Effect of herbicides on cellular growth, microbiological and physiological activities of an identified rhizosphere isolate Rhodococcus erythropolis

ABSTRACTConsidering the excessive pesticide pollution in the environment, atrazine (ATZ), butachlor (BCR) and quizalofop-p-ethyl (QUIZ) were selected to assess their toxic effect on Rhodococcus erythropolis PSB-6 (NCBI Accession No. MG028649). MIC values of ATZ, BCR and QUIZ to R. erythropolis were determined to be 100, 200 and 150 μM, respectively. Biomarker enzymatic assays including LPO, LDH and oxidative stress (CAT) induced by herbicides represented significant (p ≤ 0.005) toxicity towards strain PSB-6. Herbicide-induced morphological changes viz. aberrant margins; cellular cracking and distortion/damage in R. erythropolis cells were apparent under SEM observation. Furthermore, herbicide-treated and DAPI (4’,6-diamidino-2-phenylindole)-stained cells showed concentration-dependent reduction in cellular permeability as revealed under CLSM. Furthermore, herbicides displayed toxicity towards bioactive molecules of PSB-6 in a dose-related manner. Among them, ATZ imparted maximum negative effect, where it reduced the bacterial production of IAA, ACC deaminase and 2, 3-DHBA by 68% (p ≤ 0.001), 75% (p ≤ 0.001), and 83% (p ≤ 0.005), respectively, over control. Additionally, following herbicide exposure, bacterial counts (log10 CFU mL−1) were reduced. Higher concentrations of ATZ and BCR completely reduced the growth patten of strain PSB-6. The current investigation provides an insight into a mechanistic approach of chemical herbicide-induced hazard toward a beneficial soil isolate. Careful monitoring is therefore necessary before agricultural application of pesticides.KEYWORDS: Pesticides stressRhodococcus erythropolisEnzymatic profileBacterial activityCellular viabilityActive biomolecules AcknowledgementsThe authors extend their appreciation to the Researchers Supporting Project number (RSP2023R367), King Saud University, Saudi Arabia.Disclosure statementNo potential conflict of interest was reported by the author(s).Author contributionsConceptualisation, M.S. and M.S.K,; methodology, M.S.; software, M.S., A.S.; validation, M.S., M.S.K and A.S; formal analysis, M.S and M.S.K., and A.M.E.; investigation, M.S. and M.S.K; resources, M.S., M.S.K., A.S and A.M.E.; data curation, M.S.; writing – original draft preparation, M.S., and M.S.K; writing – review and editing, M.S., J.P., and M.S.K.; visualisation, M.S.K., and J.P.; supervision, M.S.K.; project administration, M.S. and M.S.K; funding acquisition, A.S., A.M.E., and L.S.W. All authors have read and agreed to the published version of the manuscript.Additional informationFundingThis research was funded by the Researchers Supporting Project number [RSP2023R367], King Saud University, Saudi Arabia.Notes on contributorsMohammad ShahidMohammad Shahid is a postdoctoral fellow at ICAR-National Bureau of Agriculturally Important Microorganisms (NBAIM), Mau, U.P, India. He obtained his PhD (Agricultural Microbiology) from Aligarh Muslim University, Aligarh, India. He has published a large number of papers including research and review on microbiology, plant-microbe interaction, rhizosphere biology and pesticide toxicology in various reputed journals. He has attended several national and international conferences, seminars, and workshops. He is reviewer of several national and international journals.Mohammad Saghir KhanMohammad Saghir Khan is a full Professor at the Department of Agricultural Microbiology, Aligarh Muslim University, Aligarh, India. Dr. Khan received his Ph.D. (Microbiology) degree from Govind Ballabh Pant University of Agriculture & Technology, Pant Nagar, India. He has been teaching Microbiology to post-graduate students for the last 25 years and has research experience of 29 years. In addition to his teaching, Dr. Khan is engaged in guiding students for their doctoral degree in Microbiology and has successfully supervised 12 research scholars for Ph.D. degree in Agricultural Microbiology while five research scholars are working under his supervision. He has published over 200 scientific papers with a total citation of 17484 (google citation; h- index 55; i10 index 240) including, original research articles, review articles and book chapters in various national and international publication media. Some of the notable journals in which Dr. Khan has published his work include International Journal of Nanomedicines, Chemosphere, Ecotoxicology, Environmental Pollution, Environmental Chemistry letters, Scientific Reports, Current Microbiology, Microbiological Research, Crop Protection, Pesticide Biochemistry & Physiology, ACS Omega, Food and Chemical Toxicology, European Journal of Agronomy, Archives of Environmental Contamination & Toxicology etc. Dr. Khan has edited eleven books published by the leading international publishers. Of these books, a total of 176535 book chapters have been downloaded worldwide. Dr. Khan has also completed research projects funded by UGC and ICAR. His major research area includes Ecotoxicology, Nanotoxicology, Bioremediation, Environmental Microbiology, Rhizobiology and Immunology. Dr. Khan has also served in different administrative capacities in the university.Asad SyedAsad Syed is an Associate Professor at Botany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi Arabia. He has been awarded Doctorate from the University of Pune, whereas he has completed his research work from CSIR-National Chemical Laboratory, Pune, India, where he served as Research Associate and Senior Research Fellow in the Biochemical Sciences Division. His research interest is in fabrication of nanomaterials, by utilizing fungi, bacteria, plant extracts, protein, etc. Another area of his expertise is secondary metabolite from endophytic fungi. Now he ventured into the potential application of nanomaterials in environment and healthcare. He is serving as reviewer for international peer journals that include materials science and microbiology journals. He is teaching basic microbiology and laboratory skills to bachelor's students and involved in mentoring master's and PhD students at Botany and Microbiology Department, KSU, Riyadh. He has published his findings in international peer-reviewed materials science and microbiology journals.Abdallah M. ElgorbanAbdallah M. Elgorban is an Associate Professor at Centre of Excellence in Biotechnology Research (CEBR), King Saud University, Riyadh, Saudi Arabia from March 2009 till date, with 24 years of research and academic experience. He has published 320 international research papers in peer reviewed international journal, with high impact factors such as 24.3 (Fungal Diversity, Top%1), and also having good impact on Publon as 28 h-index and 4500 citations for published papers. His research interest falls in the areas as Nanotechnology, Microbiology, Biotechnology and Molecular Biology. He has an experience and keen interest to learn and explore varied techniques from biotechnology and nanotechnology.John PichtelJohn Pichtel PhD, CHMM, is a professor in Environment, Geology, and Natural Resources, Ball State University, Muncie, IN 47306, US. Prof. Pichtel received his Ph. D in Agronomy/ Environmental Science from the Ohio State University, Columbus, OH in 1987. He did his programme in Agronomy/Soil Chemistry from the Ohio State University, Columbus, OH in 1983. He completed his BS degree in Natural Resource Management from Rutgers University, New Brunswick, NJ. 1980. His research embraces management of hazardous materials, remediation of contaminated sites, and environmental chemistry. His research group is studying the behaviour of metallic nanoparticles in soil and aquatic environments. He is particularly interested in assessing shifts in microbial communities and changes in plant physiological processes as a result of interaction with nanoparticles. They have evaluated soil chemical properties and plant response during restoration of brownfields and Superfund sites in the United States as well as highly contaminated environs in the United Kingdom, Ireland, Finland, and Thailand. Other research involves investigation of microbially-catalysed decomposition of PCBs, explosives, propellants, and other xenobiotics.Ling Shing WongLing Shing Wong is graduated from The National University of Malaysia (UKM), Bangi, Selangor, Malaysia in 2010 with Ph.D. in Environmental Science, specialized in the development of biosensor for environmental toxicity assessment. He is currently a professor in INTI International University, Nilai, Negeri Sembilan, Malaysia. His research interests include development of biosensor for environmental application, discovery of new reporter groups for bioindicator, as well as algae and cyanobacteria culture technology. He has authored and co-authored more than 130 scientific articles and extends his service as editorial member in many international journals. Dr. Wong is a senior member of Asia-Pacific Chemical, Biological & Environmental Engineering Society (APCBEES) and the Institute of Research Engineers & Doctors (theIRED), Member of Persatuan Sains Analisis Malaysia and Persatuan Pembangunan Sensor Malaysia. He won several innovation awards including a bronze medal from Malaysia Technology Expo (MTE), Kuala Lumpur, Malaysia in 2006, a gold medal from International Invention, Innovation & Technology Exhibition (ITEX), Kuala Lumpur, Malaysia in 2008, a gold medal from Product Design Competition (PRODEC) in 2013, a silver medal from International Innovation Festival (Innofest) in 2014, finalist of National Outstanding Innovator Award in 2015, a silver medal from Private Higher Education Invention and Innovation Contest (PERINTIS) in 2016, a silver medal from International Invention & Innovation Competition in 2017, two bronze medal from International Invention, Innovation and Design Expo (INNODEX) in 2021, and a silver medal from Malaysia Technology Expo (MTE) in 2021.