Abstract
Among the non-target microorganisms residing in crop fields that are potentially vulnerable to herbicides are cyanobacteria. They contribute to the maintenance of soil quality and fertility and hence are considered to be an important component of soil microflora. Consequently, the present study was aimed to check the influence of the herbicide 2,4-dichlorophenoxyacetic acid (2,4-D) on some major parameters of carbon (CO2) and nitrogen (N2) fixations of a cyanobacterium Nostoc muscorum Meg 1 isolated from a rice field in Cherrapunji, Meghalaya, India. These include various photosynthetic pigments, the oxygen-evolving complex activity of the PSII, the protein contents of RuBisCO, D1 protein, isocitrate dehydrogenase (IDH), nitrogenase and glutamine synthetase (GS) enzymes, the heterocyst percentage, nitrogenase and GS enzyme activities, and production of total proteins and carbohydrates in the cyanobacterium in a varying range of 50 to 125 ppm doses of 2,4-D. The mRNA levels of several proteins were also analyzed. Besides carotenoid concentration that enhanced at 50 ppm, all other parameters were compromised by 2,4-D in a dose-dependent manner resulting in a reduction in photosynthetic and N2-fixing activities. The negative effect on N2-fixation was partly due to compromised IDH activity. RT-PCR analysis further showed that these negative effects were initiated at transcription levels as mRNA contents of all enzymes studied were found compromised under 2,4-D exposure. The scanning and transmission electron microscopy further revealed herbicide induced adverse changes in the morphology and ultrastructure of the organism. The significance of the work lies in its detailed analysis of the effect of 2,4-D at biochemical, physiological, and molecular levels.
Similar content being viewed by others
Data availability
All the data generated during this study have been provided in the manuscript.
References
Ahad RIA, Goswami S, Syiem MB (2017) Biosorption and equilibrium isotherms study of cadmium removal by Nostoc muscorum Meg 1: morphological, physiological and biochemical alterations. 3 Biotech 7:1–12
Ahmad M, Pataczek L, Hilger TH et al (2018) Perspectives of microbial inoculation for sustainable development and environmental management. Front Microbiol 9:1–26
Aktar MW, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2:1–12
Allen MM, Turnburke AC, Lagace EA, Steinback KE (1983) Effects of photosystem II herbicides on the photosynthetic membranes of the cyanobacterium Aphanocapsa 6308. Plant Physiol 71:388–392
Antonacci A, Lambreva MD, Margonelli A et al (2018) Photosystem-II D1 protein mutants of Chlamydomonas reinhardtii in relation to metabolic rewiring and remodelling of H-bond network at QB site. Sci Rep 8:1–14
Bargaz A, Lyamlouli K, Chtouki M et al (2018) Soil microbial resources for improving fertilizers efficiency in an integrated plant nutrient management system. Front Microbiol 9:1606
Barthel S, Bernát G, Seidel T et al (2013) Thylakoid membrane maturation and PSII activation are linked in greening Synechocystis sp. PCC 6803 cells. Plant Physiol 163:1037–1046
Bennett A, Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58:419–435
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Casella S, Huang F, Mason D et al (2017) Dissecting the native architecture and dynamics of cyanobacterial photosynthetic machinery. Mol Plant 10:1434–1448
Chapman RL (2013) Algae: the world’s most important “plants”—an introduction. Mitig Adapt Strateg Glob Chang 18:5–12
Chen L, Xie M, Bi Y et al (2012) The combined effects of UV-B radiation and herbicides on photosynthesis, antioxidant enzymes and DNA damage in two bloom-forming cyanobacteria. Ecotoxicol Environ Saf 80:224–230
Chittora D, Meena M, Barupal T, Swapnil P (2020) Cyanobacteria as a source of biofertilizers for sustainable agriculture. Biochem Biophys Reports 22:100737
Damalas CA, Eleftherohorinos IG (2011) Pesticide exposure, safety issues, and risk assessment indicators. Int J Environ Res Public Health 8:1402–1419
de Castro Marcato AC, de Souza CP, Fontanetti CS (2017) Herbicide 2, 4-D: a review of toxicity on non-target organisms. Water Air Soil Pollut 228:120
Demoulin CF, Lara YJ, Cornet L et al (2019) Cyanobacteria evolution: insight from the fossil record. Free Radic Biol Med 140:206–223
Deng L, Senseman SA, Gentry TJ et al (2015) Effect of selected herbicides on growth and lipid content of Nannochloris oculata. J Aquat Plant Manag 53:28–35
DeRuyter YS, Fromme P (2008) Molecular structure of the photosynthetic apparatus. In: Herrero A, Flores E (eds) The cyanobacteria, molecular biology, genomics and evolution. Caister Academic Press, pp 217–269
Fróna D, Szenderák J, Harangi-Rákos M (2019) The challenge of feeding the world. Sustainability 11:5816
Galhano V, Peixoto F, Gomes-Laranjo J, Fernández-Valiente E (2010) Comparative toxicity of bentazon and molinate on growth, photosynthetic pigments, photosynthesis, and respiration of the portuguese ricefield cyanobacterium Nostoc muscorum. Environ Toxicol 25:147–156
Gupta SK, Chakraborty AP (2020) Cyanobacterial biofertilizer for sustainable agriculture and environment. Int J Creat Res Thoughts 8:4–10
Hall L, Beckie H, Wolf TM (1999) How herbicides work. In: How herbicides work: Biology to application. Agriculture, Food and Rural Development. Publishing Branch, Edmonton, Alberta, pp 1–146
Issa AA, Abd-Alla MH, Ohyama T (2014) Nitrogen fixing cyanobacteria: future prospect. Adv Biol Ecol nitrogen Fixat 2:24–48
Jhala YK, Panpatte DG, Vyas RV (2017) Cyanobacteria: source of organic fertilizers for plant growth. In: Panpatte D, Jhala Y, Vyas R, Shelat H (eds) Microorganisms for green revolution. Microorganisms for Sustainability, Springer, Singapore, pp 253–264
Jyothi KBL (2016) Study of herbicidal effect 0f 2, 4-D on growth and cellular metabolites in cyanobacterium Synechococcus aeruginosus from rice fields. J Algal Biomass Utln 7:1–3
Kaushik BD (2014) Developments in cyanobacterial biofertilizer. Proc Indian Natl Sci Acad 80:379–388
Kumar K, Mella-Herrera RA, Golden JW (2010) Cyanobacterial heterocysts. Cold Spring Harb Perspect Biol 2:1–20
Kumar NJI, Amb MK, Kumar RN, Bora A (2010) Consequences of 2, 4-D and pencycuron treatment on three different cyanobacterial species-Anabaena fertilissima Rao, Aulosira fertilissima Ghose and Westiellopsis prolifica Janet. Electron J Environ Agric Food Chem 9:847–859
Kuznecova J, Šulčius S, Vogts A et al (2020) Nitrogen flow in diazotrophic cyanobacterium Aphanizomenon flos-aquae is altered by cyanophage infection. Front Microbiol 11:1–14
Kynshi BL, Sachu M, Syiem MB (2021) Modulation in isocitrate dehydrogenase activity under citrate enrichment affects carbon and nitrogen fixations in the cyanobacterium Nostoc muscorum Meg 1. Biochimie 186:94–104
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278
Lopes G, Clarinha D, Vasconcelos V (2020) Carotenoids from cyanobacteria: a biotechnological approach for the topical treatment of psoriasis. Microorganisms 8:302
Mackinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322
Marin-Morales MA, Ventura-Camargo BDC, Hoshina MM (2013) Toxicity of herbicides: impact on aquatic and soil biota and human health. In: Price AJ, Kelton JA (eds) Herbicides–current research and case studies in use. InTech Rijeka, Croatia, pp 399–443
Meeks JC (1998) Symbiosis between nitrogen-fixing cyanobacteria and plants. Bioscience 48:266–276
Meeks JC, Elhai J (2002) Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66:94–121
Meena RS, Kumar S, Datta R et al (2020) Impact of agrochemicals on soil microbiota and management: a review. Land 9:1–21
Mona S, Kumar V, Deepak B, Kaushik A (2020) Cyanobacteria: the eco-friendly tool for the treatment of industrial wastewaters. In: Bharagava R, Saxena G (eds) Bioremediation of industrial waste for environmental safety. Springer, Singapore, pp 389–413
Morgan RC (1967) The carotenoids of Queensland fruits -carotenes of the watermelon (Citrullus vulqaris). J Food Sci 32:275–278
Muro-Pastor MI, Florencio FJ (1992) Purification and properties of NADP-isocitrate dehydrogenase from the unicellular cyanobacterium Synechocystis sp. PCC 6803. Eur J Biochem 203:99–105
Murton J, Nagarajan A, Nguyen AY et al (2017) Population-level coordination of pigment response in individual cyanobacterial cells under altered nitrogen levels. Photosynth Res 134:165–174
Nirmal Kumar JI, Bora A, Amb MK, Kumar RN (2011) An evaluation of pesticide stress induced proteins in three cyanobacterial species Anabaena fertilissima, Aulosira fertilissima and Westiellopsis prolifica using SDS-PAGE. Adv Env Biol 5:739–745
Nongbri BB, Syiem MB (2012) Analysis of heavy metal accumulation in water and fish (Cyprinus carpio) meat from Umiam Lake in Meghalaya, India. Int Multidiscip Res J 2:73–76
Okmen G, Turkcan O, Erdal P (2013) Effect of herbicides on chlorophyll-a, β- carotene, phycocyanin and allophycocyanin content of Anabaena sp. J Appl Biol Sci 7:20–27
Pansook S, Incharoensakdi A, Phunpruch S (2019) Effects of the photosystem II inhibitors CCCP and DCMU on hydrogen production by the unicellular halotolerant cyanobacterium Aphanothece halophytica. Sci World J 2019:1–11
Pathak J, Maurya PK, Singh SP et al (2018) Cyanobacterial farming for environment friendly sustainable agriculture practices: innovations and perspectives. Front Environ Sci 6:1–13
Pimentel D (2009) Pesticides and pest control. In: Peshin R, Dhawan AK (eds) Integrated pest management: innovation-development process. Springer, Dordrecht, pp 83–87
Popp J, Pető K, Nagy J (2013) Pesticide productivity and food security. A review. Agron Sustain Dev 33:243–255
Prasanna R, Jaiswal P, Nayak S et al (2009) Cyanobacterial diversity in the rhizosphere of rice and its ecological significance. Indian J Microbiol 49:89–97
Rahaman MM, Islam KS, Jahan M (2018) Rice farmers’ knowledge of the risks of pesticide use in Bangladesh. J Heal Pollut 8:181203
Rai AN, Borthakur M, Bergman B (1992) Nitrogenase derepression, its regulation and metabolic changes associated with diazotrophy in the non-heterocystous cyanobacterium Plectonema boryanum PCC 73110. J Gen Microbiol 138:481–491
Rashkov GD, Dobrikova AG, Pouneva ID et al (2012) Sensitivity of Chlorella vulgaris to herbicides. Possibility of using it as a biological receptor in biosensors. Sensors Actuators B Chem 161:151–155
Raven JA, Beardall J (2003) Carbohydrate metabolism and respiration in algae. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Springer, Pp 205–224
Rippka R, Deruelles J, Waterbury JB (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Robinson SJ, Deroo CS, Yocum CF (1982) Photosynthetic electron transfer in preparations of the cyanobacterium Spirulina platensis. Plant Physiol 70:154–161
Roe JH (1955) In blood and reagent*. J Biol Chem 212:335–343
Sachu M, Kynshi BL, Syiem MB (2021) Herbicide monuron mediated alterations in carbon and nitrogen fixation in the cyanobacterium Nostoc muscorum Meg 1. J Appl Phycol 33:2209–2220
Sampaio MJAM, Rowell P, Stewart WDP (1979) Purification and some properties of glutamine synthetase from the nitrogen-fixing cyanobacteria Anabaena cylindrica and a Nostoc sp. J Gen Microbiol 111:181–191
Schreiber U, Gademann R, Bird P et al (2002) Apparent light requirement for activation of photosynthesis upon rehydration of desiccated beachrock microbial mats. J Phycol 38:125–134
Senseman SA (2007) Herbicide handbook (No. 632.954 W394h9). In: Lawrence, US: Weed Science Society of America, 9th edn. Kansas, pp 458
Sharma A, Kumar V, Shahzad B et al (2020) Photosynthetic response of plants under different abiotic stresses: A review. J Plant Growth Regul 39:509–531
Sheeba SVP, Srivastava PK, Prasad SM (2011) Differential physiological and biochemical responses of two cyanobacteria Nostoc muscorum and Phormidium foveolarum against oxyfluorfen and UV-B radiation. Ecotoxicol Environ Saf 74:1981–1993
Singh AK, Singla P (2019) Biodegradation of diuron by endophytic Bacillus licheniformis strain SDS12 and its application in reducing diuron toxicity for green algae. Environ Sci Pollut Res 26:26972–26981
Singh DP, Khattar JIS, Kaur G, Singh Y (2016) Toxicological impact of herbicides on cyanobacteria. Annu Res Rev Biol 9:1–39
Singh JS, Kumar A, Rai AN, Singh DP (2016) Cyanobacteria: a precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front Microbiol 7:1–19
Singh S, Datta P (2005) Growth and survival potentials of immobilized diazotrophic cyanobacterial isolates exposed to common ricefield herbicides. World J Microbiol Biotechnol 21:441–446
Sterling TM (1994) Mechanisms of herbicide absorption across plant membranes and accumulation in plant cells. Weed Sci 42:263–276
Stewart BYWDP, Fitzgerald GP, Burris RH (1967) In situ studies on N2 fixation using the acetylene reduction technique. Proc Natl Acad Sci 58:2071–2078
Subramanian G, Shanmugasundaram S (1986) Influence of the herbicide 2, 4-D on nitrogen fixation and ammonia excretion by the cyanobacterium Anabaena. Proc Indian Natl Sci Acad Part B, Biol Sci 52:308–312
Sun C, Chen S, Jin Y et al (2016) Effects of the herbicide imazethapyr on photosynthesis in PGR5-and NDH-deficient Arabidopsis thaliana at the biochemical, transcriptomic, and proteomic levels. J Agric Food Chem 64:4497–4504
Syiem MB, Singh AK, Rai AN (2017) N2-fixing cyanobacterial systems as biofertilizer. In: Singh J, Seneviratne G (eds) Agro-Environmental Sustainability. Springer, Cham, pp 43–61
Jervekani TM, Karimmojeni H, Razmjoo J (2020) Effects of light-dependent herbicides on growth and physiology of Salvia officinalis. Planta Daninha 38:1–10
Tiwari B, Kharwar S, Tiwari DN (2019) Pesticides and rice agriculture. In: Mishra AK, Tiwari DN, Rai AN (eds) Cyanobacteria, 1st edn. Elsevier, pp 303–325
Vaishampayan A (1984) Biological effects of a herbicide on a nitrogen-fixing cyanobacterium (blue-green alga): an attempt for introducing herbicide-resistance. New Phytol 96:7–11
Vonk JA, Kraak MHS (2020) Herbicide exposure and toxicity to aquatic primary producers. Rev Environ Contam Toxicol Continuation Residue Rev 250:119–171
Win TT, Barone GD, Secundo F, Fu P (2018) Algal biofertilizers and plant growth stimulants for sustainable agriculture. Ind Biotechnol 14:203–211
Wolk CP (1965) Control of sporulation in a blue-green alga. Dev Biol 12:15–35
Yotsova EK, Stefanov MA, Dobrikova AG, Apostolova EL (2017) Different sensitivities of photosystem II in green algae and cyanobacteria to phenylurea and phenol-type herbicides: effect on electron donor side. Z Naturforsch Sect C J Biosci 72:315–324
Zakar T, Laczko-Dobos H, Toth TN, Gombos Z (2016) Carotenoids assist in cyanobacterial photosystem II assembly and function. Front Plant Sci 7:1–7
Zhang Q, Ye Y, Qu Q et al (2021) Enantioselective metabolomic modulations in Arabidopsis thaliana leaf induced by the herbicide dichlorprop. Sci Total Environ 797:149015
Acknowledgements
The authors would like to acknowledge University Grants Commission (UGC), Government of India, New Delhi, for granting fellowship under National Fellowship for higher studies of ST students being implemented by Ministry of Tribal Affairs, Government of India, and under UGC-NET/JRF; Sophisticated Analytical Instrumentation Facility NEHU, Shillong for SEM and TEM.
Funding
This study is funded by UGC, Government of India, New Delhi, under DRS III, vide Letter. F. 4-9/2015/DRS- III (SAP-II) dated 23/04/2015.
Author information
Authors and Affiliations
Contributions
Mayashree B Syiem conceptualized the theme of the manuscript, supervised the experiments, and edited the manuscript. Meguovilie Sachu and Balakyntiewshisha Lyngdoh Kynshi performed the experiments, analyzed the data, and wrote the original draft.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable
Consent for publication
Not applicable
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Robert Duran
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sachu, M., Kynshi, B.L. & Syiem, M.B. A biochemical, physiological and molecular evaluation of how the herbicide 2, 4-dichlorophenoxyacetic acid intercedes photosynthesis and diazotrophy in the cyanobacterium Nostoc muscorum Meg 1. Environ Sci Pollut Res 29, 36684–36698 (2022). https://doi.org/10.1007/s11356-021-18000-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-18000-5