Annual Research & Review in Biology 9(4): 1-39, 2016, Article no.ARRB.22614 ISSN: 2347-565X, NLM ID: 101632869

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Toxicological Impact of Herbicides on Cyanobacteria

D. P. Singh 1* , J. I. S. Khattar 1, Gurdeep Kaur 1 and Yadvinder Singh 2

1Department of Botany, Punjabi University, Patiala-147002, Punjab, India. 2Department of Botany and Environment Science, Sri Guru Granth Sahib World University, Fatehgarh Sahib-140406, Punjab, India.

Authors’ contributions

This work was carried out in collaboration between all authors. All authors read and approved the final manuscript.

Article Information

DOI: 10.9734/ARRB/2016/22614 Editor(s): (1) George Perry, Dean and Professor of Biology, University of Texas at San Antonio, USA. (2) Reviewers: (1) Petigrosso Lucas Ricardo, Universidad Nacional de Mar del Plata, Argentina. (2) Shelley Gupta, Pune University, India. (3) Kowthar Gad Aly El-Rokiek, National Research Centre, Egypt. (4) Rosilaine Araldi de Castro, Laboratorio Nacional de Ciencia e Tecnologia do Bioetanol, Brazil. Complete Peer review History: http://sciencedomain.org/review-history/13074

Received 14 th October 2015 th Review Article Accepted 5 January 2016 Published 25 th January 2016

ABSTRACT

The use of herbicides in modern agriculture to eradicate weeds has led to serious environmental contamination resulting in a loss of growth and development of many beneficial micro-organisms. Low cost, easy availability, lax in regulatory mechanism have contributed to the continuous use of the herbicides in tropical and subtropical regions. The removal of these herbicides from soil and aquatic systems is a difficult task and as a result herbicides persist in these ecosystems for a long period of time. Cyanobacteria are a diverse group of gram-negative photosynthetic prokaryotes. Their life processes require only water, carbon dioxide, inorganic substances and light and these organisms contribute greatly to terrestrial as well as aquatic ecosystems through their ability to increase soil fertility by adding nitrogen, enhancing water holding capacity, releasing vitamins and plant stimulating hormones, adding extra cellular polysaccharides and by solubilizing phosphates. The present paper review responses of cyanobacteria to herbicides and impact of herbicides on photosynthetic pigments, photosynthesis and nitrogen assimilation by cyanobacteria. The tolerance mechanisms and herbicide biodegradation potential of cyanobacteria are also reviewed.

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*Corresponding author: E-mail: [email protected];

Singh et al.; ARRB, 9(4): 1-39, 2016; Article no.ARRB.22614

Keywords: Cyanobacteria; herbicide; photosynthesis; respiration; antioxidant system; biodegradation.

1. INTRODUCTION agriculture sector also poses a great threat to micro flora of soil ecosystem [9]. Feeding of over nine billion people expected to inhabit our planet by 2050 will be an Herbicides which are used not only in agriculture unprecedented challenge for all human beings but also for many other purposes can enter [1]. The production of enough food for the human aquatic ecosystems as a result of terrestrial population across the globe in 2050 will be runoff, and to a lesser extent, of direct application possible but at an unacceptable cost. In view of and aerial spraying [10]. Thus, microbial the world’s limited croplands and growing communities in freshwater ecosystems including population [2], it is necessary to take all agri-ecosytem are directly or indirectly affected measures to increase crop production in order to by these compounds. For example, many ensure food safety [3]. This will largely depend commercial herbicides act by binding to upon the agro-research from high quality seeds Photosystem II (PS-II), which is a pigment- to low cost farming practices [4]. More than 8,000 protein membrane complex [11]. PS-II inhibitors species of weeds, 9,000 species of insects and have a direct impact on photosynthetic aquatic pests and 50,000 species of plant pathogens microorganisms that contain the same PS-II damage agricultural crops across the globe. To apparatus as the terrestrial weeds targeted by this loss, weeds account for 13% loss. Insect these herbicides. Beside this direct impact on pests and plant pathogens cause an estimated photosynthetic microorganisms, herbicides can loss of 14% and 13%, respectively [5]. It has also have an indirect impact on non- been estimated that without pesticide application, photosynthetic species that are not susceptible to the loss of cereals, vegetables and fruits from PS-II inhibitors. These effects on microbial pest injury would reach 32, 54 and 78%, communities can have a critical impact on the respectively [6]. Crop loss from pests declines by overall functioning of freshwater ecosystems. 35% from 42% when pesticides are used. Thus, Indeed, microorganisms including cyanobacteria the use of pesticides is indispensable in contribute to most of the primary production in agricultural production system. Presently, about these systems [12]. The microorganisms are also one-third of the agricultural products are involved in nutrient cycling and decomposition produced by using pesticides [7]. [13]. Depending on the kind of ecosystem, both these communities must be considered when Agriculture plays a major role in the Indian attempting to evaluate the impact of herbicides economy as more than 70% of India’s population on microbial communities. is directly dependant on it and 27% of country’s gross domestic product stems from it. After many Cyanobacteria are morphologically, physio- years of struggle with food shortages, India has logically and developmentally most diverse group made good strides in food production from 51 of photosynthetic prokaryotes with low level of million tonnes in 1950-51 to 212 million tonnes in cellular differentiation that constitute one of the 2001-02. This is due to introduction of new major eubacteria phyla [14,15]. They also share agricultural strategies and application of modern characteristics of both gram-negative bacteria agricultural technologies like high yielding seeds, and photosynthetic eukaryotes. These organisms improved irrigation, balanced use of fertilizers have existed 2.5 billion years ago in the earth's and above all proper protection technologies geological history as evidenced by the using pesticides including herbicides [8]. The use microfossils, detected from early, middle and late of pesticides on large scale in agriculture has Precambrian strata. They seem to have played increased the food grain production in India the most important role in preparing the earth for which was reached 257 million tonnes during the evolution of higher life forms by contributing 2012-13 (agricoop.nic.in/documentreport.html). to significant increase in oxygen level [16]. These On the other hand, the risks of using pesticides microorganisms exhibit relatively simple including herbicides are serious as these are morphology and show maximum three cell types: highly toxic to humans and the environment. vegetative cells, heterocysts and akinetes. Pesticides and their toxic metabolic products flow Heterocyst differentiation occurs under nitrogen into the atmosphere, soils and rivers, resulting in starvation. Structurally and functionally, the the accumulation of toxic substances and thus heterocysts are the ideal sites for nitrogen threatening human health and the environment. fixation [17]. The use of pesticides on large scale in

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Classical taxonomists have classified pool which is maintained through biological cyanobacteria into five orders i.e, Chroococcales, nitrogen fixation by both hetero- and autotrophs Chamaesiphonales, Pleurocapsales, Nostocales in soil [28]. Non-heterocystous forms of and Stigonematales [18,19]. On the basis of cyanobacteria which predominantly occur in rice number of morphological, physiological and fields may also fix atmospheric nitrogen under genetic traits, Rippka et al. [20] have anaerobic conditions [29]. Plectonema [30], taxonomically revised this group and recognized Trichodesmium [31], Phormidium , Lyngbya , five sections. Section I comprises Chroococcales Chlorogloea , Gloeocapsa and Synechocystis [32] and Chamaesiphonales which reproduce by have been reported to fix atmospheric nitrogen. binary fission in one, two or three planes or by The characteristics of cyanobacteria to fix carbon budding. Section II includes members of as well as nitrogen fixation have made them an Pleurocapsales which reproduce by baeocytes important component of both aquatic as well as (endospores or exospores) which are formed by terrestrial ecosystems. These microorganisms multiple fission. Section III comprises non- are applied in rice fields as biofertilizer for better heterocystous filamentous oscillatorian crops yield [33]. members. Section IV and V correspond to Nostocales and Stigonematales, respectively, of Soil nitrogen is the main source of nitrogen for Desikachary [19]. Following Rippka et al. [20] crop growth and rice crop consumes 50% N from new classification has been proposed which soil [25]. Nitrogen-fixing cyanobacteria are recognized Chroococcales, Pleurocapsales, abundantly present in the rice field and are Oscillatoriales, Nostocales and Stigonematales important microbes for the maintenance of rice as the five orders of cyanobacteria [21]. Nucelic field fertility through carbon and nitrogen fixation acid sequencing of cyanobacteria is the [26]. The use of cyanobacterial biofertilizer is beginning to elucidate the evolutionary considered to be a good management of paddy relationships among cyanobacteria. Recently, fields since their use not only increases fertility of Lee [22] suggested three orders of cyanobacteria the soil but is also eco-friendly. Thorough i.e. Chroococcales (unicellular cyanobacteria), investigations on deleterious effects of pesticides Oscillatoriales (filamentous cyanobacteria) and including herbicides on cyanobacteria are Nostocales (filamentous cyanobacteria with required since utilization of cyanobacterial heterocysts). biofertilizer in paddy fields requires that strains be tolerant to a variety of routinely used Cyanobacteria are ubiquitous in their distribution agrochemicals. and grow in all sorts of aquatic and terrestrial environments. They survive in a wide variety of The effects of pesticides on algae have been extreme environmental conditions when they are extensively reviewed from time to time [34-38]. exposed to various types of natural stresses, The literature surveyed by the authors revealed such as nutrient limitation, pesticides, pollution, that impact of more than fifty five herbicides on drought, salinity, temperature, pH, light intensity cyanobacteria in one or another way has been and quality, etc. [23]. Illustrating their capacity to studied. As per the classification given by acclimate to extreme environments, a protein in Mallory-Smith and Retzinger [39], these the cyanobacterial thylakoid membranes was herbicides belong to 15 groups according to their identified as a sensitive protein to environmental mode of action on target plants (Table 1). The stresses such as drought, nutrition deficiency, parameters studied include growth, tolerance heat and chemical stress [24]. Many limit, photosynthetic pigments, carbon cyanobacterial species are capable of not only assimilation, defence mechanism, nitrogen surviving, but thriving in conditions previously assimilation and biodegradation. In this review thought to be inhabitable. current status of impact of herbicides on cyanobacteria is discussed. Cyanobacteria perform biologically two important key activities carbon fixation and nitrogen fixation 2. GROWTH INHIBITION AND TOXICITY and enrich the soil with humus and nitrogen content, improve water holding capacity, release Cyanobacteria are quite sensitive to herbicides, vitamins, plant stimulating hormones, extra because they share many of the physiological cellular polysaccharides and also solubilize features of higher plants. Differences have been phosphates [21,25-27]. It has been reported that observed between the tolerance to herbicides by more than half of the total nitrogen used by cyanobacteria and other organisms. The different paddy crop derives from the native soil nitrogen algal species exhibit different sensitivity to

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different herbicides depending on the species degradation products to nitrogen fixing tested, concentration and nature of herbicide cyanobacteria Anabaena inaequalis , Anabaena used [27,40-43]. For example, it has been cylindrica and Anabaena variabilis . Atrazine had observed that hexazinone was more toxic to EC 50 values ranging from 0.03 to 4 ppm towards green algae, diatoms and duckweed than to growth yield and 0.1 to 5 ppm towards growth cyanobacteria, whereas green algae were more rate. De-ethylated atrazine, a degradation tolerant to diquat than cyanobacteria and product, was toxic to all these cyanobacteria with diatoms [44]. The chronic exposure of EC 50 values ranging between1.0 and 8.5 ppm for hexazinone to cyanobacterial dominant both growth criteria. In contrast, de-isopropyl phytoplankton community of a forest lake at 1.0 atrazine was toxic towards A. variabilis and ppm resulted in reduction of biomass of all A. inaequalis with EC 50 ranging from 2.5 to 9.2 dominant phytoplankton groups including ppm for both criteria. Both diamino and hydroxyl- cyanobacteria [45]. Ahluwalia et al. [46] proved atrazine were less toxic to cultures tested that the incorporation of relatively higher doses yielding EC 50 less than 10 ppm [54]. De-Loranzo (>5 ppm) of diquat into the culture of Nostoc et al. [38] obtained EC 50 value of atrazine at 0.47 muscorum and Cylindrospermum sp. could be ppm for cyanobacterium Anabaena flosaquae . highly toxic, thereby reducing their chlorophyll a Another study revealed that atrazine at 88 ppb content and contributing to a progressive significantly reduced the growth of unicellular decrease in growth which culminates in complete cyanobacterium Synechocystis sp. [55]. Low lysis of the cells with the increasing level of the dose of atrazine (10 ppb) did not affect the herbicide. The same authors also demonstrated growth and cell volume of Arthrospira and that same concentration of paraquat Synechocystis while more than 100 ppb atrazine supplemented into Cylindrospermum sp. cultures inhibited growth [53]. also had an algicidal effect [47]. Non- heterocystous cyanobacterium Plectonema Wild type and multiple herbicide resistant (MHR) boryanum was comparatively more sensitive to stain of Anabaena variabilis tolerated pure and paraquat action than heterocystous Anabaena formulated form of atrazine up to 4 and 1 ppm, variabilis . The cells of Plectonema boryanum respectively, indicating formulated form of lysed completely at concentration higher than 20 atrazine was more toxic than pure form [56]. x 10 -7 M of paraquat while Anabaena variabilis Atrazine at 4.2 ppm caused 50% decrease in completely lost the ability to grow and died when growth of Microcystis novacekii demonstrating concentration of paraquat was above 20 x 10 -6 M the potential of the organism to tolerate high [48]. Paraquat up to 25 ppm reduced the growth concentrations of this herbicide in fresh water of Anabaena oryzae and Nostoc ellipsosporum environments [57]. Ten species of phytoplankton while growth was completely inhibited at 25 ppm belonging to green algae, diatoms and paraquat [49]. cyanobacteria were exposed to atrazine for 72 h at EC 50 concentrations and light of different Metsulfuron-methyl caused no inhibitory effect on intensities to compare their combined effect. The Microcystis aeruginosa , Pseudanabaena sp., data revealed that cyanobacteria were less Oscillatoria sp., Aphanizomenon flosaquae and tolerant to atrazine than green algae and diatoms Anabaena inaequalis at exposure range 0.003- [58]. 0.02 ppm [50]. Nyström et al. [51] while studying the effect of sulfonylurea herbicides on various Cyanobacteria Synechocystis PCC 6803 and groups of target aquatic microorganisms Anabaena variabilis ATCC 29413 showed high observed 50% reduction in growth of degree of tolerance to glyphosate and its various cyanobacteria Synechococcus leopoliensis , formulations. Significant differences in growth Anabaena flosaquae and Phormidium luridum by were observed at 10 mM glyphosate. The metasulfuron-methyl (1-130 nM) and decreasing order of toxicity of these formulations chlorosulfuron (0.045-1.45 µM). Sabater and were as RoundupR> isopropylamine salt > free Carrasco [52] using 96 h growth inhibition test acid [59]. Other cyanobacteria such as reported 50% reduction in growth of Anabaena sp., Arthrospira fusiformis , Pseaudanabaena galeata by 16 ppm Leptolyngbya boryana, Microcystis aeruginosa , metasulfuron. Nostoc punctiforme and Spirulina platensis tolerated glyphosate in the range of 1-10 mM Cyanobacteria are more resistant to atrazine [60]. Growth of wild-type and glyphosate- than green algae and diatoms [53]. Atrazine was sensitive (Gs) cells of Microcystis aeruginosa invariably most toxic compound than its was inhibited when they were cultured with 120

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ppm glyphosate but after further incubation for cyanobacterial strain SG2 of Nostoc tolerated several weeks, occasionally the growth of rare DCMU up to 15 ppm [73]. Synechococcus PCC cells resistant (Gr) to the herbicide was found 7042, Nostoc and Spirulina platensis exhibited [61]. The effect of glyphosate (37-150 ppm) on 80% inhibition in growth by 20 µM DCMU after the growth of Merismopedia glauca was dose 48 hr of treatment [69]. DCMU (0.5 ppm) was dependent with maximum growth rate and found to be more toxic as compared to atrazine generation time being 1.5 d -1 and 0.44 d -1, (0.6 ppm) to both parent and mutant strain of respectively [62]. The application of commercial Anabaena variabilis [56]. Leunert et al. [74] formulation of glyphosate roundup (6 and 12 compared the sensitivity of cyanobacteria and ppm) on fresh water microbial communities in green algae to DCMU using delayed artificial earthen mesocosms significantly fluorescence decay kinetics. It was found that increased the population of cyanobacteria by 4.5 cyanobacteria were more sensitive to DCMU folds in periphytic assemblages [63]. Vera et al. than green algae. [64] have shown that diatoms were more susceptible than cyanobacteria to glyphosate. In Monsulfuron at low concentration (0.03-0.3 nmol a study on ecological risks assessment of L-1) stimulated growth of Anabaena flosaquae , organophosphorus pesticides on bloom forming Anabaena azollae and Anabaena azotica while cyanobacterium Microcystis wesenbergii , it was higher concentrations (3-300 nmol L -1) were observed that isopropyl ammonium salt of -1 inhibitory. The most sensitive species was A. glyphosate (6.84 µM L ) showed medium growth flosaquae followed by A. azollae and A. azotica inhibitory effect [65]. [75]. Studies also revealed that the growth of A. flosaquae decreased significantly when exposed Nitrogen-fixing cyanobacteria were relatively to monosulfuron (0.008-800 ppm) under 2000, tolerant to 2,4 D compared to non-nitrogen fixing 3000 and 4000 lux light intensity. The cell ones under field conditions. Low concentration number and growth rate were reduced with most (1 mM) of 2,4 D and 2-methyl-4- sensitive light intensity being 4000 lux followed chlorophenoxyacetic acid (MCPA) did not affect by 3000 lux and 2000 lux [76]. The the growth of Anabaena UAM 202, UAM204 and supplementation of nitrogen further decreased Nostoc UAM205 while higher dose (10 mM) was the growth of Anabaena flosaquae in presence of inhibitory when growth was measured in terms of monosulfuron (0.016- 0.3 ppm) indicating dry weight biomass [66]. The growth of synergistic effect of herbicide and nitrogen [77]. Gloeocapsa was not affected significantly at 100-

150 ppm while 175-200 ppm of 2,4 D inhibited growth by 50-75% after 8 days of incubation [67]. Butachlor exhibited moderate to high toxicity to Tiwari et al. [68] compared the tolerance level of cyanobacteria. The growth of Anacystis nidulans , 28 non-heterocystous filamentous cyanobacteria Nostoc muscorum and Anabaena doliolum was isolated from rice fields using Chl a as growth completely inhibited at 2.5, 5 and 20 ppm, parameter. The range of tolerance of respectively, of butachlor [78]. Butachlor at 6-8 cyanobacteria to 2,4 D was 25 to 200 ppm with ppm was lethal to Nostoc linckia , Nostoc Lyngbya spiralis being the most tolerant (200 calcicola , Nostoc sp., and A. doliolum [79]. ppm). Tripathi et al. [69] revealed that 2,4 D Butachlor exhibited low toxicity to Nostoc sp., N. above 600 µM was inhibitory to Nostoc punctiforme , Nostoc calcicola , Anabaena muscorum and Synechococcus PCC 7942. In a variabilis , Gloeocapsa sp., Aphanocapsa sp. and nine day exposure experiment, 50 percent Aulosira fertilissima with EC 50 values between survival of 10 cyanobacterial isolates belonging 9.7 and 15 ppm [80 and 81]. In toxicity studies, to genera Chroococcus , Microcystis and Ge–Xian–Mi ( Nostoc ) had 96 h EC 50 value of 169 Synechocystis was observed in 6.84 µM L -1 of µM butachlor [82]. Aulosira fertilissima had 16 d 2,4 D [70]. EC 50 value equivalent to 65 µM [83]. He et al. [84] observed that butachlor above 120 ppm was Herbicide 3-(3,4-dichlorphenyl)-1,1 dimethyl urea lethal to Nostoc sp. Another study revealed that (DCMU) along with fluometuron, atrazine, Nostoc muscorum tolerated butachlor upto 20 ametryn inhibited the growth of Plectonema ppm [85]. Butachlor (25-36 µM) caused 50% boryanum [71]. DCMU (0.2 ppm) inhibited the decrease in growth of Anabaena 7120, growth of diazotroph Nostoc muscorum [72]. The Anabaena doliolum and Anabaena LC31 [86].

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Table 1. Summary list of toxicity tests parameters of herbicides to cyanobacteria

Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference A Inhibitors of acetyl CoA carboxylase (ACCase) 1 Clodinafop- prop-2-ynyl (R)-2-(4-(5-chloro-3- Aryloxyphenoxy- Nostoc muscorum Toxicity Singh et al. [102] propargyl fluoro-2-pyridyloxy) phenoxy) propionate propionate 2 Cyhalofop (R)-2-(4-(4-cyano-2-luorophenoxy) Aryloxyphenoxy- Nostoc muscorum Toxicity Singh et al. [102] butachlor phenoxy)propanoic acid propionate 3 Diclofop (RS)-2-(4-(2,4-dichlorophenoxy) Aryloxyphenoxy- Anabaena flos-aquae, Microcystis Toxicity Ma et.al. [40] phenoxy)propionic acid propionate flosaquae and Microcystis aeruginosa Microcystis aeruginosa Growth, protein, ultra cell Ye et al. [98] structure Microcystis aeruginosa Oxidative stress Ye et al. [152] 4 Fenoxaprop-p- ethyl (R)-2-(4-(6-chloro-1,3- Aryloxyphenoxy- Anabaena sp. Photosynthetic pigments Okmen et al. [120] ethyl benzoxazol-2-yloxy) phenoxy) propionate propionate B Inhibitor of acetolactate synthase (ALS) 5 Bensulfuron- methyl α-((4,6-dimethoxypyrimidin- Sulfonylurea Nostoc commune and Anabaena varibilis Growth, photosynthesis and Kim and Lee [87] methyl 2-ylcarbamoyl)sulfamoyl)-o-toluate nitrogen fixation Nostoc Photosynthetic pigments and Chen et al. [82] photosynthesis Anabaena , Nostoc and Nodularia Growth and nitrogen fixation Okmen et al. [88] Nostoc spongiforme Growth rate Spencer et al. [89] 6 Bispyribac 2 2,6-bis(4,6-dimethoxypyrimidin- Pyrimidinylthio- Anabaena sp., Cylindrospermum Toxicity Netherland et al. 2-yloxy) benzoic acid benzoate raciborsckii , Microcystis aeruginosa and [116] Pseudanabaena limnetica Anabaena sp., Gloeothece sp., and Growth and nitrogen fixation Okmen and Ugur. Synechocystis sp. [145] 7 Chlorosulfuron 1-(2-chlorophenylsulfonyl)-3-(4- Sulfonylurea 20 fresh water microalgae including Growth Inhibition Nyström et al. [51] methoxy-6-methyl-1,3,5-triazin-2- cyanobacteria yl)urea Psuedanabaena galeata , Chlorella Growth inhibition Sabater and sacharophila and Scenedesmus acutus Carrasco [52] 8 Metasulfuron 2-(4-methoxy-6-methyl-1,3,5- Sulfonylurea 20 fresh water microalgae including Growth Inhibition Nyström et al. [51] (Methyl triazin-2-ylcarbamoylsulfamoyl) cyanobacteria metsulfuron) benzoic acid

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference Nostoc muscorum Toxicity Singh et al. [102] 9 Monosulfuron 2-((4-methylpyrimidin-2-yl) Pyrimidinylsulfonyl- Anabaena flosaquae, Anabaena azolae Growth, acetolactate synthetase Shen et.al. [75] carbamoylsulfamoyl) benzoic acid urea and Anabaena azotica activity and aminoacids Anabaena flosaquae Growth and photosynthetic Shen et al. pigments [76 and 77] Anabaena flosaquae, Anabaena azolae Growth, photosynthesis and Shen et al. [133] and Anabaena azotica nitrogenase activity 10 Sulfosulfuron 1-(4,6-dimethoxypyrimidin-2-yl)-3- Pyrimidinylsulfonyl- Nostoc muscorum Toxicity Singh et al. [102] (2-ethylsulfonylimidazo(1,2-a) urea pyridin-3-ylsulfonyl) urea 11 Imazamox 2-[(RS)-4-isopropyl-4-methyl-5- Imidazolinone Anabaena sp., Cylindrospermum Toxicity Netherland et al. oxo-2-imidazolin-2-yl]-5- raciborsckii , Microcystis aeruginosa and [116] methoxymethyl nicotinic acid Pseudanabaena limnetica 12 Penaxsulam 3-(2,2-difluoroethoxy)-N-(5,8- Triazolopyrimidine Anabaena sp., Cylindrospermum Toxicity Netherland et al. dimethoxy[1,2,4]triazolo[1,5- sulphonamide raciborsckii , Microcystis aeruginosa and [116] c]pyrimidin-2-yl)-α,α,α- Pseudanabaena limnetica trifluorotoluene-2-sulfonamide C Inhibitors of microtubule assembly 13 Pendimethalin N-(1-ethylpropyl)-2,6-dinitro-3,4- Dinitroaniline Nostoc muscorum Toxicity Singh et al. [102] xylidine 14 Trifluralin α,α,α-trifluoro-2,6-dinitro-N,N- Dinitroaniline Plectonema boryanum and Cyanophage LPP-1 Growth Inhibition Mallison and dipropyl-p-toluidine Cannon) [71] Chroococcus sp. , Microcystis sp. and Toxicity Aslim and Ozturk Synechococcus sp. [70] Microcystis sp ., Synechocystis sp ., Chroococcus Growth Koksoy and Aslim sp . and Synechococcus sp. [114] D Synthetic auxin 15 2,4 D (2,4, dichlorophenoxy) acetic acid Phenoxy acids Anabaena Nitrogen fixation and ammonia Subramanian and excretion Shanmugasundaram [139] Anabaena , Nostoc and Nodularia Growth, photosynthesis and Leganés and nitrogen fixation Fernández-Valiente [66] Gloeocapsa Growth and nitrogen fixation Tözüm-Calgan and Sivaci-Güner [67] Paseudanabaena, Limnothrix , Dry weight and generation times Tiwari et al. [68]

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference Phormidium, Microcoleus , Plectonema, Lyngbya and Oscillatoria Synechococcus PCC7942 , Nostoc Growth and photosynthesis Tripathi et. al. [69] muscorum and Spirulina platensis Hypersaline cyanobacterial mat Biodegradation Nostoc muscorum, N. punctiforme, Tolerance limit, protein, Singh and Datta [91 N. calcicola, Anabaena variabilis, photosynthetic pigment, and 81] Gloeocapsa sp . and Aphanocapsa sp . photosynthesis and nitrogen fixation Singh et al. [90] Oscillatoria sp. dominated cyanobacterial Sorption Kumar et. al. [177] mat Chroococcus sp. , Microcystis sp. and Toxicity Aslim and Ozturk Synechococcus sp. [70] Anabaena fertilissima, Aulosira Photosynthetic pigments, Kumar et al. [113] fertilissima and Wesiellopsis prolifica carbohydrates, amino acids, protein, phenol, NR, GS and SDH activity Anabaena fertilissima Photosynthetic pigments, Kumar et al. [113] carbohydrates, amino acids, protein, phenol, NR, GS and SDH activity Nostoc muscorum Toxicity Singh et al. [102] Anabaena variabilis Growth, photosynthesis, Singh et al. [27] photosynthetic pigments, photosynthesis, respiration, nitrogen fixation and GS activity Microcystis sp ., Synechocystis sp ., Growth (Chlorophyll a) Koksoy and Aslim Chroococcus sp . and Synechococcus [114] Anabaena fertilissima, Aulosira Protein profiling Kumar et al. [172] fertilissima and Westiellopsis prolifica Anabaena fertilissima, Aulosira Biodegradation Kumar et al. [172] fertilissima and Westiellopsis prolific Anabaena torulosa Biosensor Shing et al. [178] Synechococcus aeruginosus Growth, photosynthesis and Lakshmi and Jyothi respiration [135]

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference 16 Methylchloro (4-chloro-3-methylphenoxy)acetic Phenoxy acids Anabaena , Nostoc and Nodularia Growth, photosynthesis and Leganés and phenoxy acetic acid nitrogenase activity Fernández-Valiente acids (MCPA) [66] Anabaena sp. and Microcystis viridis Photosynthesis, antioxidant Chen et al. [125] enzymes and DNA damage 17 Triclopyr 3,5,6-trichloro-2-pyridyloxyacetic Quinolone Anabaena flosaquae, Microcystis Toxicity Ma et al. [40] acid carboxylic acid flosaquae and Microcystis aeruginosa Synechocystis sp. strain PCC 6803 Biosensor Shao et al. [179] E Inhibitors of photosynthesis at PS -II site A 18 Ametryn N2-ethyl-N4-isopropyl-6-methylthio- Triazine Plectonema boryanum and Cyanophage Growth Inhibition Mallison and 1,3,5-triazine-2,4-diamine LPP-1 Cannon [71] Anabaena flosaquae, Microcystis Toxicity Ma et al. [40] flosaquae and Microcystis aeruginosa 19 Atrazine 6-chloro-N2-ethyl-N4-isopropyl- Triazine Plectonema boryanum and Cyanophage Growth Inhibition Mallison and 1,3,5-triazine-2,4-diamine LPP-1 Cannon [71] Anabaena flosaquae and Selenastrum Growth Abou-Waly et al. capricornutum [180] Anabaena inaequalis, Aphanizomenon 7-day carbon uptake Peterson et al. [50] flos-aquae, Pseudoanabaena sp., Oscillatoria sp., Microcystis aeruginosa , Cyclotella meneghiana , Nitzschia sp., Scenedesmus quadricauda , Selenastrum capricornutum and Vibrio fisheri Synechococuss sp. Biosensor Preuss and Hall [181] Synechocystis sp. strain PCC 6893 Resistance Narusaka et al. [127] Cyanobacterial strain SG2 psbA1 gene Sajjaphan et al. [73] Synechocystis sp. strain PCC 6803 Biosensor Shao et al. [179] Synechococcus sp., Arhrospira sp., Growth Inhibition Lockert et al. [53] Ankistrodesmus falcatus , Chlorella vulgaris , Staurastrum cristatum , Cyclotella meneghiniana , Nitzschia palea , Cryptomonas ovata and Euglena gracilis Synechococcus elongates Biosensor Kobilžek et al. [182] Synechococcus elongates and Herbicide removal González-Barreiro et Chlorella vulgaris al. [173]

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference Microbial assemblages Chlorophyl a, Carbon Downing et al. [183] assimilation and biomass Thermosyneochococcus elongatus Photosystem-II Zimmermann et al. [184] Synechococcus sp., Pseudokirchneriella Low molecular weight molecules, Weiner et. al. [55] subcapitata , Isochrysis galbana , lipids, polysaccharides and Dunaliella tertiolecta and proteins Pseudodactylum tricornutum Anabaena variabilis Photosynthetic pigments and Singh et al. [56] photosynthesis Anabaena variabilis Chlorophyll a, photosynthesis, Singh et al. [56] respiration and heterocyst frequency Nostoc muscorum Toxicity Singh et al. [102] Microcystis novacekii Bioaccumulation removal Campos et al. [57] Green algae, diatoms and cyanobacteria Toxicity and photosynthesis Deblois et al. [58] 20 Bromacil (RS)-5-bromo-3-sec-butyl-6- Uracil Anabaena inaequalis, Aphanizomenon 7-day carbon uptake Peterson et al. [50] methyluracil flosaquae, Pseudoanabaena sp., Oscillatoria sp., Microcystis aeruginosa , Cyclotella meneghiana , Nitzschia sp., Scenedesmus quadricauda , Selenastrum capricornutum and Vibrio fisheri Thermosyneochococcus elongates Photosystem-II Zimmermann et al. [184] 21 Cyanzine 2-(4-chloro-6-ethylamino-1,3,5- Triazine Anabaena inaequalis, Aphanizomenon 7-day carbon uptake Peterson et al. [50] triazin-2-ylamino)-2- flos-aquae, Pseudoanabaena sp., methylpropiononitrile Oscillatoria sp., Microcystis aeruginosa , Cyclotella meneghiana , Nitzschia sp., Scenedesmus quadricauda , Selenastrum capricornutum and Vibrio fisheri Anabaena flosaquae, Microcystis Toxicity Ma et al. [40] flosaquae and Microcystis aeruginosa 22 Hexazinone 3-cyclohexyl-6-dimethylamino-1- Triazine Anabaena flosaquae and Selenastrum Growth Abou-Waly et al. methyl-1,3,5-triazine-2,4(1H,3H)- caprocornutum [180] dione

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference Anabaena inaequalis, Aphanizomenon 7-day carbon uptake Peterson et al. [ 44 flos-aquae, Pseudoanabaena sp., and 50] Oscillatoria sp., Microcystis aeruginosa, Cyclotella meneghiana , Nitzschia sp., Scenedesmus quadricauda , Selenastrum capricornutum and Vibrio fisheri 23 Metribuzin 4-amino-6-tert -butyl-4,5-dihydro-3- Triazinone Anabaena inaequalis, Aphanizomenon 7-day carbon uptake Peterson et al. [50] methylthio-1,2,4-triazin-5-one flos-aquae, Pseudoanabaena sp., Oscillatoria sp., Microcystis aeruginosa , Cyclotella meneghiana , Nitzschia sp., Scenedesmus quadricauda , Selenastrum capricornutum and Vibrio fisheri Nostoc muscorum Toxicity Singh et al. [102] Anabaena sp. Photosynthetic pigments Okmen et al. [120] 24 Prometryne N2,N 4-diisopropyl-6-methylthio- Triazine Several species of Anabaena Growth and photosynthetic Shen et al. [185] 1,3,5-triazine-2,4-diamine pigments Anabaena flosaquae, Microcystis Toxicity Ma et al. [40] flosaquae and Microcystis aeruginosa 25 Simazine 6-chloro-N2,N 4-diethyl-1,3,5- Triazine Anabaena inaequalis, Aphanizomenon 7-day carbon uptake Peterson et al. [50] triazine-2,4-diamine flos-aquae, Pseudoanabaena sp., Oscillatoria sp., Microcystis aeruginosa , Cyclotella meneghiana , Nitzschia sp., Scenedesmus quadricauda , Selenastrum capricornutum and Vibrio fisheri Synechococcus elongatus Biosensor Kobilžek et al. [182 and 186]

Anabaena flosaquae, Microcystis Toxicity Ma et al. [40] flosaquae and Microcystis aeruginosa Synechocystis sp. strain PCC 6803 Biosensor Shao et al. [179] 26 Simetryn N2,N 4-diethyl-6-methylthio-1,3,5- Triazine Anabaena flos-aquae, Microcystis flos- Toxicity Ma et al. [40] triazine-2,4-diamine aquae and Microcystis aeruginosa 27 Terbutryn N2-tert-butyl-N4-ethyl-6-methylthio- Triazine Synechococcus elongates and Chlorella Herbicide removal González-Barreiro et 1,3,5-triazine-2,4-diamine vulgaris al. [173] Thermosyneochococcus elongatus Photosystem-II Zimmermann et al. [184]

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference Thermosynechococcus elongatus Photosystem-II Broser et al. [137] 28 Trietazin 6-chloro-N,N,N9-triethyl-1,3,5- Triazine Thermosyneochococcus elongatus Photosystem-II Zimmermann et al. (Tritazine) triazine-2,4-diamine [184] 29 Irgarol 2-methylthio-4-tert-butylamino-6- Triazine Synechococcus sp. PCC 7942 Growth, lipids and antioxidant Deng et al. [100] cyclopropylamino- s-triazine F Inhibitor of photosynthesis at PS -II site B 30 Bentazon 3-isopropyl-1H-2,1,3- Benzothiadiazole Synechococcus elongatus PCC 7942 Tolerance mechanism Bagchi et al. [92 and benzothiadiazin-4(3H)-one 2,2- 130] dioxide Nostoc muscorum Photosynthesis, photosynthetic Galhano et al. [94] pigments and respiration Anabaena cylindrica Photosynthetic pigments, protein, Galhano et.al. [93 carbohydrate, photosynthesis and 151] and respiration and antioxidant system Anabaena sp. Photosynthetic pigments Gulten and Onur [112] 31 Bromoxynil 3,5-dibromo-4-hydroxybenzonitrile Nitrile Synechococcus elongatus Biosensor Kobilžek et al. [182 and 186] Synechococcus elongatus PCC7942 Stress tolerance mechanism Bagchi et.al. [92] 32 Ioxynil 4-hydroxy-3,5-diiodobenzonitrile Nitrile Synechococcus elongatus Biosensor Kobilžek et al. [182 and 186] Thermosyneochococcus elongatus Photosystem-II Zimmermann et al. [184] G Inhibitor of photosynthesis at PS -II site A but different binding behaviour as E 33 Diuron (DCMU) 3-(3,4-dichlorophenyl)-1,1- Urea Nostoc muscorum Growth and heterocyst formation Vaishampayan [187] dimethylurea Plectonema boryanum and Cyanophage Growth Inhibition Mallison and LPP-1 Cannon [71] Anabaena, Nostoc and Oscillatoria Growth and Nitrogen fixation Zargar and Dar [80] Synechococuss sp. Biosensor Preuss and Hall [181] Synechocystis sp. strain PCC 6893 Herbicide Resistance Narusaka et al. [127] Synchchococcus PCC7942 , Growth and photosynthesis Tripathi et. al. [69]

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference Nostoc muscorum and Spirulina platensis Synechocystis sp.strain PCC 6803 Biosensor Shao et al. [179] Synechococcus elongatus Biosensor Kobilžek et al. [182 and 186] Thermosynechococcus elongates Photosystem-II Zimmermann et al. [184] Microcystis aeruginosa Synechocystis sp . Photosynthetic energy Deblios et al. [136] and Synechococcus sp. dissipation Anabaena variabilis Photosynthetic pigments and Singh et al. [56] photosynthesis Anabaena variabilis Chlorophyll a, photosynthesis, Singh et al. [56] respiration and heterocyst frequency Anabaena sp. and Microcystis viridis Photosynthesis, antioxidant Chen et al. [125] enzymes and DNA damage Synechococcus sp. PCC 7942 Growth, lipids and antioxidant Deng et al. [110] Microcystis aeruginosa , Aphanizemenon Fluorescence Kinetics Leunert et al. [74] flosaquae, Scenedesmus obliquus and Desmodesmus subspicus Cyanobacterial Mat Biodegradation Safi et al. [176] 34 Fluometuron 1,1-dimethyl-3-(α,α,α-trifluoro-m- Urea herbicide Plectonema boryanum and Cyanophage Growth Inhibition Mallison and tolyl)urea LPP-1 Cannon [71] Microcystis aeruginosa, Anabaena Toxicity and biodegradation Mansy and El- cylindrica, A. flosaquae and A. spiroides Bestawy [109] 35 Isoproturon 3-(4-isopropylphenyl)-1,1- Urea herbicide Anabaena inaequalis and Chlorella Biodegradation Mostafa and Helling dimethylurea kesslerei [170] Anabaena variabilis Nitrogen metabolism Aftab et al. [150] 36 Linuron 3-(3,4-dichlorophenyl)-1-methoxy- Urea herbicide Chroococcus sp. , Microcystis sp. and Toxicity Aslim and Ozturk 1-methylurea Synechococcus sp. Isolates [70] Microcystis sp ., Synechocystis sp ., Growth (Chlorophyll a) Koksoy and Aslim Chroococcus sp . and Synechococcus sp. [114] 37 Monuron 3-(4-chlorophenyl)-1,1- Urea herbicide Nostoc muscorum Growth and heterocyst Vaishampayan [187] dimethylurea 38 Propanil 3′,4 ′-dichloropropionanilide Amide Anabaena fertilissima Dry weight, protein and Chl a Inderjit and Kaushik [117]

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference 39 Tebuthiuron 1-(5-tert-butyl-1,3,4-thiadiazol-2- Substituted urea Anabaena inaequalis, Aphanizomenon 7-day carbon uptake Peterson et al. [50] yl)-1,3-dimethylurea herbicide flos-aquae, Pseudoanabaena sp., Oscillatoria sp., Microcystis aeruginosa , Cyclotella meneghiana , Nitzschia sp., Scenedesmus quadricauda , Selenastrum capricornutum and Vibrio fisheri H Inhibitors of lipid synthesis 40 Molinate S-ethyl perhydroazepine-1- Thiocarbamate Anabaena , Nostoc and Nodularia Growth and Nitrogen fixation Okmen et al. [62] thiocarboxylate Nostoc muscorum Photosynthesis, photosynthetic Galhano et al. [94] pigments and respiration Anabaena cylindrica Photosynthetic pigments, protein, Galhano et.al. [93] carbohydrate, photosynthesis and respiration Nostoc muscorum Antioxidant system and fatty acid Galhano et. al. [124] profile 41 Thiobencarb S-4-chlorobenzyl Thiocarbamate Anabaena, Nostoc and Oscillatoria Growth and nitrogen fixation Zargar and Dar [80] (Benthiocarb) diethyl(thiocarbamate) Nostoc muscorum Growth, pigments and nitrogen Bhunia et al. [106] fixation Nostoc spaeroides Growth, photosynthetic pigment Xia, J [107] and photosynthesis Nostoc muscorum Protein profiling, nitrogenase, Dowidar et al. [144] glutamine synthetase, oxaloacetic acid transaminase and glutamic pyruvic transaminase activities Anabaena variabilis Growth and photosynthesis Battah et al. [188] I Inhibitor of 5 -enolypyruvyl -shik imate -3-phosphate synthase (EPSP) 42 Glyphosate N-(phosphonomethyl) glycine Organophosphorus Synechocystis PCC6803 and Anabaena Tolerance limit and Powell et al. [59] variabilis ATCC 29413 photosynthesis Anabaena inaequalis, Aphanizomenon 7-day carbon uptake Peterson et al. [50] flosaquae, Pseudoanabaena sp., Oscillatoria sp., Microcystis aeruginosa , Cyclotella meneghiana , Nitzschia sp., Scenedesmus quadricauda ,

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference Selenastrum capricornutum and Vibrio fisheri Wild and mutant strains of Anabaena Chlorophyll a fluorescence Shikha and Singh doliolum [129] Spirulina sp. Glyphosate degradation Lipok et. al. [167] Microcystis aeruginosa Herbicide tolerance and López-Rodas et al. resistance [61] Anabaena sp., Arthrospira fusiformis, Herbicide Tolerance and Forlani et al. [60] Leptolyngbya boryanum, Microcystis mineralization aeruginosa, Nostoc punctiforme and spirulina platensis Anabaena fertilissima Dry weight, protein and Chl a Inderjit and Kaushik [117] Anabaena sp. and Microcystis viridis Photosynthesis, antioxidant Chen et al. [125] enzymes and DNA damage Scenedesmus quadricauda and Growth, cell number, chlorophyll Issa et al. [62] Merismopedia glauca a, proteins and carbohydrates Nostoc muscorum Toxicity Singh et al. [102] Microcystis wesenbergii Chlorophyll a fluorescence Sun et al. [65] J Inhibitor of phytoene desaturase (PDS) 43 Fluridone 1-methyl-3-phenyl-5-(α,α,α- Not Known Synechococcus sp. PCC 7942 Phytoene desaturase Chamovitz et al. trifluoro-m-tolyl)-4-pyridone [189] 44 Norflurazon 4-chloro-5-methylamino-2-(α,α,α- Pyridazinone Synechococcus PCC7942 Carotenoid biosynthesis Chamovitz et al. trifluoro-m-tolyl)pyridazin-3(2H)- [189] one K Inhibitor synthesis of very long chain fatty acids 45 Acetochlor 2-chloro-N-ethoxymethyl-6′- Chloroacetamide Cyanobacterial mat Biodegradation El-Nahhal et al. ethylacet-o-toluidide [174] 46 Alachlor 2-chloro-2′,6 ′-diethyl-N- Chloroacetamide Nostoc muscorum, N. punctiforme, N. Tolerance limit, protein, Singh and Datta [91 methoxymethylacetanilide calcicola, Anabaena variabilis, photosynthetic pigment, and 81] Gloeocapsa sp. and Aphanocapsa sp . photosynthesis and nitrogen Singh et al. [90] fixation Aphanizomenon flos-aquae, Ecotoxicological impact Abrantes et al. [190] Pseudokirchnerella subcapitato, Daphnia magna, and D. longispina Anabaena variabilis Growth, photosynthesis, Singh et al. [27]

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference photosynthetic pigments, respiration, nitrogen fixation and GS activity 47 Anilofos S-4-chloro-N- Organophosphorus Nostoc muscorum, N. punctiforme, N. Tolerance limit, protein, Singh and Datta [91 isopropylcarbaniloylmethyl O,O- calcicola, Anabaena variabilis, photosynthetic pigment, and 81] dimethyl phosphorodithioate Gloeocapsa sp . and Aphanocapsa sp . photosynthesis and nitrogen Singh et al. [90] fixation Nostoc muscorum Toxicity Singh et al. [42] Anabaena variabilis Growth, photosynthesis, Singh et al. [27] photosynthetic pigments, respiration, nitrogen fixation and GS activity Anabaena torulosa Tolerance, pigments, Singh et al. [42] photosynthesis, nitrogen assimilation and antioxidants Synechocystis sp. strain PUPCCC 64 Tolerance and mineralization Singh et al. [43] 48 Butachlor N-butoxymethyl-2-chloro-2′,6 ′- Chloroacetamide Anabaena, Nostoc, Oscillatoria and Tolerance, photosynthetic Selvakumar et al. diethylacetanilide Westiellopsis pigments and ammonia excretion [119] Nostoc muscorum, N. punctiforme, N. Tolerance limit, protein, Singh and Datta [91 calcicola, Anabaena variabilis, photosynthetic pigment, and 81] Gloeocapsa sp . and Aphanocapsa sp . photosynthesis and nitrogen Singh et al. [90] fixation Nostoc Photosynthetic pigments and Chen et al. [82] photosynthesis Aulosira fertilissima Photosynthetic pigments, Kumari et. al. [83] photosynthesis and plasma membrane integrity Nostoc muscorum Protein profiling, nitrogenase, Dowidar et al. [144] glutamine synthetase, oxaloacetic acid transaminase and glutamic pyruvic transaminase activities Nostoc muscorum Toxicity Singh et al. [91] Anabaena variabilis Growth, photosynthesis, Singh et al. [27] photosynthetic pigments, respiration, nitrogen fixation and

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference GS activity Plectonema boryanum Pigments and antioxidant Kumar and Vikash [118]. Nostoc sp. Photosynthetic pigments and He et al. [84] fluorescence kinetics Anabaena 7120, Anabaena doliolum and Proteomics Agrawal et al. [86] Anabaena LC31 Anabaena variabilis Nitrogen metabolism Aftab et al. [150] Nostoc muscorum Toxicity and Biodegradation Annes et al. [85] 49 Menfenacet 2-benzothiazol-2-yloxy-N- Oxyacetamide Soil microbial communities Phospholipid fatty acid profiles Murata et al. [191] methylacetanilide 50 Metachlor 2-chloro-N-(2-ethyl-6- Chloroacetamide Plectonema boryanum and Cyanophage Growth Inhibition Mallison and methylphenyl)-N-(2-methoxy-1- LPP-1 Cannon [71] methylethyl)acetamide 51 Pretilachlor 2-chloro-2′,6 ′-diethyl-N-(2- Chloroacetamide Soil microbial communities Phospholipid fatty acid profiles Murata et al. [191] propoxyethyl)acetanilide Anabaena fertilissima Dry weight, protein and Chl a Inderjit and Kaushik [117] Nostoc muscorum Toxicity Singh et al. [102] L Photosystem -I electron diverters 52 Diquat 6,7-dihydrodipyrido(1,2-a:2 ′,1 ′-c) Bipyridylium Anabaena inaequalis, Aphanizomenon 7-day carbon uptake and growth Peterson et al. [44] pyrazine-5,8-diium flos-aquae, Pseudoanabaena sp., inhibition Oscillatoria sp., Microcystis aeruginosa , Cyclotella meneghiana , Nitzschia sp., Scenedesmus quadricauda , Selenastrum capricornutum and Duckweed 53 Paraquat 1,1 ′-dimethyl-4,4 ′-bipyridinium Bipyridylium Anabaena variabilis and Plectonema Growth inhibition, alkaline Dragolova et al. [48] dichloride dichloride boryanum phosphatase, proline, lipids, Synechocystis sp. strain PCC 6803 Biosensor Shao et al. [180] Oscillatoria sp. dominated cyanobacterial Sorption Kumar et. al. [177] mat Cylindrospermum raciborskii Toxicity Leboulanger et al. [192] Anabaena oryzae and Nostoc Growth and herterocyst formation Pandey et al. [49] ellipsosporum

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Sr. no . Herbicide Chemical name Chemical family Organism(s) Parameter(s) studied Reference Nostoc muscorum Toxicity Singh et al. [102] M Inhibitors of 4 -hydroxyphenyl -pyruvate d ioxygenase (4 -HPPD) 54 Mesotrione 2-(4-mesyl-2-nitrobenzoyl) Triketone Cyanobacterial community Dose-response effects Crouzet et al. [175] cyclohexane-1,3-dione N Inhibitors of protoporphyrinogen oxidase (Protax) 55 Carfentrazone- ethyl (RS)-2-chloro-3-{2-chloro-5- Triazolons Nostoc spongiforme Growth rate Spencer et al. [89] ethyl (Shark) [4-(difluoromethyl)-4,5-dihydro-3- methyl-5-oxo-1H-1,2,4-triazol-1- yl]-4-fluorophenyl}propionate 56 Oxyfluorfen 2-chloro-α,α,α-trifluoro-p-tolyl 3- Diphenylether Oscillatoria isolates Tolerance Ravinderan et al. ethoxy-4-nitrophenyl ether [96] Nostoc muscorum and Phormidium Growth, photosynthesis, nutrient Sheeba et al. [97] foveolarum uptake, nitrate reductase and alkaline phosphatase 57 Oxadiazon 5-tert-butyl-3-(2,4-dichloro-5- Oxadiazolone Microcystis aeruginosa Synechocystis Photosynthetic energy Deblios et al. [136] isopropoxyphenyl)-1,3,4- and Synechococcus dissipation oxadiazol-2(3H)-one O Membrane disrup tor 58 Dinoseb 2-tert-butyl-4,6-dinitrophenol Dinitrophenol Synechocystis PCC 6803 Resistance Elanskaya et al. (Dinoterb) herbicide [165] Synechococcus elongatus Biosensor Kobilžek et al. [182 and 186]

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Bensulfuron-methyl at low dose (0.1-1.0 ppm) caused reduction in dry masses by 41% and stimulated the growth of Anabaena variabillis KJ- 50% in N. muscorum and only by 6% and 15% in 013 and Nostoc commune KJ-018 while high P. foveolarum , respectively [97]. Ma et al. [40] in doses (8 and 10 ppm) caused more than 50% 96 h acute toxicity test demonstrated 50% growth growth inhibition after 24 h of incubation [87]. reduction in Anabaena flosaquae , Microcystis Anabaena sp. and Nostoc sp. tolerated butachlor flosaquae and Microcystis sp. by cynazine (0.15, up to 30 ppm whereas Nodularia sp. was able to 9.6 and 27.7 ppm), triclopyr (109, 46 and 33 tolerate this herbicide up to 50 ppm [88]. Londax, ppm), simetryn (0.006, 0.0002 and 0.002 ppm) a commercial form of bensulfuron-methyl at and by ametryn at 0.03, 0.009 and 0.02 ppm, 0.028 ppm did not affect the growth of respectively. cyanobacterium Nostoc spongiforme when applied in combination with carfentrazone ethyl In a 96 h acute toxicity test, Diclofop (0.03-0.11 herbicide [89]. Nostoc muscorum , Nostoc ppm) caused 50% reduction in growth of calcicola , Aphanocapsa sp. and Gloeocapsa sp. Anabaena flosaquae , Microcystis flosaquae and tolerated anilofos (arozin) up to 5 ppm, Nostoc Microcystis aeruginosa [40]. Exposure to 10 and punctiforme up to 10 ppm and Anabaena 20 ppm diclofop caused reduction in dry biomass variabilis up to 20 ppm [90 and 91]. Other reports by 40-50% in Nostoc muscorum and by 6-15% in showed that Oscillatoria simplicissima grew in Phormidium foveolarum [97]. To explore the Bensulfuron-methyl up to 40 ppm [41], enantioselective effect of chiral herbicide Synechocystis sp. PUPCCC 64 up to 30 ppm dichlofop-methyl and its major metabolite [43] and Anabaena torulosa up to 10 ppm of dichlofop acid (DA), the physiological anilofos [42]. Trifluralin (169-467 ppm) and linurin characteristics of Microcystis aeruginosa were (0.038-0.441 ppm) caused 50% growth reduction investigated using biomass as growth parameter. in 10 cyanobacterial isolates belonging to Stimulation of biomass by R-DA and S-DA was Chroococcus (3), Microcystis (3) and apparent up to 5 ppm concentration. Ultra Synechocystis (4) [70]. Wild and resistant strains structural changes in gas vacuole, thylakoids, of cyanobacterium Synechococcus elongatus glycogen, cyanophycean granules, polyhedral PCC 7942 exhibited 50% survival when bodies indicated different toxicity modes of these incubated in 30 and 150 µM bromoxylonil, chemicals [98]. respectively [92]. Lürling and Roessink [99] showed that Effects of molinate and bentazon were studied Scenedesmus (green alga) out competed on Anabaena cylindrica during a short-term Microcystis (cyanobacterium) in the absence of experiment of 72 h [93]. The results revealed that herbicide metribuzin whereas the reverse was both herbicides had a pleiotropic effect on the true in the presence of this herbicide. Herbicide cyanobacterium at the range of 0.75-2 mM irgarol (0.019 µM) was five times more toxic than concentrations. Cyanobacterial growth was more diuron (0.097 µM) to Synechococcus sp. PCC adversely affected by molinate than bentazon. 7942 as indicated by their EC 50 values in a 96 h More than 50% growth inhibition was observed growth experiments [100]. A 96 h EC 50 value of after 48 h treatment with 1.5-2 mM of molinate in 7.71 ppm of irgarol for a marine cyanobacterium A. cylindrica . Bentazon and molinate were also Chroococcus minor was observed [101]. toxic to Nostoc muscorum with 72 h EC 50 values Herbicide shark, a commercial form of being 22.7 and 1.2 mM, respectively [94]. In carfentrazone ethyl, at 0.147 ppm did not affect another study Sabater and Carrasco [95] the growth rate of Nostoc spongieforme [89]. The obtained 96 h EC 50 value of 13 ppm of molinate toxicity of thirteen herbicides to Nostoc for this cyanobacterium. Cyanobacteria muscorum has been studied using 94 h growth Paeudanabaena galeata , Anabaena sp., Nostoc inhibition test by taking absorbance and and Nodularia sp. were able to tolerate molinate chlorophyll a as growth parameters . The order of up to 100 ppm [88]. tolerance level of these herbicides was: 2,4 D >

Oxyfluorfen (20 ppm) inhibited growth (50-67%) methyl metusulfuron > glyphosate > butachlor > when measured in terms of protein content in atrazine > sulfosulfuron > metribuzin > four isolates of Oscillatoria [96]. Oxyfluorfen pendimethalin > clodinafop propargyl >anilofos > showed differential inhibitory effects on Nostoc cyhalofop butachlor > pretilachlor > paraquat muscorum and Phormidium foveolarum as dichloride. Further these results indicated that indicated by decreased biomass production, toxic effects of herbicides did not correlate with photosynthetic pigments and photosynthetic the nature, mode of action and class type of activities. Exposure to 10 and 20 ppm oxyfluorfen herbicide [102].

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3. PHOTOSYNTHETIC PIGMENTS Yan et al. [110] observed increased Chl a content (17-62%) in Anabaena sphaerica after 6 3.1 Chlorophyll a (Chl a) days treatment with 5-50 ppm molinate under 300-3000 lux light intensity. While Kobbia et al. Chlorophyll biosynthesis is catalysed by several [111] verified reduction in Chl a content in enzymes in multiple steps [103,104]. The effect Anabaena variabilis at all the tested of different herbicides on Chl a synthesis in concentrations (0.2-0.8 ppm) of molinate. The cyanobacteria varied due to differential nature effects of commercial formulations of two and mode of action. Carotenoid inhibiting selective herbicides molinate (Ordham) and herbicide fluridone inhibited Chl a pigment in bentazon (Basagran) recommended for Oscillatoria agardhii in a dose dependent manner integrated weed management (IWM) on rice [105]. Thiobencarb (2-6 ppm) reduced the Chl a were laboratory assessed on Anabaena content in Nostoc muscorum by 56-97% and it cylindrica during a short-term experiment of 72 h was suggested that the low pigment may be as a [93]. The results revealed that both herbicides result of photo oxidation arising from inability of had a pleiotropic effect on the cyanobacterium at Chl a to dissipate its absorbed excitation energy the range of concentrations tested (0.75-2 mM). when electron transport was inhibited by The same authors also reported that molinate (2 herbicide [106]. While other studies mM) inhibited Chl a (20%) in Nostoc muscorum demonstrated that thiobencarb (2-10 ppm) did after 72 h treatment as a result of degradation of not affect significantly the Chl a pigment in lipid complex associated with pigments in Nostoc sphaeroides [107]. thylakoids [94]. Xia [107] demonstrated that 10 ppm of thiobencarb had insignificant effect on Atrazine (10-100 ppb) inhibited Chl a pigment of Chl a synthesis of Nostoc sphaeroides . The Oscillatoria limnetica, Arthrospira sp. and constant level of Chl a content of Nostoc Synechococcus sp. [53,108]. Sub-lethal muscorum culture exposed to bentazon (0.75-2.0 concentration of pure (6 ppm) and formulated mM) demonstrated that herbicide had no effect form (2 ppm) of atrazine and DCMU (0.4 and 0.5 on this photo pigment [93]. While comparing the ppm) inhibited Chl a content by 74-80% in wild Chl a content of two strains of Anabaena isolated type and 68-77% in multiple herbicide resistant from Turkey rice fields, Gulten and Onur [112] strain of cyanobacterium Anabaena variabilis reported that bentazon (100 ppm) inhibited Chl a [56]. Fluometuron (140-1400 ppm) caused content severely in Anabaena sp. GO10 than reduction in Chl a pigment in time and dose Anabaena sp. GO4. dependent manner in six cyanobacterial strains belonging to Microcystis aeruginosa , Anabaena Low concentration (1 mM) of 2,4 D and MCPA cylindrica , Anabaena flosaquae and Anabaena did not affect the Chl a synthesis in Anabaena spiroides , with complete inhibition after 2-3 days UAM 202 while higher dose (10 mM) of both of exposure. The inhibition of Chl a content was herbicides completely degraded Chl a after 48 h species specific. The order of affected species at treatment [66]. 2,4 D (5-20 ppm) inhibited Chl a highest tested dose was: Anabaena spiroides > synthesis by 30-52% in immobilized Nostoc Microcystis aeruginosa (11) > Microcystis muscorum , Nostoc punctiforme , Nostoc aeruginosa (15) > Microcystis aeruginosa (1) calcicola , Anabaena variabilis , Aphanocapsa sp., >Anabaena cylindrica >Anabaena flosaquae and Gloeocapsa sp. [91]. The decrease in Chl a [109]. content by 60-77% was reported in Anabaena fertilissima , Aulosira fertilissima and Monosulfuron (0.008-800 ppm) exerted its effect Westiellopsis prolifica after treatment with 60-120 on Chl a of Anabaena flosaquae in a dose ppm of 2,4 D was reported [113]. Koksy and dependent manner under 2000-4000 lux light Aslim [114] reported inhibition of Chl a by 2,4 D intensity. Chl a synthesis was more sensitive (123-748 ppm), trifluralin (139-882 ppm) and under 2000 lux light intensity than other light linurin (0.02-0.77 ppm) in several strain of intensities [76]. The herbicide also exhibited a cyanobacteria. dose dependent reduction in Chl a of Anabaena flosaquae in presence of different nitrogen Anilofos (10 ppm) enhanced Chl a synthesis in contents. The content of Chl a was reduced by Anabaena variabilis ARM310 [115]. The 47-73% in presence of 0.05 ppm nitrogen and commercial formulation of anilofos, arozin at 85-97% in 0.8 ppm nitrogen after treatment wih IGC 50 concentration severely affected Chl a in monosulfuron (0.016-0.30 ppm) for 144 h Nostoc muscorum, Gloeocapsa sp. and indicating synergistic effect [77]. Aphanocapsa sp. as compared to Anabaena

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variabilis , Nostoc punctiforme and Nostoc completely inhibited at 400 ppm fenoxaprop calcicola [90]. Immobilized forms of Nostoc [120]. muscorum , Nostoc punctiforme , Nostoc calcicola , Anabaena variabilis , Aphanocapsa sp., 3.2 Phycobiliproteins and Gloeocapsa sp. exhibited a reduction in chl a (44-67%) when treated with at IGC 50 dose of Phycobiliproteins (PBS) are major light anilofos [91]. Treatment with anilofos (10-20 harvesting pigments and reserve of nitrogen in ppm) for 6 day caused a reduction in Chl a cyanobacteria [121] and it has been shown that content by 18-47% in Oscillatoria simplicissima these pigments are also affected by herbicides. [41] while a decrease of 21-60% in chl a content The differential response of PBS to herbicides of Synechocystis sp. PUPCCC 64 by 5-20 ppm may be due to their exterior distribution on [43] and by 21-43% in Anabaena torulosa with thylakoid membrane of cyanobacteria and thus 1.25- 5.0 ppm anilofos [42] was reported. direct contact with herbicides. Carotenoid inhibiting herbicide fluridone did not exhibit Penoxasulam, an acetolactate synthesis inhibitory effect on phycocyanin in filamentous inhibiting herbicide, at 100 ppb reduced Chl a by non-heterocystous cyanobacterium Oscillatoria 90% in Anabaena sp. and 58% in up to 100 ppb [105]. The phycocyanin (PC), Pseudanabaena limnetica but did not affect phycoerythrin (PE) and allophycocyanin (APC) noxious cyanobacterium Microcystis aeruginosa content in Nostoc sphaeroides significantly [116]. Propanil (0.187-1.5 ppm) and glyphosate declined (60%) on exposure to 10 ppm (10-80 ppm) also suppressed Chl a production thiobencarb [107]. Monosulfuron (0.008-0.08 by 5-38% in Anabaena fertilissima , while ppm) exerted stimulatory effect on PBS pretilachlor (5-40 ppm) exhibited 10-45% (increased by 11-46%) of Anabaena flosaquae reduction in Chl a content [117]. Alachlor (15-20 but exhibited inhibitory effect (decreased by 33- ppm) and butachlor (10-20 ppm) caused a 98%) at higher concentrations (0.8-800 ppm) of decrease (27-47%) in Chl a content in herbicide when exposed to varied light intensities immobilized cyanobacteria Nostoc muscorum , (2000, 3000 and 4000 lux). Further, these Nostoc punctiforme , Nostoc calcicola , Anabaena billiprotien were more sensitive to herbicide at variabilis , Aphanocapsa sp., and Gloeocapsa sp. 2000 lux light intensity than other light intensities [91]. When the wild type and MHR strain of [76]. Treatment of Aulosira fertilissima with Anabaena variabilis were exposed to 10-100 butachlor (65 µM) for 15 days showed severe ppm each of alachlor, arozin, butachlor and 2,4 inhibition in synthesis of APC (75%) followed by D, the wild type exhibited 42-58% reduction in APC (50%) and PE (49%) [83]. The effect of Chl a content while MHR strain showed 65-72% monosulfuron on PBS of Anabaena flosaquae decrease [27]. Chl a content in Plectonema grown in presence of nitrogen source displayed boryanum sharply declined (40%) in five day dose dependent affect. Exposure to treatment with 40 ppm butachlor [118]. The dose monosulfuron (0.016-0.30 ppm) in presence of dependent reduction in Chl a of Merismopedia three nitrogen concentrations (0.05-0.8 ppm), the glauca by glyphosate (37-150 ppm) was content of biliprotein decreased by 10-37% observed by Issa et al. [62]. Butachlor compared to control cultures [77]. considerably declined Chl a in Aphanocapsa , Anabaena fertilissima, Anabaena variabilis, The sub-lethal doses of pure and formulated Gleocapsa , Nostoc sp., Nostoc punctiforme , forms of atrazine and DCMU reduced PC (73- Nostoc calcicola , and N. muscorum [82-84, 91]. 79%) and PE (66-71%) content on day 8 in both Other studies have revealed that butachlor at 3- wild type and MHR strain of Anabaena variabilis 12 ppm concentrations affected Chl a production [56]. Phycobillins were adversely affected by in strains of Anabaena , Nostoc and Oscillatoria 2,4 D than Chl a and carotenoids in sp. but did not effect Chl a of Westiellopsis Anabaena fertilissima , Aulosira fertilissima and strains [119]. Fenoxaprop-p-ethyl (6.25 ppm) Westiellopsis prolifica [113]. stimulated Chl a contents in Anabaena sp. GO10. Further, increasing herbicide Commercial formulation of anilofos, arozin (5-20 concentrations suppressed Chl a synthesis in a ppm) inhibited PC and PE content in range of 53- dose dependent manner. Chl a contents was 71% and 57-83%, respectively, in immobilized completely suppressed by 100 ppm of Nostoc muscorum , Nostoc punctiforme , Nostoc fenoxaprop. Another herbicide cyhalofop-butyl at calcicola , Anabaena variabilis , Aphanocapsa sp., 25 ppm partly stimulated this pigment in this and Gloeocapsa sp. [91]. Anilofos (10-20 ppm) cyanobacterium but pigment synthesis was decreased PC content by 14-36%, APC by

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12-32% and PE by 15-37% on day 6 in damage by stressors such as herbicides [123]. Oscillatoria simplicissima [41]. In diazotrophic Carotenoids in non-nitrogen fixer Oscillatoria cyanobacterium Anabaena torulosa, anilofos agadhii were severely inhibited by herbicide (1.25-5.0 ppm) decreased PC content by 20- fluridone up to 100 ppb [105]. The carotenoid 50%, APC by 17-46% and PE by 14-48% [42]. synthesis in this organism, exposed to 4000 lux Treatment of Synechocystis sp. PUPCCC 64 light, was more sensitive to herbicide compared with 5-20 ppm anilofos for six days caused a loss to other light intensities. Monosulfuron (0.008- of PC APC and PE by 55-99%, 25-85% and 47- 0.08 ppm) reduced carotenoid production in 80%, respectively [43]. Anabaena flosaquae by 28-90% when colonies were exposed to 3000 and 4000 lux light Alachlor (15-20 ppm) decreased PC and PE intensity after 144 h treatment [76]. Treatment for content in the range of 29-75%, in Ca-alginate 8 days with sub-lethal doses of pure and immobilized Nostoc muscorum , Nostoc formulated forms of atrazine and DCMU punctiforme , Nostoc calcicola , Anabaena exhibited reduction in carotenoids synthesis (40- variabilis , Aphanocapsa sp., and Gloeocapsa sp. 47%) in both wild type and MHR strain of whereas butachlor (10-20 ppm) caused 59-81% Anabaena variabilis [56]. The production of reduction. 2,4 D (5-20 ppm), on the other hand carotenoid by Anabaena flosaquae was inhibited reduced PC and PE content in the range of 30- synergistically with increase in both nitrogen and 88% in these cyanobacteria [91]. Total PBS monsulfuron concentrations. The content of content was more adversely affected by carotenoids in cells of A. flosaquae was reduced commercial formulations of molinate than by 31-100% when exposed to 0.05- 0.8 ppm bentazon in Anabaena cylindrica [93]. Gulten and nitrogen and 0.016-0.3 ppm monosulfuron [77]. Onur [112] compared the phycobilins of two Carotenoids of Anabaena cylindrica were more species of Anabaena isolated from Turkey paddy adversely affected by commercial formulations of fields and found that inhibition of these pigments molinate (ordham) than bentazon (basagran) at was more pronounced in Anabaena sp. GO10 0.75-2.0 mM concentration [93]. Molinate (0.75- than GO4 when treated with 100 ppm bentazon. 2.0 mM) after 72 h of treatment drastically inhibited carotenoids (96-98%) in Nostoc Butachlor (3-12 ppm) significantly reduced muscorum [124]. phycobiliproteins (PBPS) in Anabaena , Nostoc and Oscillatoria strains but did not affect PBPS of The carotenoid synthesis in diazotrophic Westiellopsis [119]. A reduction in PBPS content Anabaena fertilissima , Aulosira fertilissima and in Anabaena doliolum by machete was reported Westiellopsis prolifica was affected in a time and by Kashyap and Pandey [122]. Chen et al. [82] dose dependent manner by 2,4 D. At the end of showed that PC and APC content significantly experiments after 16 days, carotenoids in increased when Ge–Xian–Mi ( Nostoc ) colonies Anabaena fertilissima were depleted by 80% at were treated with 10 µM butachlor, but contents 60 ppm of 2,4 D. However, carotenoid content declined with further increase in butachlor was decreased by 64% at 120 ppm in W. concentration. Kumari et al. [83] observed a prolifica followed by A. fertilissima where dose-dependent rise in PE, APC and PC of A. reduction was 72% relative to control [113]. fertilissima cells, while He et al. [84] reported the Treatment with anilofos (10-20 ppm) for 6 days decline in PBPS content in Nostoc sp. in caused more than 53% inhibition in synthesis of presence of butachlor. Fenoxaprop-p-ethyl (6.25 carotenoids in non-heterocystous Oscillatoria ppm) stimulated PBPS in Anabaena sp. GO10. simplicissima [41], 26-45% reduction by 1.25-5.0 Further, increase in herbicide concentrations ppm in Anabaena torulosa [42] and 32-90% suppressed PBPS synthesis in a dose reduction by 5-20 ppm of herbicide in dependent manner. The PBPS was completely Synechocystis sp. PUPCCC 64 [43]. suppressed by 100 ppm of fenoxaprop. Other herbicide cyhalofop-butyl at 25 ppm partly The addition of 10 µM each of glyphosate and stimulated PBPS in this cyanobacterium but MCPA significantly decreased the carotenoid completely repressed at 400 ppm concentration content in UV irradiated cells of Microcystis [120]. novaci and Anabaena sp. while the addition of DCMU (10 µM) did not affect carotenoids in 3.3 Carotenoids these cyanobacteria [125]. Compared to untreated control cultures, sub-lethal doses of Carotenoids are the essential pigments which pure and formulated forms of atrazine (2 and 6 protect the photosynthetic system from oxidative ppm) and DCMU (0.4 and 0.5 ppm) reduced

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carotenoids by 40-47% on day 8 in wild type and algae, cyanobacteria and diatoms resulted in MHR strain of Anabaena variabilis [56]. Five significant inhibition of photosynthetic activities of days exposure to 40 ppm butachlor sharply all phytoplankton species acclimated to low to declined (70%) carotenoids in Plectonema high light conditions. Inhibition of PS-II quantum boryanum [118]. Fenoxaprop-p-ethyl (6.25 ppm) yield varied between different groups of algae. stimulated β-carotene in Anabaena sp. GO10. Data showed that 50% inhibition in quantum yield Further, increase of herbicide suppressed this of PS-II was observed at 315 nM and 282 nM pigment in a dose dependent manner. The β- atrazine for diatoms and green algae, carotene was completely suppressed by 100 respectively, while 50% inhibition in quantum ppm of fenoxaprop. Herbicide cyhalofop-butyl at yield of PS-II of cyanobacteria were caused by 25 ppm partly stimulated β-carotene in this 102 nM of atrazine [58]. cyanobacterium but completely repressed at 400 ppm concentration [120]. The photosynthetic activities of Nodularia and Nostoc treated with 2,4 D or MCPA at 1 mM 4. PHOTOSYNTHESIS were not affected while were inhibited significantly with higher concentrations of The inhibition of pigment synthesis by alteration herbicide. Addition of 2,4 D at 10 mM to cultures in pigment synthesizing enzymes or due to resulted in 80% inhibition in photosynthesis while different mode of action of herbicides results in the effect of MCPA was more severe in a way alteration in photochemical activity which may that the cells began to consume oxygen in disturb the light harvesting complex or energy presence of light [66]. Photosynthetic electron transfer within photosystems which ultimately transport (Hill activity) and oxygen evolution in affect photosynthesis [97,126]. Thus, the both wild type and mutant cells of Anabaena response of cyanobacteria varied with type and doliolum were stimulated by glyphosate (50-200 nature of herbicide used. Atrazine was more ppm) but exhibited extreme inhibition by high toxic than its metabolites towards photosynthesis concentrations (200-400 ppm) of herbicide [129]. of cyanobacteria Anabaena inaequalis , Thiobencarb at 10 ppm decreased Anabaena cylindrica , Anabaena variabilis and photosynthesis by nearly 50% in Nostoc green algae Chlorella pyrenoidosa and sphaeroides [107]. Over 50% inhibition in Scenedesmus quadricauda with EC 50 values photosynthesis was observed in Anabaena ranging from 0.1 to 0.5 ppm [35]. The variabilis and Nostoc commune , when 8 to 10 supplementation of atrazine (1000 ppm) in ppm bensulfuron-methyl was applied to cultures growth medium marginally affected [87]. photosynthetic rate (10% of control) in resistant SG2 cyanobacterial strains falls of Mutant strain (Mu1) of Synechococcus sp. PCC Synechocystis /Pleurocapsa /Microcystis group 7942 exhibited superior photosynthetic activities and had no effect on growth rate. However, more in presence of butachlor under regular growth than 89% inhibition in photosynthesis was conditions compared to wild type. Further, Mu1 observed in Synechocystis sp. strain 6803 [73]. had an increased expression of PsbO at mRNA This is in contrast to results of Narusaka et al. and protein level and PsbO was tightly bound to [127] who showed that several herbicide Photosystem II, relative to wild type [130]. The resistant mutants of Synechocystis sp. strain effects of the commercial bentazon (basagran) PCC 6803 which grew slower under and molinate (ordham), recommended for IWM photosynthetic growth conditions and evolved on rice, were laboratory assessed on Anabaena 70% less oxygen than control strain grown under cylindrica in a short-term experiment of 72 h. The herbicide free conditions. Interestingly, Dalla- results revealed that photosynthesis was Chiesa and co-workers [128] reported that inhibited in a time and dose-response manner mutation in the D1 protein in serine 264 to proline and higher concentrations of ordham fully 264 of Synechocystis sp. strain PCC 6803 stopped O 2 evolution after 48 h [93]. allowed the strain to grow photoautotrophically and slightly resistant to atrazine, but oxygen Butachlor and fluchloralin exerted little effect on evolution was only 60% of that of wild-type photosynthetic oxygen evolution in Nostoc control 659 strain. The treatment of carotenoid muscorum and Gloeocapsa sp. whereas propanil inhibiting herbicide fluridone up to 100 ppb severely inhibited oxygen evolution in both the inhibited photosynthesis in light saturated cells of organisms [131,132]. Exposure of wild type and Oscillatoria agardhii [105]. Exposure to atrazine multiple herbicide resistant (MHR) strain of for 72 h at EC 50 doses to ten species of green Anabaena variabilis to 10-100 ppm of alachlor,

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arozin, butachlor and 2,4 D, led to the inhibition dependent manner in the presence of high of photosynthesis by 41-61% at 15 ppm and by concentrations (500-1000 ppm) of 2,4 D [135]. 50-55% at 80 ppm, respectively [27]. In another Sheeba et al. [97] reported reduction in study, butachlor (65 µM) treatment to photosynthesis, PS-I, PS-II and WCA in Nostoc Aulosira fertilissima for 15 days decreased muscorum and Phormidium foveolarum in photosynthesis, PS-I, PS-II and whole chain presence of 2,4 D with more pronounced effect activity by 24-48% [83]. Butachlor at LC 50 dose on former species than later one. When exposed significantly inhibited PS-I, PS-II and whole chain to diuron, the quantum yield of PS-II in activities of three species of Anabaena . These Synechocystis sp. and Microcystis aeruginosa activities declined in the range of 33-40% after decreased while oxadiazon (2.89 µM) decreased one day treatment which recovered gradually in PS-II quantum yield only in Synechocystis sp. subsequent days in Anabaena sp. PCC 7120, [136]. while A. doliolum and Anabaena LC31 exhibited continuous decrease with time [86]. Broser et al. [137] presented the first crystal structure of PS-II with bound herbicide terbutryn. Application of monosulfuron at 0.001-10 ppm The crystallized PS-II core complexes were exerted an inhibitory effect on photosynthesis in isolated from the thermophilic cyanobacterium three nitrogen fixing cyanobacteria Anabaena Thermosynechococcus elongatus . The herbicide azollae , A. flosaquae , and A. azotica leading to a terbutryn was bound via at least two hydrogen lower net photosynthetic rate and a smaller bonds to the Q(B) of reaction centers. Herbicide Fv/Fm ratio as revealed by chlorophyll a binding to PS-II further influenced the redox fluorescence studies [133]. DCMU (5 ppm) potential of Q(A), which is known to affect inhibited oxygen evolution by 75% in photoinhibition. cyanobacterial strain SG2 of Synechocystis /

Pleurocapsa /Microcystis group as reported by Sajjaphan et al. [73]. DCMU treated wild type 5. NITROGEN METABOLISM (0.4 ppm) and MHR strain (0.5 ppm) of Anabaena variabilis showed 80-87% inhibition in 5.1 Nitrogen Fixation photosynthetic O 2 evolution compared to untreated control cultures [56]. Butachlor, fluchloralin and propanil did not affect The study of Guanzon and Nakahara [134] nitrogenase activity of Nostoc muscorum but in revealed that Microcystis aeruginosa evolved Gloeocapsa sp. caused stimulation in nitrogen 50% less oxygen when treated with 8.4x10 -4 ppb fixation [131]. Nitrogenase activity of Nostoc G3 p-nitrophenyl 2,4,6-trichlorophenyl ether was completely inhibited in presence of goltix (50 compared to untreated control. Anilofos (1.25- and 100 ppm), arelon (15 and 30 ppm), paraquat 5.00 ppm) decreased photosynthetic oxygen (10 and 20 ppm) and 1 M DCMU [138]. evolution by 15-57%, PS-I and PS-II activity by Nitrogen fixing capacity of Anabaena inaequalis 18-61% and 25-75%, respectively, and whole and Anabaena cylindrica was sensitive to chain activity by 25-75% in Anabaena torulosa atrazine and its degradation products. Fifty [42]. Issa et al. [62] showed stimulation of percent reduction in nitrogen fixation was photosynthetic activity in Merismopedia glauca observed with all compounds at more than 100 by simazine (37-150 ppm) in a dose dependent ppm with the exception of atrazine when tested manner. Inhibition of photosynthesis was towards A. inaequalis which gave 50% inhibition maximum at IGC 50 concentration of 2,4 D in at 55 ppm [54]. Low concentration of 2,4 D (1 Nostoc muscorum followed by Gloeocapsa sp. and 10 ppm) stimulated nitrogen fixation in all the and Aphanocapsa sp. [81]. However, in strains of Anabaena while higher dose (100 ppm) Gloeopcapsa sp. and Anabaena UAM202 inhibited nitrogen fixation in strain ARM 299, photosynthesis was inhibited at higher ARM 308 and ARM 311 [139]. In another study, concentration of 2,4 D [66,67]. Photosynthetically cultures of Nostoc muscorum ISU exhibited 2 driven oxygen evolution was 10% less in fold inhibition in nitrogenase activity at IGC 50 resistant strain of Synechocystis strain SG2 while concentration of 2,4 D followed by Gloeocapsa wild strain exhibited 90% inhibition in oxygen sp. and Aphanocapsa sp. However, such evolution in presence of 2,4 D [73]. The rate of reduction in nitrogenase activity in Gloeocapsa photosynthesis in the unicellular cyanobacterium sp. and Anabaena UAM202 was found at much Synechococcus aeruginosus , isolated from rice higher concentration 175 ppm and 10 mM, field of India, declined in time and dose respectively [66,67].

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Alachlor (80 ppm) completely inhibited nitrogen sp. and Aphanocapsa sp. also exhibited fixation in Anabaena doliolum , Nostoc muscorum substantial inhibition in nitrogenase activity as and Aphanothece stagnina [140]. Butachlor compared to A. variabilis , N. punctiforme and N. enhanced the growth of Anabaena sphaerica calcicola at IGC 50 concentration of butachlor and and accelerated nitrogen fixation [141]. Alachlor alachlor [81]. When wild type and MHR strain of and butachlor at IGC 50 concentration (10-15 Anabaena variabilis were exposed to 10-100 ppm) exhibited substantial inhibition in nitrogen ppm alachlor, arozin, butachlor and 2,4 D, the fixation in Nostoc muscorum , Gloeocapsa sp. wild type at 15 ppm of all the herbicides exhibited and Aphanocapsa compared to Anabaena 75-95% nitrogenise activity while MHR strain at variabilis , Nostoc punctiforme and Nostoc 80 ppm of these herbicides exhibited 65-70% calcicola [81]. Likhitkar and Tarar [142] reported nitrogenase activity [27]. partial inhibition in nitrogenase activities at 200 ppm of butachlor in Nostoc commune and 5.2 Nitrogen Uptake and Its Assimilation Nostoc muscorum . Cyanobacteria use nitrate, nitrite and ammonium Isopropyl salt of glyphosate caused significant as nitrogen source for growth and development. inhibition in nitrogen fixation by Anabaena Scanty reports are available on effect of variabilis compared to free acid. The free acid herbicides on nitrogen source uptake and its form of glyphosate had no effect on nitrogen assimilation by cyanobacteria. The uptake of fixation even at 20 mM whereas 5 mM of nitrate and ammonium was inhibited by Machete isopropylamine salt caused 50% inhibition [59]. and Saturn in Nostoc sp., Nostoc calcicola and Nitrogenase activity of Anabaena variabillis Anabaena doliolum . However, 2,4-D (100 ppm) decreased by 94-98% and by 85-86% in Nostoc stimulated the uptake of nitrate but not of commune after 24 h of incubation with 10 ppm ammonium but higher doses of 2,4-D inhibited and 20 ppm of bensulfuron-methyl, respectively the uptake of both nitrogen sources [79]. Ethyl [87]. Molinate at 100 ppm inhibited nitrogen fixing ester salt of 2,4 D (15-60 ppm) inhibited nitrate capacity of Anabaena sp., Nostoc and Nodularia reductase and glutamine synthetase activities in sp. [88]. a dose dependent manner in Anabaena

Shaaban Dessouki et al. [143] observed that low fertilissima , Aulosira fertilissima and concentration of thiobencarb (1 ppm) enhanced Westiellopsis prolifica [113]. Singh et al. [149] nitrogenase activity of Nostoc kihlmani and reported that 30 µM of glyphosate inhibited Anabaena oscillatoriodes while higher ammonium uptake by Nostoc muscorum but the concentration was inhibitory. Butachlor (2-20 authors did not mention which formulation of ppm) exhibited significant reduction in glyphosate was used. Nitrate uptake by Nostoc nitrogenase activity (2-54%) of Nostoc muscorum muscorum and Phormidium foveolarum than thiobencarb which at 5 and 8 ppm decreased after exposure to oxyfluorfen (10 and concentrations caused a reduction of 16 and 20 ppm) and UV-treatment. Further, oxyfluorfen 32%, respectively [144]. Okmen and Ugur [145] alone and together with UV-B drastically compared the effect of herbicide bispyric sodium decreased NR activity in N. muscorum however on nitrogen fixing capacity of ten cyanobacterial NR activity increased in P. foveolarum [97]. isolates belonging to Anabaena , Gloeothece and Synechocystis . Nitrogen fixation was completely Treat ment with anilofos (5 ppm) for 12 h caused inhibited by 100 ppm of bispyribac in 12% reduction in nitrate and 26% reduction in Synechocystis sp. while in other cyanobacteria ammonium uptake with 22% inhibition in 500 ppm bispyribac was effected. The reduction glutamine synthetase activity in Anabaena in nitrogen fixation in cyanobacteria by herbicides torulosa . The decrease in photosynthetic rate by may be due to low photosynthetic rate anilofos may probably have caused low rate of [93,107,146] which provides reductant and ATP nitrate uptake. Interference of herbicide with to nitrogenase and carbon skeleton to fix membrane potential of cyanobacterium may nitrogen [147,148]. have caused low uptake of ammonium which further reduced GS activity due to less availability Arozin (10 ppm) has been reported to enhance of ammonium [42]. Herbicides isoproturon and nitrogenase activity in Anabaena variabilis ARM butachlor at 10 µM inhibited nitrate and nitrite 310 [115]. Likhitkar and Trar [142] reported uptake in time dependent manner in Anabaena partial inhibition of nitrogenase activity in Nostoc variabilis up to 24 h treatment. Further, nitrate commune and Nostoc muscorum at 200 ppm of and nitrite reductase activities of this butachlor . Nostoc muscorum ISU, Gloeocapsa cyanobacterium were also inhibited [150].

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6. STRESS TOLERANCE MECHANISM whereas resistant strain exhibited increasing trend (increased by 2-3 folds) with treatment of Toxicity of herbicides may lead to the generation 150 µM bromoxynil [92]. To determine whether of free radicals and cyanobacteria may respond diclofop acid and its enantiomers affected to this stress by inducing enzymatic as antioxidants of Microcystis aeruginosa , the well non enzymatic antioxidant mechanism activity of SOD was determined after treatment [42,43,124,151]. Superoxide dismutase (SOD) is with 1-5 ppm of herbicide. After 48 h exposure, involved in the neutralization of highly reactive all the species of herbicide increased SOD oxygen species (ROS) such as superoxide activity. Diclofop acid (1-5 ppm) increased radicals and singlet oxygen resulting in the activity by 1.3-1.53 folds while R-diclofop generation of the lesser toxic hydrogen peroxide increased activity of SOD by 1.7-3.36 folds, (H 2O2). H 2O2 is still harmful to cells requiring whereas S-enantiomers increased the activity of removal by catalase (CAT) and/ or peroxidase SOD by 1.91-3.41 folds [152]. The increase in (POD) enzymes [123]. the level of free radicals by butachlor (5-40 ppm) in a five day experiment triggered the production 6.1 Enzymatic Antioxidant System of SOD, POD and CAT in a dose dependent manner in Plectonema boryanum [118]. Few reports are available in literature on the Butachlor at 40 and 80 ppm enhanced the response of enzymatic antioxidant system of activities of SOD, CAT, POD and GR significantly cyanobacteria to herbicides. Bentazon induced in Nostoc sp. [84]. Oxyflurafen (10 ppm) alone oxidative stress is a manifestation of multistep increased level of SOD and CAT in Nostoc reactions, resulting in membrane damage muscorum , however, when oxyflurafen treatment leading to the production of free radicals which was combined with UV-B, the activities of these may be scavenged by antioxidant enzymes such enzymes decreased. On the other hand, in as SOD, CAT and POD. Galhano et al. [151] Phormidium foveolarum only 20 ppm oxyflurafen reported significant increase in SOD (13-15%), could cause a decrease in CAT activity and 20 POD (20-188%) and CAT (35-46%) activities in a ppm herbicide along with UV-B decreased POD time- and dose-dependent manner in Anabaena activity as well [97]. cylindrica when treated with bentazon (0.75- 2 mM). Anilofos (20 ppm) caused 3 fold increase in Irgarol 1051 (0.01 µM) and diuron (0.09 µM) SOD, 2 fold increase in POD and 2.8 fold greatly enhanced CAT activity in Synechococcus increase in CAT activities in Oscillatoria sp. PCC 7942 which gave evidence of enhanced simplicissima [41] while the activity of these free radical production under herbicide stress. enzymes increased by 1.8-3.5 fold in Anabaena However, the suppression of CAT activity under torulosa after treatment with 1.25 - 5 ppm of high concentrations of Irgarol 1051 (>0.01 µM) herbicide [42]. The stimulation SOD (137-180%), and diuron (>0.09 µM) indicated that antioxidant POD (104-174%) and CAT (109-131%) activities defense enzymes might be an important site of over control by 5-20 ppm of the same herbicide action for Irgarol 1051 and diuron in this in another cyanobacterium Synechocystis sp. cyanobacterium [100]. PUPCCC 64 has also been reported [43]. Contrary to these reports, molinate (0.75-2.0 Glutathion-s-transferase catalyses the mM) decreased the activity of SOD (34-92%), conjugation of the reduced form POD (70-88%) and CAT (25-95%) in a time and of glutathione (GSH) in response to pollutants in concentration dependent manner in Nostoc order to make the compounds more soluble muscorum [124]. [153]. This activity detoxifies endogenous compounds such as peroxidised lipids and In bloom forming Microcystis novaci and nitrogen enables the breakdown of xenobiotics. GSTs fixing Anabaena sp. cultures, the addition of may also bind toxic substances and function as DCMU (10 µM) did not have significant effect on transport proteins [154]. Herbicide stress also SOD activity in the UV-B irradiated cells however influences the activity of GST in cyanobacteria the addition of glyphosate and MCPA decreased which depends upon its nature and type of SOD activity compared with UV treatment alone cyanobacteria. and the activity was not restored even after glyphosate and MCPA were removed during Treatment with bentazon (0.75-2 mM) for 72 h recovery process [125]. Wild strain of significantly increased GST activity by 25- 296% Synechococcus elongatus PCC 7942 showed an in Anabaena cylindrica [151]. In another study, downward trend of SOD and POD activity however, molinate (0.75-2.0 mM) decreased the

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activity of GST in a time and concentration PCC 7942 [92]. Butachlor at LC 50 dose dependent manner in Nostoc muscorum [124]. registered a slight increase in total glutathione Wild strain of Synechococcus elongatus PCC content in Anabaena LC31 (2.7 fold) than in 7942 exhibited time dependent inactivation of Anabaena 7120 (2.5 fold) and Anabaena GST in presence of bromoxynil (30 µM). The doliolum (2.48) [86]. response of mutant strain on the other hand, was different with the addition of bromoxynil (150 µM) Accumulation of proline has been reported to be which exhibited significant increase (65-80%) in an important biomarker of tolerance capacity in the activity of GST [92]. Agrawal et al. [86] plants, bacteria, protozoa, algae, marine reported that treatment with butachlor at LC 50 invertebrates, and also in cyanobacteria, due to appreciably increased the GST activity in three its function as a stabilizer, a metal chelator, an species of cyanobacterium Anabaena, being inhibitor of lipid peroxidation, and a scavenger of maximum in Anabaena LC31 (2.49 fold) followed singlet oxygen and hydroxyl radicals [162 and by Anabaena 7120 (2.1 fold) and A. doliolum 163]. Paraquat at concentration ranging from 1- (1.92 fold). 20 x 10 -7 M increased proline content by 136- 605% in Anabaena variabilis and by 105-297% in 6.2 Non-enzymatic Antioxidant System Plectonema boryanum indicating its involvement in detoxification of free radicals [48]. Proline A number of low molecular weight compounds content increased significantly in a time- and such as reduced glutathione (GSH), proline, dose-dependent manner under bentazon (0.75- ascorbate, tocopherol and carotenoids are 2.0 mM) stress conditions in Anabaena reported to play key role to counter abiotic stress cylindrica . After 72 h, proline content was higher caused by pollutants in plants [123,155]. The than control by 31, 166, and 655% in 0.75, 1.5, primary function of GSH appears to be in the and 2 mM of bentazon concentration, maintenance of intracellular redox homeostasis respectively [151]. Oxyflurafen (10 and 20 ppm) by affording protection against ROS [156,157]. and UV-B individually showed accumulation of The effect of abiotic stresses on GSH proline in Nostoc muscorum while in combination concentration in cyanobacteria is controversial as of these stresses, proline content decreased some researchers reported an increase in GSH indicating severity of toxicity. In contrast to this, with increasing stress while, others reported a proline showed continuous increase in decrease in GSH [158,159]. Bhunia et al. [158] Phormidium foveolarum under oxyflurafen and reported that total glutathione (GSH and GSSG) UV-B treatments suggesting its protective role level was reduced in a dose-dependent manner during stress [97]. Molinate (0.75-2.0 mM) in Nostoc muscorum when exposed to the treatment significantly increased endogenous carbamate herbicide benthiocarb. GSH (14-66%) level of proline by 45-156% above control in and GSSG (20-54%) levels significantly Nostoc muscorum [124]. Anilofos (10-20 ppm) decreased in time- and concentration dependent stimulated the synthesis of proline in Oscillatoria manner in a 72 h experiment of bentazon (0.75-2 simplicissima in a dose dependent manner and mM) exposure to Anabaena cylindrica [151]. In maximum increase (369%) was reported in another study, the same authors have reported a highest tested dose (20 ppm) of herbicide [41]. decrease in GSH and GSSG content in Nostoc Significant enhancement of proline content (1.6 muscorum with treatment of 0.75-2 mM molinate fold over control) by anilofos in Anabaena [124]. Cellular GSH content of Synechocystis sp torulosa and Synechocystis sp. PUPCCC 64 has PUPCCC 64 was significantly less under stress also reported [42,43]. of 10 and 20 ppm anilofos [43]. Kumari et al. [83] demonstrated a decrease in the total GSH Ascorbate functions as a source of reductant for content in Aulosira fertilissima with 65 µM many reactive oxygen species, thereby butachlor treatment. Since chloroacetanilides are minimizing the damage caused by pollutant known to react with sulfhydryl group [160] and stress. Ascorbate scavenges not only H 2O2 but - metachlor (analogue of butachlor) covalently also other free radicals such a O 2 and OH` and modifies the cysteine residue in vitro [161], lipid hydroperoxide without enzyme catalysis therefore, butachlor might react with thiol and [164]. Only few reports on the role of ascorbate glutathione, thereby reducing their contents. The in mitigating the herbicide stress in cyanobacteria cellular levels of GSH significantly increased in are available. Cellular ascorbate content was response to treatment with bromoxynil whereas affected by anilofos in dose dependent manner in GSSG level reduced in both wild and Oscillatoria simplicissima . Maximum decrease mutant strains of Synechococcus elongatus (85%) was reported in 20 ppm of anilofos [41]. In

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another study, herbicide anilofos (1.25-5.0 ppm) The cyanobacterium Anabaena inaequalis significantly decreased the ascorbate content by metabolized isoproturon ((3-(4-isopropyl phenyl)- 60-75% in Anabaena torulosa [42]. 1,1- dimethyl urea). The rate of degradation of isoproturon was 25% faster at pH 5.5 than at pH 7. BIODEGRADATION OF HERBICIDES 7.5 when measured in ten day old culture. This 14 was confirmed by using C labelled isoproturon Cyanobacteria have been fully exploited for and its metabolites accumulated in cells. Four biological treatment of polluted waters, but only detectable metabolic products such as little information is available on as how monodesmethyl-IPU, OH-monodesmethyl-IPU, cyanobacteria participates in the process of Didesmethyl-IPU and iso-propylaniline of biodegradation of chemical pollutants. It has isoproturon have been identified in this been suggested that wild type cells of cyanobacterium [170]. Synechocystis sp. PCC 6803 contain Mansy and Bestawy [109] studied the nitroreductase like DrgA protein encoded by Drg biodegradation potential of fluomenturon by six A gene which is involved in detoxification of cyanobacterial species belonging to Microcystis herbicide dinoseb via the reduction of the nitro aeruginosa (three strains), Anabaena cylindrica , group(s) and this process is accompanied by the Anabaena flosaquae and Anabaena spiroides . formation of toxic superoxide anions [165]. Exposure of these cyanobacterial strains to different concentrations of fluomenturon (0.14, Cyanobacteria Anabaena variabilis and 0.7 and 1.4 ppm) at different exposure times (1-5 Synechocystis 6803 take up intracellularly day) showed that biodegradation of herbicide different formulations of glyphosate when was species specific and primarily correlated with supplied in growth medium in the concentration exposure time reaching maximum efficiency after range of 5-20 mM. The rate of uptake of 5 days. Efficiency of these strains to biodegrade herbicide was highest for roundup and lowest for fluometuron was in the range 39-100%. free acids [59]. Ravi and Balakumar [166] Grötzschel et al. [171] studied biodegradation of reported that extracellular phosphatases 2,4 D by hypersaline cyanobacterial dominated produced by Anabaena variabilis were able to mat collected from Guerrero Negro, Mexico hydrolyze the C-P bond of glyphosate, With under both photoautotrophic and heterotrophic regard to degradation of herbicide in aqueous conditions. Within 13 days, light/dark incubated medium, Lipok et al. [167] concluded that mixed mats degraded 97% of the herbicide in light culture of Spirulina spp. exhibited a remarkable where as in permanent darkness only ability to degrade glyphosate. The rate of 13% herbicide was degraded. Another glyphosate biodegradation in the medium was cyanobacterium Anabaena fertilissima was also independent of its initial concentration. They reported to biodegrade this herbicide. The further suggested that glyphosate degradation exposure of cyanobacterium to 60 ppm of 2,4 D pathway in Spirulina might be different from produced butyl ester after 4 days while isobutyric those exhibited in other bacteria. According to acid, allyl ester and 3-bromobutyric acid were them, occurrence of herbicide metabolism in this recorded after 60 days. The exposure of this cyanobacterium is evident, as the species was cyanobacterium to 80 ppm 2,4 D for 4 days able to grow in a medium supplemented with yielded hydroxyl urea and trifluroacetic acid, 2- phosphonate herbicide as the only source of methyl propyl ester. Acetic acid 2-propenyl ester, phosphorus, where the rate of herbicide another product of 2,4 D was observed after 16 transformation was found to be depended upon days of treatment. Another cyanobacterium the cells phosphorus status. Lipok et al. [168] re- Westiellopsis prolifica produced 2,4 D methyl confirmed the ability of the S. platensis to ester and acetic acid after 4 and 16 days of catalyze glyphosate metabolism. Four exposure to 120 ppm of 2,4 D, respectively [172]. cyanobacterial strains ( Anabaena sp., Leptolyngbya boryana , Microcystis aeruginosa Commercially available mixed culture of Spirulina and Nostoc punctiforme ), out of the six strains spp. exhibited a remarkable ability to biodegrade studied by Forlani et al. [60], were able to use the the widely used herbicide glyphosate that served glyphosate as the only source of phosphorus. as a sole source of either phosphorus or Dyhrman et al. [169] reported the existence nitrogen. Phosphorus starvation of cells of phosphorous dependent glyphosate influenced the rate of glyphosate degradation. transformation in marine cyanobacterium Further, the occurrence of additional peaks in Trichodesmium erythraeum . NMR spectra which did not overlap with those of

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the most common intermediate of glyphosate biomass, pH 8.0 and 30 oC. The growth of degradation suggested that the cyanobacterium cyanobacterium in phosphate deficient basal might degrade herbicide through a pathway medium supplemented with 2.5 ppm anilofos different from previously elucidated in bacteria indicated that herbicide was used by the strain [168]. Forlani et al. [60] evaluated the ability of PUPCCC 64 as a source of phosphorus [43]. six strains of cyanobacteria to use glyphosate as a source of phosphorus when incorporated in Crouzet et al. [175] developed a microcosm in growth medium in the absence of phosphate laboratory containing soil cyanobacterial source. Of these, four cyanobacteria Arthrospira communities to study the dissipation of pure form fusiformis , Leptolyngbya boryana, Nostoc of mesotrione and its formulation callisto. punctiforme and Spirulina platensis were able to Application of mesotrione at the rate of field grow in presence of glyphosate indicating use of application (3.4 µg kg -1) caused approximately herbicide as a source of phosphorus. 75% dissipation within 14 days of treatments both in pure and formulation form while The cyanobacterium Synechococcus elongatus application at 10 folds concentration to field dose takes up triazine herbicides atrazine and application, only resulted in 49 and 38% terbutryn (0.025-0.75 µM) intracellularly from the dissipation of initial applied pure mesotrione and growth medium. The maximum uptake (50%) of formulation, respectively. The cyanobacterial these herbicides was observed at 12 and 6 h for communities in microcosm were able to remove atrazine and terbutryn, respectively. Data on 20% herbicide from 100 fold concentration to herbicides bioaccumulation revealed that the limit field dose. The nitrogen fixing cyanobacterium value of accumulated herbicide after 12 h was 9 Nostoc muscorum took up butachlor µmol g -1 dry biomass for atrazine and 12 µmol g -1 intracellularly from medium. The GC-MS analysis dry biomass for terbutryn after 18 h of incubation of cell extract made from butachlor treated cells [173]. Another cyanobacterium Microcystis after 72 h treatment indicated the presence of 1, novacekii grown in medium containing 50-500 2- benzenedicarboxylic acid and phenol as major ppb atrazine removed 27% atrazine after 96 h. biodegradation products [85]. Spontaneous degradation was found to be less than 9% at 500 ppb concentration indicating a Safi et al. [176] investigated the bioremediation high efficiency for bioaccumulation of atrazine by of diuron in soil environment by cyanobacterial the test organism. No metabolite was detected in mats collected from agricultural fields of Gaza, the culture medium at any of the doses studied Palestine. Diuron (0.055-0.88 ppm) was injected [57]. in water saturated soil samples pre-treated with cyanobacterial mat for several times. Growth of Biodegradation of acetachlor by cyanobacterial Jews mallow as a test plant was taken as mat collected from Wadi Gaza near indicator of biodegradation of Diuron. Results mediterranean sea was studied by El-Nahhal et revealed that diuron was degraded in soil and al. [174]. Acetachlor (0.2-1.0 mg/kg soil) was degradation was more pronounced when diuron added to soil and water samples pre-inoculated was incubated with cyanobacterial in the with cyanobacterial mat were inoculated. Results irrigation water. These encouraging results showed that acetachlor was degraded in both suggest that application of cyanobacterial mats soil and water system with much faster rate in could be a suitable method to remediate soil later system. Acetachlor concentration above pollution. Sorption of herbicides, Paraquat and 2, field rate did not affect the biodegradation 4-D by Oscillatoria sp. dominated cyanobacterial process in the water whereas it did in soil. mat was studied as a function of pH, temperature Furthermore, bioremediation in water system and biomass. Mat biomass was an effective was nearly completed in 15 days of treatment but sorbent for paraquat but not for 2, 4 D. Increase did not reach high percentage of degradation in in temperature also increased sorption of soil system. paraquat while 2,4 D showed opposite trend [177]. The cyanobacterium Synechocystis sp. strain PUPCCC 64 was able to take up anilofos (10 8. FUTURE PROSPECTS ppm) intracellularly and metabolized it. The uptake of herbicide by the microorganism was • Although effect of herbicides on toxicity, fast in the initial six hours followed by slow photo pigments and photosynthesis of uptake until 120 hours. The organism exhibited cyanobacteria are well document in maximum anilofos removal at 100 mg protein -1 literature, interaction of herbicides on

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enzymes of these physiological processes 7. Liu CJ, Men WJ, Liu YJ, Zhang H. The needs further attention. pollution of pesticides in soils and its • It would be interesting to know the detailed bioremediation. Syst Sci Compreh Stud mechanism of degradation of herbicides Agricul. 2002;18:295-97. by cyanobacterial enzymes / or genes(s) 8. Mukerjee SK. Pesticide use. In: Chadha involved. KL, Swaminathan MS, eds. Environment • Cyanobacterial biosensors are not popular and Agriculture. New Delhi: Malhotra as compared to bacterial biosensors and Publishing House. 2006;211-227. thus there is plenty of scope for future 9. Pimentel D. Environmental and economic research and development in this field. costs of the application of pesticides

primarily in the United States. In: Rajinder 9. CONCLUSION P, Dhawan A. eds. Integrated pest

management: Innovation-development The toxic effect of herbicides on photosynthetic process. Springer. 2009b;1:88-11. pigments, photosynthesis and nitrogen assimilation by cyanobactieria varied with the 10. Dorigo U, Leboulanger C, Bérard A, nature, class and mode of action of chemical(s) Bouchez A, Humbert JF, Montuelle B. and type and nature of organisms. These Lotic biofilm community structure and microorganisms tolerated herbicides by pesticide tolerance along a contamination stimulatiion of enzymatic and non enzymatic gradient in a vineyard area. Aquat antioxidant system or they followed the route of Microbial Ecol. 2007;50:91-102. herbicide biodegradation. 11. Schuler LJ, Rand GM. Aquatic risk assessment of herbicides in fresh water ACKNOWLEDGEMENT ecosystem of South Floida. Arch Environ Contam Toxicol. 2008;54:571-83. The authors thank Head and Coordinator, DRS 12. Aoki I. Diversity-productivity-stability SAP-II of UGC and FIST of DST for providing relationship in fresh water ecosystems: facilities to assess literature through net. Whole-systemic view of all trophic levels. Ecol Res. 2003;18:397-04. COMPETING INTERESTS 13. Fenchel T. The microbial loop-25 years

later. J Exp Marine Biol Ecol. Authors have declared that no competing 2008;366:99-103. interests exist. 14. Vermaas WFJ. Photosynthesis and REFERENCES respiration in cyanobacteria. In: Encyclopedia of Life Sciences. London: 1. Ash C, Jasny BR, Malakoff DA, Sugden Nature Publishing Group. 2001;245-51. AM. Feeding the future. Science. 15. Berry JP, Gantar M, Perez MH, Berry G, 2010;327:797. Noriega FG. Cyanobacterial toxins as 2. Zhang WJ. A forecast analysis on world allelochemicals with potential applications population and urbanization process. as algaecides, herbicides and insecticides. Enviro Develop Sustain. 2008;10:717-30. Marine Drugs. 2008;6:117-46. 3. Zhang WJ, Pang Y. Impact of IPM and 16. Schopf JW. The fossil record: Tracing of transgenics in the Chinese agriculture. In: the roots of the cyanobacteria lineage. In: Peshin R, Dhawan AK, eds, Integrated Whitton BA, Potts M, eds. The ecology of Pest Management: Dissemination and cyanobacteria: their diversity in time and Impact. Springer. 2009;525-55. space. Dordrecht, The Netherland: Kluwer 4. Anonymous. Editorial - How to feed a Academic Publishers. 2000;13-35. hungry world? Nature. 2010;466:531-532. 17. Wolk CP, Ernst A, Elhai J. Heterocyst 5. Pimentel D. Pesticides and pest control. In: metabolism and development. In: Bryant Rajinder P, Dhawan A, eds. Integrated DA, ed. The molecular biology of pest management: innovation- cyanobacteria. Dordrecht, The development process. Springer. 2009a; Netherlands: Kluwer Academic Publishers. 1:83-87. 1994;769-823. 6. Cai DW. Understand the role of chemical pesticides and prevent misuses of 18. Fritsch FE. The structure and reproduction pesticides. Bull Agricul Sci Technol. of the algae. Cambridge University Press, 2008;1:36-38. Cambridge. 1945;2:796-800.

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Peer-review history: The peer review history for this paper can be accessed here: http://sciencedomain.org/review-history/13074

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