh et al., 2020) various electrodes, the Moussa et al.,
contaminants recalcitrant aqueous media 2017)
into toxic pollutants; needs to be
intermediate effective in the conductive, high
byproducts, removal of electricity
intermediate organic, consumption,
products could inorganic, and and operating
be more harmful emerging costs are
and less contaminants expensive.
removable than with negligible
the parent formation of by-
compounds, e. product wastes.
g., formation of Electrooxidation Removes various Less effective for (Borràs et al.,
Oxon. persistent and treating 2010; Feng et al.,
Ozonation Produces highly High ozone (Joseph et al., recalcitrant wastewater with 2023; Liu et al.,
reactive free generation cost, 2021; Malakootian organic a high 2021; Ouarda
radicals, less dependent on et al., 2020; Song pollutants, high concentration of et al., 2020; Yang,
selective, and pH, short et al., 2023) efficiency, ease of suspended 2020)
generates less lifetime of automation and solids,
secondary waste. ozone, low transportation, expensive, and
ozone solubility and treatment of halogenated by-
in aqueous large volumes of products are
solution, and wastewater. produced.
mass transfer. Reverse osmosis Filters the most More expensive (Chen et al., 2020;
Fenton oxidation High removal Narrow working (Cuerda-Correa contaminants, to remove all Ketharani et al.,
rates of organic pH range, high et al., 2019; safe and minerals and 2022; Matin et al.,
contaminants (up costs and risks Dolatabadi et al., environmentally challenging to 2021; Moreira
to 100%), Fe2+ is associated with 2021; M. Zhang friendly. install. et al., 2021;
abundant and handling, et al., 2019b) Niewersch et al.,
non-toxic, transportation, 2020;
hydrogen and storage of Vigneswaran et al.,
peroxide is easy reagents (H2O2 2021)
to handle and and catalyst), Adsorption Simple Produces waste (Garba et al., 2021;
environmentally and significant operations, products, Mojiri et al., 2020)
benign, and no iron sludge- relatively downstream
chlorinated related inexpensive, and processing of
compounds are secondary several regenerating
formed as in other pollutants. commercial agents can be
techniques. adsorbents are challenging, and
Photocatalytic Chemical-free Inability to work (Guo et al., 2017; available. agglomeration
degradation treatment; in solar Khan and Pathak, of nanosized
requires radiation, fast 2020; Koe et al., adsorbents
relatively low charge 2020; Tyagi et al., decreases their
maintenance and recombination, 2022) performance.
operational costs, and low Nanofiltration No chemicals Requires (Abdel-Fatah,
environmentally migration ability required, Low membrane 2018; Crini and
friendly, energy- of the photo- solid waste replacement in a Lichtfouse, 2019;
saving and can generated generation, shorter time, Jafari et al., 2021;
quickly degrade electrons and efficient high energy Le Phuong et al.,
highly complex, holes, requires elimination of requirements, 2020; Zhang et al.,
and concentrated more energy, particles, high 2021)
pollutants in lower quantum suspended solids, maintenance
water. efficiency, limit and and operation
of reusability, microorganisms. costs, and
recovery of limited flow
catalyst, and rates.
exhibits toxicity. Membrane 100% removal, Low permeate (Pan et al., 2019;
Coagulation and Used for fine Multiple step (Abujazar et al., distillation operates at flux, membrane Sushvanth Reddy
flocculation particle removal, process, release 2022; Saravanan atmospheric fouling, and et al., 2021; Ying
removes metals, of hazardous et al., 2021; Uysal conditions, and pore wetting. Shi et al., 2020)
color, and monomers and and Boyacioglu, cost-effective.
turbidity, and residue of 2021; Zhao et al., Electrodialysis Potential to reuse Fouling of ion (Arana Juve et al.,
economically coagulants/ 2021, 2021, 2021) the secondary exchange 2022; Oztekin and
feasible. flocculants in streams, simple membranes and Altin, 2016)
the effluents, setup, and large high energy
and high sludge scale treatment. consumption.
production. Iron-enhanced Efficiently Not a promising (Fairbairn and
Electrocoagulation Ease of operation, Electrodes (Barrera-Díaz sand filters remove dissolved method for Trojan, 2023;
low footprint, should be et al., 2011; phosphorus from pesticide Westerhoff et al.,
eco-friendly replaced Bazrafshan et al., stormwater. removal. 2018)
(continued on next page)

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T. Fayaz et al. Journal of Environmental Management 357 (2024) 120723

Table 1 (continued ) Microcystis sp. and Scenedesmus quadricauda, were shown to be tolerant
Approaches for Advantages Limitations Reference and capable of eliminating 18.3% and 15.2% of mesotrione, when
pesticide removal cultivated for 96 h in axenic BG-11 medium supplemented with meso­
from wastewater trione at 5 mg L− 1 concentration, respectively (Ni et al., 2014). There are
Microalgal based Cost-effective, Environmental (Molinuevo-Salces three primary mechanisms by which microalgae can remove pesticides,
treatment efficiently and operational et al., 2019; Sheng i.e., biosorption, bio-uptake or bioaccumulation, and biodegradation
remediated, conditions et al., 2022) (Goh et al., 2022). Alone, phycoremediation is not economically
environmentally influence
feasible; microalgae-derived biomass synthesizes many novel materials
friendly, solar- pesticide
driven, nutrient removal and value-added products, viz., biofuel, alcohols, bio-oils, biochar
recovery, and efficiency, methane, hydrogen, syngas, food, feed, and cosmetics, making it a
industrial biomass cost-effective treatment method (Sarwer et al., 2022). Microalgal
application of harvesting, and biomass can be co-processed with other relevant bio-refinery applica­
algal biomass. vaporization.
tions to reduce costs and increase the sustainability of
microalgae-mediated bioremediation processes (Rizwan et al., 2018;
Madaan, 2021; Saleh et al., 2020). Among biological treatments, Geremia et al., 2021). However, the presence of micropollutants like
microalgal technology has received a lot of scientific interest in suc­ pesticides can modulate the biochemical composition of microalgae
cessfully removing pesticides as an environmentally friendly and sus­ (Almeida et al., 2019).
tainable approach (Nie et al., 2020). Microalgae are ubiquitous There are available reviews on the capability of microalgae-based
autotrophic microorganisms that inhabit aquatic environments and systems for pesticide removal (Goh et al., 2022; Nie et al., 2020;
have proven promising to eradicate inorganic and organic contaminants Sheng et al., 2010); however, the effect of these micropollutants on
(Sutherland and Ralph, 2019; Tang et al., 2020). These microorganisms microalgae growth, biochemical composition, and gene expression has
are also considered an effective bioremediation tool for treating indus­ not yet been reviewed. Thus, in the present paper, the bioremediation of
trial effluents containing pesticides (Pacheco et al., 2020; Wang et al., pesticides through microalgal systems and factors affecting the removal
2021) because they can remove nutrients, metals, and organic con­ efficiency have been reviewed. The effect of pesticides on biomass
taminants and capture CO2 from the air (Fig. 1). Microalgae can use production, gene expression, and the biochemical composition of
environmental pollutants, including phosphorus, nitrogen, heavy microalgae for commercial applications are also discussed.
metals, dyes, pesticides, and pharmaceuticals, for their growth and
development (Hultberg et al., 2016; Fayaz et al., 2023; Kumar et al., 2. Phycoremediation technology for pesticide removal
2022; Pratiwi et al., 2019; Zhang et al., 2019c). As a result, they are
found to be an effective tool for wastewater treatment and biomass Several research studies have demonstrated that microalgae can
production for industrial applications (Priya et al., 2022; Peter et al., potentially remove pesticides from the aqueous environment (Table 2).
2022). Species of Chlorella are most exploited for their potential for pesticide
The microalgae can degrade pesticides from water by natural removal at different scales (Table 2). Mojiri et al. (2022) studied the
metabolic processes, transforming them into organic matter and efficiency of C. vulgaris in removing chlorpyrifos and cypermethrin in a
releasing oxygen (Singhal et al., 2021). Various pesticides, including photobioreactor at a concentration of 0.32 mg L− 1. It was revealed that
atrazine, propanil, metolachlor, pyriproxyfen, dimethoate, carbofuran, 93.12% of cypermethrin and 88.80% of chlorpyrifos were reduced after
isoproturon, molinate, and simazine, can be degraded by microalgae up 69.7 h of treatment. C. sorokiniana degraded 90% of malathion in 14
to 87–96% under controlled conditions (Hussein et al., 2017). At 100 days in Bold’s basal medium (BBM) containing 25 μg L− 1 of malathion
mg L− 1 trichlorfon, Chlamydomonas reinhardtii demonstrated 100% (Nanda et al., 2019). Kurade et al. (2016) reported 94% removal of
removal; however, higher concentrations of 200 mg L− 1 hindered diazinon in 12 days using C. vulgaris when cultivated in a BBM medium
microalgae growth (51%) (Wan et al., 2020). Two microalgal strains, supplemented with a pesticide concentration of 20 mg L− 1.

Fig. 1. A schematic diagram showing phycoremediation of pesticides, mitigation of environmental risks, and revenue generation.

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T. Fayaz et al. Journal of Environmental Management 357 (2024) 120723

Table 2
The efficiency and mechanisms of pesticide removal by different microalgal strains.
Pesticide Microalgal species Scale of study Culture conditions Initial Mechanism Biomass Reference
(medium, temperature, Concentration, application
light, pH, photoperiod, removal
Agitation) percentage, time

Atrazine Chlamydomonas 250 mL Erlenmeyer BBM medium, 27 ◦ C, 100 μg L− 1, 36%, Biodegradation Bioremediation Kabra et al.
mexicana flask 45–50 μmol m− 2 s− 1, 14 d (2014)
NA, 24: 0 h, 150 rpm in
incubator shaker
Chlorella vulgaris 500 mL Erlenmeyer BG-11 medium, 27 ◦ C, 2 μg L− 1, 88.15%, Sorption Bioremediation Hussein et al.
flask 62.04 μmol m− 2 s− 1, 1h (2017)
NA, 24: 0 h, NA
Chlorella sp. 500 mL Erlenmeyer BG-11 medium, 25 ◦ C, 40–80 μg L− 1, Photocatalytic Bioremediation Hu et al.
Flask 100 μmol m− 2 s− 1, NA, 85–87.0%, 8 d Degradation (2021)
12: 12 h, 180 rpm in
isothermal shaker
Bifenthrin Chlorella sp. and 250 mL Erlenmeyer BBM medium, 25 ◦ C, 1 mg L− 1, 55.5%, Biodegradation Bioremediation, Avila et al.
Scenedesmus sp. flask 31 μmol m− 2 s− 1, NA, 7d and Biogas (2021)
24: 0 h, 100 rpm orbital production
agitation
Parachlorella kessleri 70 L NA, 29 ◦ C, 20 μmol 5 mg L− 1, 96.19%, Biodegradation Bioremediation Weis et al.
Photobioreactor m− 2 s− 1, 6.5–7.5 pH, 20 d (2020)
Glass shake flask 12: 12 h, 190 rpm in
orbital shaker
Chlorpyrifos Chlorella sp. and 250 mL Erlenmeyer BBM medium, 25 ◦ C, 1 mg L− 1, 61.9%, Sorption Bioremediation, Avila et al.
Scenedesmus sp. flask 31 μmol m− 2 s− 1, NA, 7d and Biogas (2021)
24: 0 h, 100 rpm orbital production
agitation
Chlorella vulgaris 5 L Photobioreactor BG-11 medium, 25 ◦ C, 0.5 mg L− 1, 87.2%, Biodegradation Bioremediation Mojiri et al.
containing biochar 100 μmol m− 2 s− 1, 7 3d Photocatalytic (2022)
pH, 12: 12 h, NA Degradation
Skeletonema costatum 250 mL Erlenmeyer F/2 medium, 20 ◦ C, 0.0572 mg L− 1, Biodegradation Bioremediation
Zhang et al.
flask 77.55 μmol m− 2 s− 1, 77.1%, ∼ 6 d
NA, 14: 10 h, NA (2023)
Cypermethrin Chlamydomonas 250 mL Erlenmeyer Tris-acetate-phosphate 600 μg L− 1, 98.3%, NA Bioremediation Yılmaz and
reinhardtii flask medium, 24 ◦ C, NA, 96 h Taş (2021)
NA, 16: 8 h, NA
Chlorella vulgaris Photobioreactor BG-11, 25 ◦ C, 100 0.5 mg L− 1, 93.4%, Biodegradation and Bioremediation Mojiri et al.
containing biochar μmol m− 2 s− 1, 7 pH, 3d Photocatalytic (2022)
12:12 h, NA Degradation
Chlorella sp. and 250 mL Erlenmeyer BBM medium, 25 ◦ C, 1 mg L− 1, 60.1%, Sorption Bioremediation, Avila et al.
Scenedesmus sp. flask 31 μmol m− 2 s− 1, NA, 7d and Biogas (2021)
24: 0 h, 100 rpm orbital production
agitation
Diazinon Chlorella sp. Glass cubic BG-11 medium, 25 ◦ C, 10–50 mg L− 1, Biodegradation Bioremediation Deng et al.
chamber 68 μmol m− 2 s− 1, NA, 57.20–61.66%, 12 (2022)
12: 12 h, NA d
Fenamiphos Chlorella vulgaris Erlenmeyer flask NA, 27 ◦ C, NA, 5–9 pH, 50 mg L− 1, Biosorption Bioremediation Reyad et al.
NA, NA 66.20%, 15 min (2022)
Imidacloprid Chlorella sp. Glass cubic BG-11 medium, 25 ◦ C, 50 mg L− 1, Biodegradation Bioremediation Deng et al.
chamber 92 μmol m− 2 s− 1, NA, 61.66%, 12 d (2022)
12: 12 h, NA
Chlorella vulgaris Erlenmeyer flask NA, 27 ◦ C, NA, 5–9 pH, 50 mg L− 1, Biosorption Bioremediation Reyad et al.
NA, NA 40.76%, 15 min (2022)
Nannochloropsis sp. Erlenmeyer flask F/2 medium, 25 ◦ C, 9.59 μg L− 1, 50%, Sorption Bioremediation Encarnação
100 μmol m− 2 s− 1, 8 20 h et al. (2021)
pH, 24: 0 h, NA
Scenedesmus sp. and 250 mL Erlenmeyer Synthetic wastewater, 20 mg L− 1, 9.71 %, Sorption and Bioremediation Cheng et al.
bacteria consortium flask 25 ◦ C, 20 μmol m− 2 s− 1, 15 d Biodegradation (2022b)
NA, 12: 12 h, NA
Scenedesmus sp. TXH 250 mL Erlenmeyer Synthetic wastewater, 20 mg L− 1, 71.25 Photo- Bioremediation Cheng et al.
and bacteria flask 25 ◦ C, 20 μmol m− 2 s− 1, %, 15 d biodegradation, (2022b)
consortium NA, 12: 12 h, NA Sorption and
Biodegradation
Ulva lactuca Erlenmeyer flask NA, 27 ◦ C, NA, 5–9 pH, 50 mg L− 1, Biosorption Bioremediation Reyad et al.
NA, NA 28.44%, 5 min (2022)
Lindane Chlorella sp. and 2 L Batch NA, 23 ◦ C, 150 μmol 10 μg L− 1, 99%, 10 Biodegradation Bioremediation Matamoros
Scenedesmus sp. bioreactors and 5 L m− 2 s− 1, 7.8–8.8 pH in d and Rodríguez
Continuous reactors continuous reactors (2016)
and 8.8–9.8 pH in
batch reactors, 12: 12
h, NA
Malathion Chlamydomonas 250 mL Flask BG-11 medium, 25 ◦ C, 200 mg L− 1, Biodegradation Bioremediation (Wan et al.,
reinhardtii 103 μmol m− 2 s− 1, NA, 96.2%, 10 d 2020)
12: 12 h, 120 rpm
incubator shaker
(continued on next page)

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Table 2 (continued )
Pesticide Microalgal species Scale of study Culture conditions Initial Mechanism Biomass Reference
(medium, temperature, Concentration, application
light, pH, photoperiod, removal
Agitation) percentage, time

Chlorella vulgaris 250 mL Erlenmeyer BBM medium, 27 ◦ C, 20 mg L− 1, 94 %, Biodegradation Bioremediation Kurade et al.
flask 40–50 μmol m− 2 s− 1, 12 d (2016)
NA, 150 rpm incubator
shaker
Chlorella sp. and 2 L batch NA, 23 ◦ C, 150 μmol 10 μg L− 1, 97%, 10 Biodegradation Bioremediation Matamoros
Scenedesmus sp. bioreactors and 5 L m− 2 s− 1, 7.8–8.8 pH in d and Rodríguez
continuous reactors continuous reactors (2016)
and 8.8–9.8 pH in
batch reactors, 12:12 h,
NA
Coccomyxa 250 mL Erlenmeyer BBM medium, 25 ◦ C, 0.15 mg mL− 1, ROS assisted Bioremediation Nicodemus
subellipsoidea flask 170 μmol m− 2 s− 1, NA, undetectable level, hydrolysis et al. (2020)
NA, gyrator shaker 10 d
Micractinium 500 mL Erlenmeyer BBM medium, 25 ◦ C, 25 mg L− 1, 90%, Intracellular Bioremediation Nanda et al.
pusillum, Chlorella flask 200 μmol m− 2 s− 1, NA 14 d metabolism (2019)
singulari, and 18: 6 h, NA
Chlorella sorokiniana
Nostoc muscorum 500 mL Erlenmeyer BG-11 medium, 28 ◦ C, 0.02–100 ppm, Biodegradation Bioremediation Ibrahim et al.
flask 40 μmol m− 2 s− 1, NA, 91%, 20 d (2014)
24: 0 h, continuous
shaking at 80 rpm
Oxadiazon Chlorella sorokiniana 500 mL Erlenmeyer BBM medium, 25 ◦ C, 25 ppm, 90%, 14 d Biodegradation Bioremediation Nanda et al.
flask 200 μmol m− 2 s− 1, NA (2019)
18: 6 h, NA
Oxamyl Chlorella vulgaris Erlenmeyer flask NA, 27 ◦ C, NA, 5–9 pH, 50 mg L− 1, Biosorption Bioremediation Reyad et al.
NA, NA 70.28%, 5 min (2022)
Scenedesmus sp. and Flask BG-11 medium, NA, 50 mg L− 1, 100%, Biodegradation Bioremediation Kumari et al.
Paenibacillus sp. NA, NA, NA, NA 3d (2020)
Ulva lactuca Erlenmeyer flask NA, 27 ◦ C, NA, 5–9 pH, 50 mg L− 1, Biosorption Bioremediation Reyad et al.
NA, NA 70.07%, 5 min (2022)
Paraoxon Coccomyxa 250 mL Erlenmeyer BBM medium, 25 ◦ C, 0.17 mg L− 1, ROS assisted Bioremediation Nicodemus
subellipsoidea flask 170 μmol m− 2 s− 1, NA, 14.7%, 10 d hydrolysis et al. (2020)
NA, Gyratory shaker is
used
Propanil Chlorella sp. and 10 L Pilot Mann and Myers 50 μg L− 1, 99%, 38 Biodegradation Bioremediation Avila et al.
Scenedesmus sp. Photobioreactor culture medium, 25 ◦ C, d and Biofuel (2022)
35 μmol m− 2 s− 1, production
8.8–9.6 pH, 14: 10 h,
100 rpm orbital shaker
Thiacloprid Chlamydomonas 250 mL Flask BG-11 medium, 25 ◦ C, 200 mg L− 1, Biodegradation Bioremediation Wan et al.
reinhardtii 103 μmol m− 2 s− 1, 6.8 96.2%, 10 d (2020)
pH, 12:12 h, 120 rpm
incubator shaker
Trichlorfon Chlorella sp. 500 mL Erlenmeyer BG-11 medium, 25 ◦ C, 40 μg L− 1, 83.0%, Biodegradation and Bioremediation Hu et al.
flask 100 μmol m− 2 s− 1, NA, 8d Photodegradation (2021)
12: 12 h, 180 rpm in
isothermal shaker
Scenedesmus sp. 250 mL Flask BG-11 medium, 25 ◦ C, 40 mg L− 1, Biodegradation Bioremediation Quan et al.
40 μmol m− 2 s− 1, NA, 96.81%, 12 d (2023)
12: 12 h, NA

*d: day; h: hour; min: minute; BBM: Bold’s Basal Medium; NA: Not Available; ROS: Reactive Oxygen species; rpm: rotations per minute.

Castellanos-Estupiñan et al. (2022) collected runoff water from rice degradation after 24 h of incubation (Tiwari et al., 2017). Singh et al.
production containing 15.3 mg L− 1 of chlorpyrifos. They found that (2013) investigated that Synechocystis sp. strains PUPCCC 64 cultivated
microalgae viz., Hapalosyphon sp., Scenedesmus sp., and Chlorella sp. in a culture medium containing 10 mg L− 1 of anilofos could biodegrade
showed overall chlorpyrifos removal efficiencies of 100%, 75%, and 79% anilofos on the 6th day of incubation. Chlamydomonas reinhardtii
50%, respectively. grown in BBM could effectively remove 96.2 % of 200 mg L− 1 of
Reyad et al. (2022) compared the pesticide removal efficiencies of trichlorfon in 10 days through biodegradation (Wan et al., 2020). Nanda
C. vulgaris and Ulva lactuca from contaminated water samples containing et al. (2019) evaluated the ability of a marine microalga Dunaliella salina
imidacloprid, fenamiphos, and oxamyl. C. vulgaris and Ulva lactuca for pesticide removal in sterilized well water supplemented with four
removed 66.20% and 61.91% of fenamiphos, 40.76% and 28.44% of organophosphate pesticides from the well water. The results revealed
imidacloprid, and 70.28% and 70.07% of oxamyl, respectively (Reyad that Dunaliella salina could eliminate diazinon (70.25%), profenofos
et al., 2022). Shinde (2021) studied the influence of furadan and rogor (53.89%), ethion (47.65%), and chlorpyrifos (41.84%), respectively, at
on the blue-green algae by growing them at 100 μg L− 1 dose and found an initial concentration of 5 mg L− 1 concentration of pesticides (Nasiri
no adverse effect on their growth. Nannochloris oculata grown in BBM et al., 2023).
medium with 0.1 mg L− 1 and 0.5 mg L− 1 lindane showed removal ef­ Microalgal synergistic interactions may improve the current bio­
ficiencies of 73% and 68.2%, respectively, during seven days of incu­ logical wastewater treatment system by increasing nutrient absorption
bation (Pérez-Legaspi et al., 2016). Fischerella sp. grown in BG-11 and resilience to unfavorable conditions (Chan et al., 2022). The
medium containing 20 mg L− 1 of methyl parathion displayed 80% microalgal consortia for bioremediation of pesticides offer many

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T. Fayaz et al. Journal of Environmental Management 357 (2024) 120723

benefits as an environmentally friendly method that produces biomass, for studying microalgae removal efficiencies in different studies
which can be used as bioenergy (Sheng et al., 2022). The microalgal (Table 2). Microalgal strains such as Chlorella vulgaris, Chlorella sor­
consortium of Scenedesmus sp. and Chlorella sp. removed 74% cyper­ okiniana, Chlamydomonas reinhardtii, Scenedesmus sp., etc. have shown
methrin, 88% oxadiazon, and 97% chlorpyrifos from the liquid phase, high pesticide tolerance and removal efficiencies (Table 2). These
which was cultured in BBM with 1 mg L− 1 of pesticide (Avila et al., microalgal strains can tolerate 100–200 mg L− 1 of pesticides with a
2021). The combined use of photobioreactor and cork filter removed removal efficiency of ≥90%. Thus, it can be presumed that microalgae
97% and 98% of atrazine and bromacil in 12 days at an initial concen­ can easily remove environmentally relevant pesticide concentrations
tration of 100 μg L− 1, respectively, when inoculated with without any growth inhibition. The researchers should also focus on
co-immobilized microalgae and bacteria consortium with Scenedesmus environmentally relevant concentrations of pesticides and consideration
obliquus being the dominant species (Rambaldo et al., 2022). Another of multiple wastewater contaminants and factors to prove the com­
report revealed that the algal consortia grown in BG-11 media con­ mercial feasibility of microalgae-mediated pesticide remediation.
taining 50 μg L− 1 of lindane removed 100% after 72 h of incubation
(Kumari et al., 2020). There is limited information on the efficiency of 3. Mechanisms and factors influencing pesticide removal
microalgae for pesticide removal in original wastewater (Abdelrazek
et al., 2019). Abdelrazek et al. (2019) evaluated the potential of a The minuscule size of the microalgal cell provides a large surface
microalgal consortium of Chlorella vulgaris, Scenedesmus quadricuda, and area to make contact with pesticide compounds for detoxification. Two
Spirulina platensis for the bioremediation of pesticide malathion and essential processes involved in pesticide removal using microalgae are
heavy metals (cadmium, nickel, lead) from the mixture of urban biodegradation and sorption (bioadsorption, bioabsorption, and bio­
wastewater, agricultural wastewater, and their combinations in accumulation) (Fig. 2). Hazardous molecules attached to the microalgal
different glass aquaria with a working volume of 10 L. The microalgal cell surface through bio-adsorption are passive and independent of
consortium could remove 95%, 85%, and 99% of pesticide malathion metabolic activity (Saket et al., 2022). The cell surface of microalgae
from the urban, agricultural, and combined wastewater, respectively. constitutes a negative charge due to functional groups like hydroxyl,
Limited information on pilot scale evaluation of microalgal efficiency for amine, phosphoryl, and carboxyl group (-OH, –NH2, -PO2- 3 and -COO ,
-

pesticide removal on original wastewater under indoor and/or outdoor respectively) which facilitates the attachment of toxic compounds with a
conditions emphasizes the need for future studies to prove the com­ net positive charge and allows their sorption (Xiong et al., 2018). The
mercial viability of the technology. However, there are studies that have biodegradation method employs enzymes as catalysts to transform a
proven the potential of microalgae for wastewater treatment and pesticide or any other complex compound into less dangerous forms
biomass production in photobioreactors and raceway ponds under in­ (Dubey et al., 2023). Malathion exposure enhanced the activity of the
door and outdoor conditions at the pilot scale (Tan et al., 2021; Naaz carboxylesterase enzyme in Chlorella sorokiniana, which helped in the
et al., 2019; Van Den Hende et al., 2014; Nobre et al., 2024). degradation of malathion by releasing phosphate as one of the degra­
The efficiency of microalgae in removing a pesticide depends upon dation products (Nanda et al., 2019). Mojiri et al. (2022) obtained
the concentration of pesticide, type of pesticide, type of algal strain, and similar findings, revealing that the enzyme carboxypeptidase acts as a
growth conditions (Table 2). It is clear from the studies presented in catalytic hydrolase in microalgae to aid in the degradation of cyper­
Table 2 that microalgae can remove a wide range of pesticides at methrin and chlorpyrifos. The exact mechanism of enzymatic degrada­
different concentrations in the aqueous environment. However, envi­ tion is unknown; however, esterase, cytochrome P450, transferase,
ronmentally relevant concentrations of pesticides reported in different oxygenase hydrolase, oxidoreductase, phosphotriesterase, and
studies (Supplementary Fig. S1) are usually not higher than those used phosphatase-like enzymes may have a role in biodegradation (Laura

Fig. 2. Mechanisms of pesticide removal and cellular responses of microalgae towards pesticide stress (Adewuyi, 2020; Nanda et al., 2019; Quan et al., 2023).

6
T. Fayaz et al. Journal of Environmental Management 357 (2024) 120723

et al., 2013). Some pesticides have a functional group interacting with of eliminating pesticides from the aquatic environment (Cheng et al.,
these enzymes and metabolizing them (Coleman et al., 1997; Pang et al., 2022a; Liu and Yildiz, 2018). These factors vary among the microalgae
2012). Detailed mechanisms of pesticide removal have also been and are specific for each microalgal strain to increase their overall
reviewed in previous publications (Morais et al., 2022; Nie et al., 2020; bioremediation capability. Different biochemical approaches, such as
Singh et al., 2022). carbon supplementation and phytohormones, have been reported to
Different studies in Table 2 indicate that microalgae can potentially enhance the bioremediation potential of microalgae for pesticide
remove pesticide pollutants. However, the bioremediation capability removal. Optimized cultural conditions may promote the activation of
varies among the microalga strains and depends upon various factors. enzymes that facilitate the metabolism and degradation of pollutants,
Culture conditions such as light, temperature, CO2 concentration, pH, thereby increasing the efficiency of pesticide degradation processes.
and medium composition may influence microalgae bioremediation However, limited studies are available on the molecular mechanisms
capability (Binnal and Babu, 2017; Sutherland et al., 2015). Carbon involved in improving microalgal efficiency using different approaches.
supplementation in the form of CO2 and organic sources up to the It would be helpful to have more research and information on this topic
threshold concentrations can improve the bioremediation potential of to understand better how microalgal efficiency can be further improved
microalgae; however, further increases in the concentration have been for their utilization for pesticide removal.
reported to reduce their removal efficiency. For example, adding a
carbon source (glucose, saccharose, and glycine) in the medium at a 4. Effect of pesticides on microalgal growth and metabolism
concentration of 300 mg L− 1, increases exopolymeric substances and
enzyme concentration by 2–100 folds in Chlorella sp. This increased the The recycled microalgae-derived biomass after wastewater treat­
removal efficiency of tetracycline, bisphenol, and sulfamethoxazole ment has been proposed as a sustainable solution to improve the eco­
(16–99%, 58–99%, and 32–92%, respectively) as compared to the nomic and environmental feasibility of microalgae-mediated
control (27–41%) (Vo et al., 2020). Zhao et al. (2019) observed that bioremediation technology (Liu and Hong, 2021). Microalgae are
Tetraselmis cordiformis cultivated in BG-11 medium supplemented with diverse species with enormous potential to be a promising biomass
indole-3-acetic acid, zeatin, and brassinosteroid (concentration used feedstock for various purposes (Abdul-Latif et al., 2020; Wells et al.,
10− 5, 10− 7 and 10− 9 M, respectively), enhanced total phosphorous and 2017). Microalgal biomass can synthesize bioplastics, pigments, nutra­
nitrogen use efficiency by 53.2% and 184.3%, respectively, compared to ceuticals, biofuels, animal feed, food, fertilizers, etc. (Levasseur et al.,
the culture without phytohormones. Similarly, phytohormone supple­ 2020; C. Zhang et al., 2019a). However, micropollutants like pesticides
mentation can effectively improve microalgae growth, biomass pro­ can impact microalgal biochemical composition that directly impact
ductivity, and bioremediation of environmental organic contaminants their biomass applications.
(Gao et al., 2022; Wang et al., 2023). Plant hormones like gibberellic Pesticides have varying effects on the biochemical content and
acid stimulate the degradation of organic pollutants and tolerance effi­ growth of microalgae (Table 3). At lower concentrations, pesticides are
ciency of microalgae by increasing the expression of antioxidase-related found to be less toxic, slightly toxic at moderate concentrations, and
genes (Yang et al., 2023). highly toxic at high concentrations (Lu et al., 2021). Pesticides can affect
The influence of light intensity and photoperiod on four microalgal the microalgal morphology, biochemical composition, and genetic di­
strains (Synechocystis salina, Microcystis aeruginosa, Chlorella vulgaris, and versity, altering gene expression (De Souza et al., 2023). Pesticide stress
Pseudokirchneriella subcapitata) was studied. Lower light intensity (36 under varied concentrations substantially affects microalgal growth,
and 60 μm− 2 s− 1) and photoperiod of 10:14 (light: dark) showed low pigments, the amounts of proteins, carbohydrates, lipids, and dry weight
total nitrogen removal. Whereas more than 70% removal of nitrogen is (Fernández-Naveira et al., 2016). Raphidocelis subcapitata exposed to
seen under high light intensity (120 and 180 μm− 2 s− 1) and photoperiod diflufenican for 72 h at a concentration of 10 ng L− 1 showed no adverse
of 14:10 (light: dark) (Gonçalves et al., 2014). The pH values can either effect on the photosynthetic activity, pigment composition, and growth
promote or impede the bioremediation of pollutants by the microalgae (Gómez-Martínez et al., 2023). However, high concentrations of diflu­
(Sutherland et al., 2015). Low pH reduces the bioremediation potential fenican (310 ng L− 1) were highly toxic and suppressed the genes
of heavy metals. Microalgae exhibit a significant increase in the involved in cellular division, DNA repair, and replication. Another study
adsorption of heavy metals when the pH is increased (Yan et al., 2022). showed low concentrations of imidacloprid and acephate (up to 15 mg
Acutodesmus acuminatus grown at 40 ◦ C and 4.7 pH resulted in maximum L− 1) increased the microalgal growth rate, while concentrations above
adsorption of europium (Furuhashi et al., 2019). Salinity is another 15 mg L− 1 readily declined the growth of Chlamydomonas mexicana
determining physical factor for microalgae-mediated bioremediation (Kumar et al., 2016). The lipid concentration was increased by 17%
(Liu and Yildiz, 2018). In Dunaliella salina, an enhanced nutrient when Chlorella sorokiniana was grown at high glyphosate concentrations
removal efficiency was observed when the salinity level was increased of 30 mg L− 1, although the growth was inhibited (Jaiswal et al., 2020).
from 20 ppt to 30 ppt. A downfall was seen in the further increase in Chlorella sp. was tolerant to imidacloprid at 10–50 mg L− 1 concentra­
salinity to 40 ppt, but when moving to 40 ppt, phosphorus removal tions and showed an efficient increase in biomass production (Deng
decreased from 63% to 21.3% (Liu and Yildiz, 2018). et al., 2022).
Similar studies have been reported in microalgae to enhance pesti­ Several genes involved in growth, photosynthesis, protein and en­
cide removal efficiency by optimizing cultural conditionsand modifying ergy metabolism, signal transduction, redox homeostasis, and mecha­
other physical factors (Cheng et al., 2022a; Du et al., 2023). The high nistic cellular defense are altered by pesticide exposure in microalgae
light intensity has been reported to enhance microalgal pesticide (Tiwari et al., 2018). When Chlorella sp. was exposed to cypermethrin
removal ability and tolerance capability (Du et al., 2023). Scenedesmus (16.22 mg L− 1), it was observed that the proteins involved in cell divi­
sp. was grown in synthetic wastewater with 20 mg L− 1 and 60 mg L− 1 of sion, nucleotide and amino acid biosynthesis, stress response, secondary
imidacloprid at a light intensity of 20 μmol m− 2 s− 1 and 60 μmol m− 2 metabolite production, photosynthesis, lipid metabolism, transporters,
s− 1. It was revealed that Scenedesmus sp. could not remove imidacloprid signal transduction, translation, post-translational modification, and
beneath 20 μmol m− 2 s− 1 of light, but at 60 μmol m− 2 s− 1 of light in­ transcription were significantly accumulated (Chanu et al., 2023). The
tensity, more than 90% removal rate was achieved (Cheng et al., 2022a). low concentrations of pesticides promote growth slightly, while a more
For the effective microalgal bioremediation of pesticides, it is necessary significant concentration severely inhibits microalgae growth and in­
to understand the abiotic and biotic factors influencing duces oxidative stress (Quan et al., 2023; Zhang et al., 2014).
microalgae-mediated pesticide bioremediation. Different factors, such Chlorella vulgaris subjected to 4–50 mg L− 1 of mesotrione revealed
as light intensity, temperature, nutrient availability, microalgal that lower concentrations of mesotrione have no significant effect on
biomass, pesticide concentration and composition affect the success rate Chlorella vulgaris. However, higher concentrations strongly inhibited the

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T. Fayaz et al. Journal of Environmental Management 357 (2024) 120723

Table 3 Table 3 (continued )

Different studies on the impact of pesticides on microalgae growth and Microalgal strain Pesticide, Impact on Reference
physiology. exposure time, microalgae
Microalgal strain Pesticide, Impact on Reference initial
exposure time, microalgae concentration
initial Chlorella Chlorpyrifos,72 Growth inhibition Chen et al. (2016)
concentration pyrenoidosa h, 2.4–38.4 mg was concentration-
Chlamydomonas Atrazine, 96 h, Growth was Fernández-Naveira L− 1 dependent; SOD
reinhardtii 0.1–0.5 μM unaffected by et al. (2016) started to decline
concentrations at 2.4 mg L− 1
below 0.1 μM, concentration, and
although the between 2.4 and
decline in growth, 4.8 mg L− 1, CAT
pigment levels, enzyme increased
and nitrate but decreased
reductase activity upon further
occurred at greater increase in
concentrations. concentration.
Chlamydomonas Fluroxypyr, 120 Growth increased Zhang et al. (2011) Chlorella Malathion, 14 d, Reduction of cell Nanda et al. (2019)
reinhardtii h, 0.50–1 mg L− 1 at the initial sorokiniana 25–100 mg L− 1 size and biomass
concentration but productivity at
decreased at 100 ppm; increase
higher lipid productivity
concentrations; and pigment at 50
SOD, APX, and ppm; decreased
GST increased as protein and
the concentration carbohydrate
increased, while contents with
CAT dropped. increased
Chlamydomonas Atrazine, 96 h, Growth and Esperanza et al. malathion
reinhardtii 0.25 μM pigment content (2015) concentration; and
decreased; ROS increased ROS
considerably production
increased; 124 Dunaliella salina Diazinon and No significant Nasiri et al. (2023)
genes’ expression Ethion, 17 d, change occurs in
levels were 0.1–10 mg L− 1 the growth rate
downregulated, Dunaliella salina Chlorpyrifos and The growth rate Nasiri et al. (2023)
whereas 61 genes’ Profenofos,17 d, declined with the
expression levels 0.1–10 mg L− 1 increasing
were up-regulated. concentration
Chlamydomonas Cypermethrin, Increased growth Yılmaz and Taş Nannochloris Lindane, 96 h, Between 0.1 and Pérez-Legaspi et al.
reinhardtii 96 h, 150− 600 at 150 μg L− 1; (2021) oculata 0.1–2.5 mg L− 1 0.5 mg L− 1 (2016)
μg L− 1 however, higher biomass increased;
concentrations above 0.5 mg L− 1,
(300–600 μg L− 1) biomass decreased
showed a toxic with increasing
effect, and concentration
inhibited growth Skeletonema Cypermethrin, Algal growth, Wang et al. (2012)
and costatum, 96 h, 1–205 μg protein content,
photosynthesis. Scrippsiella, L− 1 and superoxide
Chlamydomonas Bifenox and After 24-h Almeida et al. trochoidea, and dismutase (SOD)
reinhardtii metribuzin, 4 exposure, ROS was (2019) Chattonella activity are
d (2 × 103 nM to enhanced, reduced marina enhanced at low
1 × 105 nM) glutathione, lipid doses (1–5 μg L− 1)
peroxidation, and inhibited at
photosystem II high quantities
(PSII) (>50 μg L− 1),
performance, and which also
loss of increases
photosynthetic malondialdehyde
pigments. and ROS content.
Chlorella sp. Cypermethrin, Significant growth Baruah and
*h: hour; SOD: superoxide dismutase; CAT: catalase; APX: ascorbate peroxidase;
96 h, 6− 48 mg inhibition, Chaurasia (2020)
GST: glutathione s-tansferase
L− 1 enhanced
generation of ROS,
intracellular lipid growth and photosynthetic activity by downregulating the
accumulation, photosynthesis-related genes and the cell pigment content (Zhang et al.,
decreased
photosynthetic
2020). Chlorella sacchararophila unexpectedly displayed an increase in
pigment content, growth at low concentrations (20–80 μg L− 1) of 3-(3,4-dichlor­
and increased o-phenyl)-1,1-dimethyl-urea (Xie et al., 2023). Chlamydomonas rein­
antioxidant hardtii exposed to paraquat 0.05–0.25 μM, showed no significant
enzyme activity
changes in gene expression at lower concentrations. However, sub­
and
malondialdehyde stantial changes occur when concentration increases. The gene expres­
content. sion of glutathione S transferase, catalase, peroxiredoxin, and
mitogen-activated protein kinase was up-regulated during the para­
quat stress. In contrast, ascorbate peroxidase, a cyclin-dependent kinase

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T. Fayaz et al. Journal of Environmental Management 357 (2024) 120723

inhibitor, glutaredoxin, photosystem I reaction center subunit II and XI, the techno-economic analyses of wastewater treatment of different types
photosystem II reaction centre W protein, thioredoxin, etc. were of wastewater using several microalgal strains and demonstrated the
downregulated (Jamers and De Coen, 2010). Hence, microalgae show economic feasibility of the technology (Kumar et al., 2020; Ranganathan
the variable effects of pesticides on gene expression and biomass pro­ and Savithri, 2019; Shukla et al., 2022). For instance, a techno-economic
duction, depending upon the pesticide type, pesticide application, and analysis conducted on a wastewater treatment plant in northern
microalgae strain. Portugal by integrating Chlorella vulgaris as tertiary treatment could
The exposure of microalgae to pesticides leads to an increase in the result in a yearly gross profit of approximately 619,100 € (Nobre et al.,
ROS produced as a stress response, which may result in cellular damage 2024). Recently, (Vázquez-Romero et al., 2024) conducted a
(Esperanza et al., 2015). Glufosinate supplemented in Chlorella vulgaris techno-economic analysis of using microalgae for the treatment of
culture at a concentration of 10 μg L− 1 induced oxidative stress along aquaculture-generated wastewater in a 10-ha area. They revealed that
with an increase in malondialdehyde concentration and the activity of the treatment expenses can vary between 1.37 and 1.66 € m− 3, with up
ascorbate peroxidase (APX), superoxide dismutase (SOD), and catalase to 81% of the treatment costs being covered by the revenue generated by
(CAT). Meanwhile, the gene expression related to photosynthesis was the biomass. These studies indicated that microalgae-mediated waste­
significantly dropped (Qian et al., 2008). Increased antioxidant activity, water treatment is economically viable at an industrial scale, and the
including that of the enzymes APX, CAT, and SOD, suggested that generated biomass can considerably cover the costs incurred.
microalgae develop a defense mechanism against pesticide stress The biomass obtained from microalgae after wastewater treatment
(Kumar et al., 2016). The harmful effect of ROS can be reversed by the systems has many industrial applications (biofuels, biofertilizers,
upregulation of genes that codes for antioxidant enzymes such as APX, aquafeed, etc.), which helps mitigate the cost of this innovative
CAT, and SOD (Jin et al., 2012). The free radical, such as O−2 anion, is approach (Yap et al., 2021; Ferreira et al., 2024). The studies showed
first converted into O2 and H2O2 by SOD, then CAT catalyzes the con­ that some microalgae have high bioremediation capability for pesticide
version of H2O2 into H2O and O2. At the same time, APX plays a role in removal but lower biomass production or vice-versa (Nanda et al., 2019;
the ascorbate-glutathione cycle, alleviating stress (Mittler et al., 2004). Castellanos-Estupiñan et al., 2022). Pesticide stress can induce meta­
This defense is crucial for microalgal cells and protection against bolic changes in the microalgal cells, decreasing microalgal biomass
pesticide-induced oxidative stress. productivity and altering biochemical composition. These predicaments
can be overcome using emerging approaches, such as co-culture, gene
5. Discussion and perspectives editing, genetic engineering, etc. (Fig. 3).
The genome of microalgae can be successfully modified through
Microalgae bioremediation is a promising technology that uses their genetic engineering methods like transcription activator-like effector
inherent capacity to eliminate environmental pollutants. Along with nucleases, clustered regulatory interspaced short palindromic repeats
pesticides, many other emerging contaminants, such as heavy metals, (CRISPR-Cas9), and zinc-finger nucleases to improve growth rate, in­
pharmaceuticals, dyes, etc., can be effectively removed from aquatic crease resistance to environmental contaminants, improve bioremedia­
environments by microalgae. Most studies on microalgal bioremediation tion capability, and improve specific products like lipids, carbohydrates,
of pesticides are carried out under controlled conditions in the labora­ etc. for different industrial applications (Patil et al., 2022). By altering
tory, showing high removal efficiency and biomass productivity their genomes, numerous microalgae have achieved desirable charac­
(Table 2). Nevertheless, choosing appropriate strains for particular teristics. For example, in Chlamydomonas reinhardtii, knocking out
environment and culture conditions with high removal efficiency and phospholipase A2 using CRISPR-Cas9 technology increased lipid pro­
biomass productivity is essential to make this treatment more cost- duction up to 64.25% without negatively impacting growth (Shin et al.,
effective and practically feasible on a large scale. Large-scale micro­ 2019). Similarly, significantly improved lipid content was observed in
algae cultivation requires photobioreactors and high-rate algal ponds Coccomyxa sp. strain Obi by changing the gene expression for the large
that are exposed directly to the environment and, thus, can be prone to subunit of ATP: α-d-glucose-1-phosphate adenylyl transferase by using
contamination and predators, leading to declined productivity. Hence, the transcription activator-like effector nuclease technique (Takahashi
scaling up is essential for the advancement of this technology and more et al., 2018). In Euglena gracilis, the glucan synthase-like gene was suc­
emphasis should be given to evaluating the efficiency of algal systems on cessfully modified using CRISPR-based gene targeting technology (Chen
a large scale under outdoor conditions. et al., 2022). Thus, genome editing of microalgae can be a promising tool
Utilization of industrial or sewage wastewater for microalgae culti­ for strain stability and improvement of industrially relevant traits
vation at pilot scale in photobioreactors and raceway ponds has been (Sproles et al., 2021). However, engineering microalgal strains for
reported not only to remediate contaminants but also to enhance bioremediation applications is still in its early phases (He et al., 2011;
microalgal biomass productivity (Cheng et al., 2022a; Naaz et al., 2019; Ranjbar and Malcata, 2022). Future research can concentrate on
Shahid et al., 2020, 2021; Tan et al., 2021; Wang et al., 2022; Rossi et al., developing engineered microalgal strains that are more tolerant to
2022). Pesticide supplementation at lower concentrations in the culture specific contaminants including pesticides, possess higher contaminant
media for microalgae cultivation at laboratory scale studies is found to removal efficiency, and have higher biomass production for industrial
enhance biomass production with efficient pesticide removal (Chang applications. The engineered microalgal strains can be made more
et al., 2023). Nevertheless, to achieve the cost-effectiveness of micro­ acceptable for bioremediation by conducting environmental risk
algal technology for pesticide removal, the cost of using microalgae for assessment studies and addressing controversies.
wastewater treatment must be carefully considered (Vázquez-Romero Choosing an appropriate microalgal strain or developing an
et al., 2022). The microalgal strains to be utilized must be wisely chosen improved strain using genetic engineering having high bioremediation
based on their growth rate, environmental tolerance to contamination, efficiency, biomass productivity, and increased carbon sequestration
nutritional requirements, biochemical composition, and the final prod­ efficacy can assist in making this process economically feasible. It also
uct (Hussain et al., 2021; Koul et al., 2022). For this, techno-economic necessitates improvements in farming, harvesting, and processing
analysis (costs of cultivation, energy consumption, productivity, har­ methods. Optimizing culture conditions can also advance the bioreme­
vest, capital investment, operational expenditures, and income genera­ diation potential of microalgae (Rezvani et al., 2018). Culture conditions
tion) is required to prove the feasibility and sustainability at an such as light intensity, photoperiod, and adding a co-substrate like CO2,
industrial scale (Vázquez-Romero et al., 2022). However, there is no and phytohormone, strongly influence the bioremediation potential and
available information on techno-economic analysis on the use of biomass productivity of microalgae (Table 2). Recent research has
microalgal technology for wastewater treatment of pesticide-containing revealed that hybrid microalgae systems can be an emerging
wastewater at a pilot scale. Numerous studies have been carried out on cutting-edge technique to boost the effectiveness of microalgae

9
T. Fayaz et al. Journal of Environmental Management 357 (2024) 120723

Fig. 3. Schematic representation of the challenges of microalgae cultivation in pesticide-containing wastewaters and emerging approaches to overcome
these challenges.

bioremediation (Xiong et al., 2021). The hybrid system of microalgae 6. Conclusion

bioremediation uses microalgae in addition to other systems, including a
combination of microalgal remedies using photobioreactors, open Microalgal systems show a positive outlook for pesticide removal as
ponds, biofilters with artificial wetlands, sophisticated oxidation tech­ an environmentally friendly, cost-effective, and efficient technological
niques, etc. (De Mendonça et al., 2018; Khurana et al., 2021; Leong and alternative to conventional and advanced wastewater treatment
Chang, 2020). Pesticides used for agricultural land leach into the methods, as the biomass generated can be utilized for industrial appli­
groundwater or runoff directly into the water streams, making it chal­ cations. However, pesticide stress may alter microalgal gene expression
lenging to be treated by microalgal systems (Dugan et al., 2023). and biochemical composition and compromise its use for commercial
However, it may be possible to collect the agricultural runoff and bio­ applications. Most microalgal strains show a hormesis effect on their
remediate on the collection site using microalgal systems. growth in the presence of pesticides. The pesticide stress may induce
Furthermore, various studies have also indicated that the use of oxidative stress in the microalgal cell, which can be reversed by SOD,
indigenous microalgal strains can be beneficial in ensuring high pesti­ ROS, and APX enzymes of the microalgal metabolic system. Emerging
cide removal efficiency and biomass productivity because indigenous biochemical and molecular methods can be employed to improve
strains show higher resilience to environmental changes and can adapt bioremediation potential and biomass production of microalgae under
to fluctuations in conditions such as temperature, pH, light, specificity of pesticide stress. More information is needed to develop efficient ap­
contaminants, and nutrient levels (AlMomani and Örmeci, 2016; proaches for enhancing microalgal efficiency for pesticide removal and
Romero-Villegas et al., 2021). The microalgae are reported to show a their implementation at the commercial scale.
mutualistic relationship with the indigenous microorganisms present in
the wastewater, leading to enhanced contaminant removal efficiency CRediT authorship contribution statement
(Choudhary et al., 2016). Thus, this necessitates more research to un­
derstand the complex association of microalgae with other organisms for Tufail Fayaz: Writing – review & editing, Writing – original draft,
further optimizing the efficiency of microalgal technology at the pilot Data curation, Conceptualization. Soujanya S. Rana: Writing – original
scale. Microalgae pesticide remediation efficiency studies were con­ draft, Data curation. Esha Goyal: Writing – original draft, Data curation.
ducted either on standard culture media or synthetic wastewater, and Sachitra Kumar Ratha: Writing – review & editing, Validation,
the removal efficiency of pesticides has not been reported in the original Conceptualization. Nirmal Renuka: Writing – review & editing, Writing
wastewater at the demonstration scale. In addition, more than one – original draft, Validation, Supervision, Conceptualization.
pesticide or multiple types of contaminants are present in the original
wastewater, which can impact the microalgal efficiency for pesticide Declaration of competing interest
removal. Thus, future research on investigating the bioremediation po­
tential of microalgae for pesticide removal in original wastewater on a The authors declare that they have no known competing financial
pilot scale is important to prove their wastewater treatment potential at interests or personal relationships that could have appeared to influence
a commercial level. More than 1000 pesticides are used worldwide, the work reported in this paper.
having different chemical compositions (WHO, 2022). The microalgal
degradation products of these pesticides are not the same. Hence, it is Data availability
also essential to analyze whether these degradation products are more or
less toxic to their parent compounds. Pesticide degradation by envi­ Data will be made available on request.
ronmental factors can produce secondary pollutants. Thus, the ability of
microalgal systems can also be assessed for their capability to remove
these secondary pollutants.

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T. Fayaz et al. Journal of Environmental Management 357 (2024) 120723

Acknowledgments Borràs, N., Oliver, R., Arias, C., Brillas, E., 2010. Degradation of atrazine by
electrochemical advanced oxidation processes using a boron-doped diamond anode.
J. Phys. Chem. A 114, 6613–6621. https://doi.org/10.1021/jp1035647.
Author Tufail Fayaz (Grant number: 202021-JK04602587) and Esha Carazo-Rojas, E., Pérez-Rojas, G., Pérez-Villanueva, M., Chinchilla-Soto, C., Chin-
Goyal (Grant number: 221610125980) are thankful to the University Pampillo, J.S., Aguilar-Mora, P., Alpízar-Marín, M., Masís-Mora, M., Rodríguez-
Grants Commission, Govt. of India for PhD fellowship. Author Nirmal Rodríguez, C.E., Vryzas, Z., 2018. Pesticide monitoring and ecotoxicological risk
assessment in surface water bodies and sediments of a tropical agro-ecosystem.
Renuka is thankful to the Central University of Punjab, Bathinda, India Environ. Pollut. 241, 800–809. https://doi.org/10.1016/j.envpol.2018.06.020.
for providing research seed money (Grant number: CUPB/Acad./2022/ Castellanos-Estupiñan, M., Carrillo-Botello, A., Rozo-Granados, L., Becerra-Moreno, D.,
1194). Author Sachitra Kumar Ratha is thankful to the Director, CSIR- García-Martínez, J., Urbina-Suarez, N., López-Barrera, G., Barajas-Solano, A.,
Bryan, S., Zuorro, A., 2022. Removal of nutrients and pesticides from agricultural
National Botanical Research Institute, Lucknow, India. All the authors runoff using microalgae and cyanobacteria. Water 14, 558. https://doi.org/
are thankful to the Central University of Punjab, Bathinda for providing 10.3390/w14040558.
research facilities. Chan, S.S., Khoo, K.S., Chew, K.W., Ling, T.C., Show, P.L., 2022. Recent advances
biodegradation and biosorption of organic compounds from wastewater: microalgae-
bacteria consortium - a review. Bioresour. Technol. 344, 126159 https://doi.org/
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Chang, X., He, Y., Song, L., Ding, J., Ren, S., Lv, M., Chen, L., 2023. Methylparaben
toxicity and its removal by microalgae Chlorella vulgaris and Phaeodactylum
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