Abstract
Currently, heavy metal-resistant (HMR) marine actinomycetes have attracted much attention worldwide due to their unique capabilities. In this study, 27 marine-derived actinomycetes were isolated from coastal beaches in the Arabian Gulf of Al-Jubail in Saudi Arabia and screened for resistance to 100 mg/L of the heavy metals Cd2+, Cr6+, Cu2+, Fe2+, Pb2+, and Ni2+ using different assay techniques. Six isolates were selected as HMRs, of which two isolates, JJB5 and JJB11, exhibited the highest maximum tolerance concentrations (200– > 300 mg/L). Both isolates were the highest among six-HMR screened for their biodegradation potential of plastics low-density polyethylene, polystyrene, and polyvinyl chloride, recording the highest weight loss (15 ± 1.22 – 65 ± 1.2%) in their thin films. They also showed the highest biodegradability of the pesticides acetamiprid, chlordane, hexachlorocyclohexane, indoxacarb and lindane, indicating promising removal capacities (95.70–100%) for acetamiprid and indoxacarb using HPLC analysis. Additionally, the cell-free filtrate (CFF) of both isolates displayed the highest antimicrobial activity among the six-HMR screened against a variety of microbial test strains, recording the highest inhibition zone diameters (13.76 ± 0.66 – 26.0 ± 1.13 mm). GC‒MS analyses of the ethyl acetate extract of their CFFs revealed the presence of diverse chemical compounds with a multitude of remarkable biological activities. Based on their spore morphology and wall-chemotype, they were assigned to the nocardioform-actinomycetes. Furthermore, their phenotypic characteristics, together with 16S rRNA gene sequencing (OR121525-OR121526), revealed them as Nocardia harenae JJB5 and Amycolatopsis marina JJB11. Our results suggest that marine HMR actinomycetes are promising candidates for various biotechnological applications.
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References
Abdelfattah MS, Elmallah MIY, Hawas UW, Abou El-Kassema LT, Eid MAG (2016) Isolation and characterization of marine-derived actinomycetes with cytotoxic activity from the red sea coast. Asian Pac J Trop Biomed 6:651–657. https://doi.org/10.1016/j.apjtb.2016.06.004
Ait Assou S, Anissi J, Sendide K, El Hassouni M (2023) Diversity and antimicrobial activities of actinobacteria isolated from mining soils in midelt region. Morocco Sci World J 2023:6106673. https://doi.org/10.1155/2023/6106673
Al-Ansari M, Kalaiyarasi M, Almalki MA, Vijayaraghavan P (2020) Optimization of medium components for the production of antimicrobial and anticancer secondary metabolites from streptomyces sp. AS11 isolated from the marine environment. J King Saud Univ - Sci 32:1993–1998. https://doi.org/10.1016/j.jksus.2020.02.005
Albarracín VH, Amoroso MJ, Abate CM (2005) Isolation and characterization of indigenous copper-resistant actinomycete strains. Geochemistry 65:145–156. https://doi.org/10.1016/j.chemer.2005.06.004
Al-Dhabi NA, Mohammed Ghilan AK, Esmail GA, Arasu MV, Duraipandiyan V, Ponmurugan K (2019) Bioactivity assessment of the saudi arabian marine streptomyces sp. Al-Dhabi-90, metabolic profiling and its in vitro inhibitory property against multidrug resistant and extended-spectrum beta-lactamase clinical bacterial pathogens. J Infect Public Health 12:549–556. https://doi.org/10.1016/j.jiph.2019.01.065
Alferova IV, Terekhova LP (1988) Primenenie metoda obogashcheniia pochvy karbonatom kal’tsiia s tsel’iu vydeleniia aktinomitsetov [Use of the method of enriching of soil samples with calcium carbonate for isolation of Actinomyces]. Antibiot Khimioter = Antimicrob Agents Chemother 33:888–890
Almasoud FI, Usman AR, Al-Farraj AS (2015) Heavy metals in the soils of the arabian gulf coast affected by industrial activities: analysis and assessment using enrichment factor and multivariate analysis. Arab J Geosci 8:1691–1703. https://doi.org/10.1007/s12517-014-1298-x
Amin SA, Almahasheer H (2022) Pollution indices of heavy metals in the western arabian gulf coastal area. Egypt J Aquat Res 48:21–27. https://doi.org/10.1016/j.ejar.2021.10.002
Amoroso MJ, Castro GR, Carlino FJ, Romero NC, Hill RT, Oliver G (1998) Screening of heavy metal-tolerant actinomycetes isolated from the sali river. J Gen Appl Microbiol 44:129–132. https://doi.org/10.2323/jgam.44.129
Ashbolt NJ, Amézquita A, Backhaus T, Borriello P, Brandt KK, Collignon P, Coors A, Finley R, Gaze WH, Heberer T et al (2013) Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ Health Perspect 121:993–1001. https://doi.org/10.1289/ehp.1206316
Basu M, Paul M (1999) Chromium-resistant soil actinomycetes: their tolerance to other metals and antibiotics. Acta Microbiol Immunol Hung 46:25–32. https://doi.org/10.1556/amicr.46.1999.1.3
Becker B, Lechevalier MP, Gordon RE, Lechevalier HA (1964) Rapid differentiation between nocardia and streptomyces by paper chromatography of whole-cell hydrolysates. Appl Microbiol 12:421–423. https://doi.org/10.1128/am.12.5.421-423.1964
Benimeli CS, Amoroso MJ, Chaile AP, Castro GR (2003) Isolation of four aquatic streptomycetes strains capable of growth on organochlorine pesticides. Bioresour Technol 89:133–138. https://doi.org/10.1016/s0960-8524(03)00061-0
Benimeli CS, Castro GR, Chaile AP, Amoroso MJ (2006) Lindane removal induction by streptomyces sp. M7. J Basic Microbiol 46:348–357. https://doi.org/10.1002/jobm.200510131
Bian J, Li Y, Wang J, Song FH, Liu M, Dai HQ, Ren B, Gao H, Hu X, Liu ZH et al (2009) Amycolatopsis marina sp. nov., an actinomycete isolated from an ocean sediment. Int J Syst Evol Microbiol 59:477–481. https://doi.org/10.1099/ijs.0.000026-0
Bull AT, Stach JEM (2007) Marine actinobacteria: new opportunities for natural product search and discovery. Trends Microbiol 15:491–499. https://doi.org/10.1016/J.tim.2007.10.004
Chen J, Chen J, Wang S, Bao X, Li S, Wei B, Zhang H, Wang H (2022) Amycolachromones A-F, isolated from a streptomycin-resistant strain of the deep-sea marine actinomycete amycolatopsis sp. WP1. Mar Drugs 20:162. https://doi.org/10.3390/md20030162
Cimermanova M, Pristas P, Piknova M (2021) Biodiversity of actinomycetes from heavy metal contaminated technosols. Microorganisms 9:1635. https://doi.org/10.3390/microorganisms9081635
Colquhoun JA, Mexson J, Goodfellow M et al (1998) Novel rhodococci and other mycolate actinomycetes from the deep sea. Antonie Van Leeuwenhoek, Int J Gen Mol Microbiol 74:27–40. https://doi.org/10.1023/A:1001743625912
Croom KF, Goa KL (2003) Levofloxacin: a review of its use in the treatment of bacterial infections in the united states. Drugs 63:2769–2802. https://doi.org/10.2165/00003495-200363240-00008
Dilika F, Bremner PD, Meyer JJM (2000) Antibacterial activity of linoleic and oleic acids isolated from helichrysum pedunculatum: a plant used during circumcision rites. Fitoterapia 71:450–452. https://doi.org/10.1016/s0367-326x(00)00150-7
Duxbury T (1981) Toxicity of heavy metals to soil bacteria. FEMS Microbiol Lett 11:217–220. https://doi.org/10.1111/j.1574-6968.1981.tb06967.x
El Baz S, Baz M, Barakate M, Hassani L, El Gharmali A, Imziln B (2015) Resistance to and accumulation of heavy metals by actinobacteria isolated from abandoned mining areas. Sci World J 2015:761834. https://doi.org/10.1155/2015/761834
El-Sayed MH, Alshammari FA, Sharaf MH (2023a) Antagonistic potentiality of actinomycete-derived extract with anti-biofilm, antioxidant, and cytotoxic capabilities as a natural combating strategy for multidrug-resistant ESKAPE pathogens. J Microbiol Biotechnol 33:61–74. https://doi.org/10.4014/jmb.2211.11026
El-Sayed MH, Kobisi AA, Elsehemy IA, El-Sakhawy MA (2023b) Rhizospheric-derived nocardiopsis alba BH35 as an effective biocontrol agent actinobacterium with antifungal and plant growth-promoting effects: in vitro studies. J Microbiol Biotechnol 33:607–620. https://doi.org/10.4014/jmb.2301.01001
El-Sorogy AS, Nour H, Essa E, Tawfik M (2013) Quaternary coral reefs of the red sea coast, egypt: diagenetic sequence, isotopes and trace metals contamination. Arab J Geosci 6:4981–4991. https://doi.org/10.1007/s12517-012-0806-0
Fernandes LL, Nayak GN (2012) Geochemical assessment in a creek environment in mumbai, west coast of India. Environ Forensics 13:45–54. https://doi.org/10.1080/15275922.2011.643340
Fetzner S, Lingens F (1994) Bacterial dehalogenases: biochemistry, genetics, and biotechnological applications. Microbiol Rev 58:641. https://doi.org/10.1128/mr.58.4.641-685.1994
Freel KC, Edlund A, Jensen PR (2012) Microdiversity and evidence for high dispersal rates in the marine actinomycete “salinispora pacifica”. Environ Microbiol 14:480–493. https://doi.org/10.1111/j.1462-2920.2011.02641.x
Fuentes MS, Benimeli CS, Cuozzo SA, Amoroso MJ (2010) Isolation of pesticide-degrading actinomycetes from a contaminated site: bacterial growth, removal and dechlorination of organochlorine pesticides. Int Biodeterior Biodegrad 64:434–441. https://doi.org/10.1016/j.ibiod.2010.05.001
Gillard B, Chatzievangelou D, Thomsen L, Ullrich MS (2019) Heavy-metal-resistant microorganisms in deep-sea sediments disturbed by mining activity: an application toward the development of experimental in vitro systems. Front Mar Sci 6:453954. https://doi.org/10.3389/fmars.2019.00462
GoodfellowKämpferBusseTrujilloSuzukiLudwigWhitman MPH-JMEKWWB (2012) Bergey’s manual of systematic bacteriology, volume 5: the actinobacteria, part a. Springer, New York
Goodfellow M, Lechevalier M (1989) Genus nocardia trevisan 1889. In: Holt J, Williams S, Sharpe M (eds) Bergey’s manual of systematic bacteriology, vol 4. Williams & Wilkins, Baltimore, pp 2350–2361
Gozari M, Zaheri A, Jahromi ST, Gozari M, Karimzadeh R (2019) Screening and characterization of marine actinomycetes from the northern oman sea sediments for cytotoxic and antimicrobial activity. Int Microbiol 22:521–530. https://doi.org/10.1007/s10123-019-00083-3
Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47:453–467. https://doi.org/10.1002/jobm.200700275
Han Z, Fina A, Camino G (2014) Chapter 12 - Organosilicon compounds as polymer fire retardants. In: Papaspyrides CD, Pantelis K (eds) Polymer green fame retardants. Elsevier, Amsterdam, pp 389–418. https://doi.org/10.1016/b978-0-444-53808-6.00012-3
Huang Y, Ho SH, Lee HC, Yap YL (2002) Insecticidal properties of eugenol, isoeugenol and methyleugenol and their effects on nutrition of sitophilus zeamais motsch. (coleoptera: curculionidae) and tribolium castaneum (herbst) (coleoptera: tenebrionidae). J Stored Prod Res 38:403–412. https://doi.org/10.1016/s0022-474x(01)00042-x
Hussain M, Aftab K, Iqbal M, Ali S, Rizwan M, Alkahtani S, Abdel-Daim MM (2020) Determination of pesticide residue in brinjal sample using HPTLC and developing a cost-effective method alternative to HPLC. J Chem 2020:8180320. https://doi.org/10.1155/2020/8180320
Jagannathan SV, Manemann EM, Rowe SE, Callender MC, Soto W (2021) Marine actinomycetes, new sources of biotechnological products. Mar Drugs 19:365. https://doi.org/10.3390/md19070365
Janczak K, Hrynkiewicz K, Znajewska Z, Dąbrowska G (2018) Use of rhizosphere microorganisms in the biodegradation of PLA and PET polymers in compost soil. Int Biodeterior Biodegrad 130:65–75. https://doi.org/10.1016/j.ibiod.2018.03.017
Jangir M, Sharma S, Sharma S (2020) Synergistic effect of oilseed cake and biocontrol agent in the suppression of fusarium wilt in solanum lycopersicum. Brazilian J Microbiol 51:1929. https://doi.org/10.1007/s42770-020-00344-8
Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182. https://doi.org/10.1093/bmb/ldg032
Javed MR, Salman M, Tariq A, Tawab A, Zahoor MK, Naheed S, Shahid M, Ijaz A, Ali H (2022) The antibacterial and larvicidal potential of bis-(2-ethylhexyl) phthalate from lactiplantibacillus plantarum. Molecules 27:7220. https://doi.org/10.3390/molecules27217220
Jayabarath J, Musfira SA, Giridhar R, Sundar SS, Arulmurugan R (2010) Biodegradation of carbofuran pesticide by saline soil actinomycetes. Int J Biotechnol Biochem 6:187–193
Kathiresan K (2003) Polythene and plastics-degrading microbes from the mangrove soil. Rev Biol Trop 51:629–633
Kim PS, Shin JH, Jo DS, Shin DW, Choi DH, Kim WJ, Park K, Kim JK, Joo CG, Lee JS et al (2018) Anti-melanogenic activity of schaftoside in rhizoma arisaematis by increasing autophagy in B16F1 cells. Biochem Biophys Res Commun 503:309–315. https://doi.org/10.1016/j.bbrc.2018.06.021
Kupferman A, Leibowitz HM (1975) Therapeutic effectiveness of fluorometholone in inflammatory keratitis. Arch Ophthalmol 93:1011–1014. https://doi.org/10.1001/archopht.1975.01010020793011
Lam KY, Ling APK, Koh RY, Wong YP, Say YH (2016) A review on medicinal properties of orientin. Adv Pharmacol Sci 2016:4104595. https://doi.org/10.1155/2016/4104595
Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematic. John Wiley & Sons, New York, pp 115–175
Lechevalier H (1989) Nocardioform actinomycetes. In: Williams S, Sharpe M, Holt J (eds) Bergey’s manual of systematic bacteriology, vol 4. Williams & Wilkins, Baltimore, pp 2348–2350
Lechevalier M, Prauser H, Ruan D, Labeda J (2012) Genus V. Amycolatopsis. In: Goodfellow M, Kampfer P, Busse HJ, Trujillo ME, Suzuki KLW (eds) Bergey’s manual of systematic bacteriology, volume 5: the actinobacteria, part a, 2nd edn. Springer, New York, pp 1334–1358
Lechevalier MP, Lechevalier H (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 20:435–443. https://doi.org/10.1099/00207713-20-4-435
Lu Z, Zhang C, Han C, An Q, Cheng Y, Chen Y, Meng R, Zhang Y, Su J (2019) Plasticizer bis(2-ethylhexyl) phthalate causes meiosis defects and decreases fertilization ability of mouse oocytes in vivo. J Agric Food Chem 67:3459–3468. https://doi.org/10.1021/acs.jafc.9b00121
Mahmoud HM, Kalendar AA (2016) Coral-associated actinobacteria: diversity, abundance, and biotechnological potentials. Front Microbiol 7:204. https://doi.org/10.3389/fmicb.2016.00204
Martin YE, Johnson EA (2012) Biogeosciences survey: studying interactions of the biosphere with the lithosphere, hydrosphere and atmosphere. Prog Phys Geogr 36:833–852. https://doi.org/10.1177/0309133312457107
Masindi V, Muedi KL (2018) Environmental contamination by heavy metals. In: Saleh HE, Aglan RF (eds) Heavy metals. IntechOpen, Rijeka, pp 115–113. https://doi.org/10.5772/intechopen.76082
Miller DN, Bryant JE, Madsen EL, Ghiorse WC (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol 65:4715–4724. https://doi.org/10.1128/aem.65.11.4715-4724.1999
Mohamed H, Hassane A, Rawway M et al (2021) Antibacterial and cytotoxic potency of thermophilic streptomyces werraensis MI-S.24-3 isolated from an egyptian extreme environment. Arch Microbiol 203:4961–4972. https://doi.org/10.1007/s00203-021-02487-0
Mondal H, Thomas J (2022) Isolation and characterization of a novel actinomycete isolated from marine sediments and its antibacterial activity against fish pathogens. Antibiotics 11:1546. https://doi.org/10.3390/antibiotics11111546
Nakei MD, Misinzo G, Tindwa H, Semu E (2022) Degradation of polyethylene plastic bags and bottles using microorganisms isolated from soils of morogoro. Tanzania Front Microbiol 13:1077588. https://doi.org/10.3389/fmicb.2022.1077588
NCCLS 2003 Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically Sixth Edition Document M7-A6 Wayne 60
Niño J, Espinal CM, Mosquera OM, Correa YM (2003) Antimycotic activity of 20 plants from colombian flora. Pharm Biol 41:491–496. https://doi.org/10.1080/13880200308951341
Nunes M, Leston S (2020) Coastal pollution: an overview. In: Leal Filho W, Azul AM, Brandli L, Lange Salvia A, Wall T (eds) Life below water. Encyclopedia of the UN sustainable development goals. Springer, Cham, pp 1–11. https://doi.org/10.1007/978-3-319-71064-8_9-1
Oliveira J, Almeida PL, Sobral RG, Lourenço ND, Gaudêncio SP (2022) Marine-derived actinomycetes: biodegradation of plastics and formation of PHA bioplastics—a circular bioeconomy approach. Mar Drugs 20:760. https://doi.org/10.3390/md20120760
Pazirandeh M, Wells BM, Ryan RL (1998) Development of bacterium-based heavy metal biosorbents: enhanced uptake of cadmium and mercury by escherichia coli expressing a metal binding motif. Appl Environ Microbiol 64:4068. https://doi.org/10.1128/aem.64.10.4068-4072.1998
Phillips TM, Seech AG, Lee H, Trevors JT (2001) Colorimetric assay for lindane dechlorination by bacteria. J Microbiol Methods 47:181–188. https://doi.org/10.1016/s0167-7012(01)00299-8
Rahman Z, Singh VP (2019) The relative impact of toxic heavy metals (THMs) (arsenic (As), cadmium (Cd), chromium (Cr)(VI), mercury (Hg), and lead (Pb)) on the total environment: an overview. Environ Monit Assess 191:419. https://doi.org/10.1007/s10661-019-7528-7
Rajivgandhi G, Gnanamangai BM, Ramachandran G, Chackaravarthy G, Chelliah CK, Maruthupandy M, Alharbi NS, Kadaikunnan S, Li WJ (2022) Effective removal of heavy metals in industrial wastewater with novel bioactive catalyst enabling hybrid approach. Environ Res 204:112337. https://doi.org/10.1016/j.envres.2021.112337
Rajivgandhi G, Vimala RTV, Maruthupandy M, Alharbi NS, Kadaikunnan S, Khaled JM, Manoharan N, Li WJ (2021) Enlightening the characteristics of bioflocculant of endophytic actinomycetes from marine algae and its biosorption of heavy metal removal. Environ Res 200:111708. https://doi.org/10.1016/j.envres.2021.111708
Rashad FM, Fathy HM, El-Zayat AS, Elghonaimy AM (2015) Isolation and characterization of multifunctional streptomyces species with antimicrobial, nematicidal and phytohormone activities from marine environments in egypt. Microbiol Res 175:34–47. https://doi.org/10.1016/j.micres.2015.03.002
Sajayan A, Ravindran A, Selvin J, Ragothaman P, Seghal Kiran G (2023) An antimicrobial metabolite n- hexadecenoic acid from marine sponge-associated bacteria bacillus subtilis effectively inhibited biofilm forming multidrug-resistant P. aeruginosa. Biofouling 39:502–515. https://doi.org/10.1080/08927014.2023.2232722
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467. https://doi.org/10.1073/pnas.74.12.5463
Sarkar G, Suthindhiran K (2022) Diversity and biotechnological potential of marine actinomycetes from india. Indian J Microbiol 62:475–493. https://doi.org/10.1007/S12088-022-01024-X
Shady NH, Tawfike AF, Yahia R, Fouad MA, Brachmann AO, Piel J, Abdelmohsen UR, Kamel MS (2022) Cytotoxic activity of actinomycetes nocardia sp. and nocardiopsis sp. associated with marine sponge Amphimedon sp. Nat Prod Res 36:2917–2922. https://doi.org/10.1080/14786419.2021.1931865
Shirling EB, Gottlieb D (1966) Methods for characterization of streptomyces species. Int J Syst Bacteriol 16:313–340. https://doi.org/10.1099/00207713-16-3-313
Singh LS, Sharma H, Talukdar NC (2014) Production of potent antimicrobial agent by actinomycete, streptomyces sannanensis strain SU118 isolated from phoomdi in loktak lake of manipur. India BMC Microbiol 14:278. https://doi.org/10.1186/s12866-014-0278-3
Sivan A, Szanto M, Pavlov V (2006) Biofilm development of the polyethylene-degrading bacterium rhodococcus ruber. Appl Microbiol Biotechnol 72:346–352. https://doi.org/10.1007/S00253-005-0259-4
Sparks D (1996) Methods of soil analysis part 3: chemical methods. Soil Science Society of America, American Society of Agronomy, Madison
Supreeth M, Chandrashekar MA, Sachin N, Raju NS (2016) Effect of chlorpyrifos on soil microbial diversity and its biotransformation by streptomyces sp. HP-11. 3 Biotech 6:147. https://doi.org/10.1007/S13205-016-0462-2
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
Terahara T, Xu X, Kobayashi T, Imada C (2015) Isolation and characterization of Cr(VI)-reducing actinomycetes from estuarine sediments. Appl Biochem Biotechnol 175:3297–3309. https://doi.org/10.1007/s12010-015-1501-x
Thirumurugan D, Cholarajan A, Raja S, Vijayakuma R (2018) An introductory chapter: secondary metabolites - an overview. In: Vijayakumar R, Raja S (eds) Secondary metabolites. IntechOpen, Rijeka, pp 1–8. https://doi.org/10.5772/IntechOpen.79766
Timková I, Sedláková-Kaduková J, Pristaš P (2018) Biosorption and bioaccumulation abilities of actinomycetes/streptomycetes isolated from metal contaminated sites. Separations 5:54. https://doi.org/10.3390/separations5040054
Tresner HD, Davies MC, Backus EJ (1961) Electron microscopy of streptomyces spore morphology and its role in species differentiation. J Bacteriol 81:70–80. https://doi.org/10.1128/jb.81.1.70-80.1961
Uchida H, Nakajima-Kambe T, Shigeno-Akutsu Y, Nomura N, Tokiwa Y, Nakahara T (2000) Properties of a bacterium which degrades solid poly(tetramethylene succinate)-co-adipate, a biodegradable plastic. FEMS Microbiol Lett 189:25–29. https://doi.org/10.1111/J.1574-6968.2000.tb09201.x
Undabarrena A, Ugalde JA, Seeger M, Cámara B (2017) Genomic data mining of the marine actinobacteria streptomyces sp. H-KF8 unveils insights into multistress related genes and metabolic pathways involved in antimicrobial synthesis. Peer J 2017:2912. https://doi.org/10.7717/peerj.2912
Valgas C, De Souza SM, Smânia EFA, Smânia A (2007) Screening methods to determine antibacterial activity of natural products. Brazilian J Microbiol 38:369–380. https://doi.org/10.1590/S1517-83822007000200034
Venkatramanan S, Ramkumar T, Anithamary I, Vasudevan S (2014) Heavy metal distribution in surface sediments of the tirumalairajan river estuary and the surrounding coastal area, east coast of india. Arab J Geosci 7:123–130. https://doi.org/10.1007/s12517-012-0734-z
Wang L, Zheng M, Xu H, Hua Y, Liu A, Li Y, Fang L, Chen X (2022) Fate and ecological risks of current-use pesticides in seawater and sediment of the yellow sea and east china sea. Environ Res 207:112673. https://doi.org/10.1016/J.envres.2021.112673
Watanabe E, Kobara Y, Baba K, Eun H (2014) Aqueous acetonitrile extraction for pesticide residue analysis in agricultural products with HPLC-DAD. Food Chem 154:7–12. https://doi.org/10.1016/J.foodchem.2013.12.075
Williams ST, Goodfellow M, Alderson G, et al (1983) Numerical classification of Streptomyces and related genera. J Gen Microbiol 129:1743–1813. https://doi.org/10.1099/00221287-129-6-1743
Williams S, Sharpe M, Holt J (1989) Bergey’s manual of systematic bacteriology, vol 4. Williams & Wilkins, Baltimore
Wright L, Katouli M, Kurtböke Dİ (2021) Isolation and characterization of nocardiae associated with foaming coastal marine waters. Pathogens 10:579. https://doi.org/10.3390/pathogens10050579/S1
Yi J, Lo LSH, Liu H, Qian PY, Cheng J (2021) Study of heavy metals and microbial communities in contaminated sediments along an urban estuary. Front Mar Sci 8:741912. https://doi.org/10.3389/fmars.2021.741912
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El-Sayed, M.H., Abdellatif, M.M., Mostafa, H.M. et al. Biodegradation and antimicrobial capability-induced heavy metal resistance of the marine-derived actinomycetes Nocardia harenae JJB5 and Amycolatopsis marina JJB11. World J Microbiol Biotechnol 40, 202 (2024). https://doi.org/10.1007/s11274-024-04006-x
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DOI: https://doi.org/10.1007/s11274-024-04006-x