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Properties of Streptomyces Bacteria from the Rhizosphere of Some Halophytes at North-East of Qatar: Al Ghariya Case Study

The biological activities performed by plants and microorganisms in dry and saline soil play an important role in making them thrive in these extreme environmental conditions. Our previous studies have shown the presence of Streptomyces bacteria in various drylands in Qatar. To understand and elucidate the roles of these bacteria in such unfavorable environments, it is important to investigate the distribution and properties of Streptomyces bacteria in rhizospheric soil of halophytes and compare them with non-rhizospheric soils. Therefore, in this research, four halophyte plants namely: Caroxylon imbricatum, Sporobolus ioclados, Tamarix aphylla, and Tetraena qatarensis, were chosen to investigate the properties, characteristics, and activities of Streptomyces isolates in these habitats. The chemical and physical properties of soil at the study area (Al Ghariya Sabkha) revealed that pH levels are almost uniform and homogenous across the Sabkha; ranging between 7.7-7.9, and salinity levels were very high at non-rhizospheric soil as compared to the rhizospheric soils, thus, all elements at the rhizospheres of the studied plants have lower concentrations than those at the non-rhizospheric soils. The colony characteristics of isolates at the rhizospheric soil of halophytes showed various types of isolates with different colony characteristics and peculiarities which indicate that a significant number of strains of Streptomyces bacteria have thrived under such mini-habitats of the canopy of these plants. The enzyme activities of the isolates that have been studied in the rhizospheric and non-rhizospheric soils have shown more variable isolates in the rhizosphere of the plants under investigation than those of non-rhizospheric soils. The antibacterial primary activity of the isolates of Streptomyces at these mini-habitats showed that most of them had clear antibacterial action against the tested strains: Gram-negative (E. coli), and Gram-positive (B. subtilis, S. aureus, and S. epidermidis). The details about these parameters and the possible use of modern approaches to identifying Streptomyces bacteria, and the possible roles of halophytes and their associated microbes in saline lands are also discussed in this paper. Overall, the results of this research showed that the properties and characteristics of Streptomyces bacteria explaining their biodiversity were high in rhizospheric soils of halophytes as compared to non-rhizospheric soils.

Antibacterial Activity, Biochemical Characteristics, Colony Features, Elements, Halophytes, Streptomyces

APA Style

Fahad Al-Thani, R., Al-Mohannadi, A., Deyab, D., Abdulla Al-Yafei, F., Yousaf Ashfaq, M., et al. (2023). Properties of Streptomyces Bacteria from the Rhizosphere of Some Halophytes at North-East of Qatar: Al Ghariya Case Study. Frontiers in Environmental Microbiology, 9(3), 34-51. https://doi.org/10.11648/j.fem.20230903.11

ACS Style

Fahad Al-Thani, R.; Al-Mohannadi, A.; Deyab, D.; Abdulla Al-Yafei, F.; Yousaf Ashfaq, M., et al. Properties of Streptomyces Bacteria from the Rhizosphere of Some Halophytes at North-East of Qatar: Al Ghariya Case Study. Front. Environ. Microbiol. 2023, 9(3), 34-51. doi: 10.11648/j.fem.20230903.11

AMA Style

Fahad Al-Thani R, Al-Mohannadi A, Deyab D, Abdulla Al-Yafei F, Yousaf Ashfaq M, et al. Properties of Streptomyces Bacteria from the Rhizosphere of Some Halophytes at North-East of Qatar: Al Ghariya Case Study. Front Environ Microbiol. 2023;9(3):34-51. doi: 10.11648/j.fem.20230903.11

Copyright © 2023 Authors retain the copyright of this article.
This article is an open access article distributed under the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

1. E. Montesinos, “Plant-associated microorganisms: a view from the scope of microbiology, “International Microbiology, vol. 6, pp. 221–223. doi 10.1007/s10123-003-0141-0, 2003.
2. C. J. Dong, L. L. Wang, Q. Li, and Q. M. “Shang, Bacterial communities in the rhizosphere, phyllosphere and endosphere of tomato plants,” PLoS One, vol. 14 (11), e0223847. doi: 10.1371/journal.pone.0223847, 2019.
3. L. L. Barton, and D. E. Northup, “Microbial Ecology,” Wiley-Blackwell, Oxford, UK, ISBN: 978118015841, http://onlinelibrary.wiley.com/book/1, 2011.
4. B. T. Yasseen, and R. F. Al-Thani, “Ecophysiology of Wild Plants and Conservation Perspectives in the Stat of Qatar“Chapter 3, Agricultural Chemistry, M Stoytcheva, M. and Zlatev, R. (Eds.), pp. 37-70. ISBN: 978-953-51-1026-2, InTech, doi: 10.5772/55305, 2013.
5. B. T. Yasseen, and R. F. Al-Thani, “ Wild Plants in the Qatari Peninsula are Hidden Gene Bank for Future Research: Perspectives of Desirable Traits, “Chapter 6. B P International, pp. 207-252. doi: 10.9734/bpi/cerb/v8/6473A, 2023.
6. R. F. Al-Thani, and B. T. Yasseen, “Solutes in native plants in the Arabian Gulf region and the role of microorganisms: Future research, “J. Plant Ecology, vol. 11 (5), pp. 671-684. https://doi.org/10.1093/jpe/rtx066, 2018.
7. R. F. Al-Thani, and B. T. Yasseen, “Biological soil crusts and extremophiles adjacent to native plants at Sabkhas and Rawdahs, Qatar: The possible roles,“Frontiers in Environmental Microbiology, vol. 4 (2), pp. 55-70. doi: 10.11648/j.fem.20180402.13, 2018.
8. R. F. Al-Thani, and B. T. Yasseen, “Perspectives of future water sources in Qatar by phytoremediation: Biodiversity at ponds and modern approach,”International Journal of Phytoremediation, vol. 23 (8), pp. 866-889. doi: 10.1080/15226514.2020.1859986, 2021.
9. R. F. Al-Thani, and B. T. Yasseen, “Microbial ecology of Qatar, the Arabian Gulf: Possible roles of microorganisms,” Front. Mar. Sci., voil. 8, 697269. doi: 10.3389/fmars.2021.697269, 2021.
10. N. A. Koza, A. A. Adedayo, O. O. Babalola, and A. P. Kappo,” Microorganisms in plant growth and development: Roles in abiotic stress tolerance and secondary metabolites secretion, “Microorganisms, vol. 10 (8), pp. 1528. doi: 10.3390/microorganisms10081528, 2022.
11. N. Barros, and S. Feijóo,”A combined mass and energy balance to provide bioindicators of soil microbiological quality,” Biophys. Chem., vol. 104, pp. 561–72, 2003.
12. S. Afrasayab, M. Faisal, S. Hasnain, “Comparative study of wild and transformed salt tolerant bacterial strains on Triticum aestivum growth under salt stress,” Braz. J. Microbiol, vol. 41, pp. 946–55, 2010.
13. C. Gougoulias, J. M. Clark, L. J. Shaw,” The role of soil microbes in the global carbon cycle: tracking the below-ground microbial processing of plant-derived carbon for manipulating carbon dynamics in agricultural systems,” J. Sci. Food Agric., vol. 94, pp. 2362–2371, 2014.
14. P. Shrivastava, and R. Kumar, “Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation,” Saudi J. Biol. Sci., vol. 22, pp. 123–131, 2015.
15. J. I. Vílchez, C. García-Fontana, D. Román-Naranjo, J. Gonzalez-Lopez, and M. Manzanera,” Plant drought tolerance enhancement by trehalose production of desiccation-tolerant microorganisms,” Front. Microbiol., vol. 7, 1577. https://doi.org/10.3389/fmicb.2016.01577, 2016.
16. B. T. Yasseen, and R. F. Al-Thani, “Endophytes and halophytes to remediate industrial wastewater and saline soils: Perspectives from Qatar, “PLANTS, vol. 11 (11), 1497. https:// doi.org/10.3390/plants1111149, 2022.
17. M. Nikolaidis, A. Hesketh, N. Frangou, D. Mossialos, Y. Van de Peer, S. G. Oliver, G. D. Amoutzias,” A panoramic view of the genomic landscape of the genus Streptomyces,” Microbial Genomics, vol. 9, 001028. doi: 10.1099/mgen.0.001028, 2023.
18. R. F. Al-Thani, and I. A. K. Mahasneh, “Ecology and Distribution of Streptomyces in the Soil of Qatar,” Legal deposit No.- at qul 212/ 2004. Doha: Environmental Studies Centre (ESC), Qatar University, 69, 2002.
19. R. F. Al-Thani, and B. T. Yasseen, “Halo-thermophilic bacteria and heterocyst cyanobacteria found adjacent to halophytes at Sabkhas – Qatar: Preliminary study and possible roles,” African Journal of Microbiology Research, vol. 11 (34), pp. 1346-1354, 2017.
20. E. M. Abdel-Bari, “The Flora of Qatar, The Dicotyledons, The Monocotyledons, “Vol. 1, 2, Environmental Studies Centre, Qatar University, Doha, Qatar, 2012.
21. S. A. Ghazanfar, B. Böer, A. W. Al Khulaidi, A. El-Keblawy, and S. Alateeqi, “Plants of Sabkha ecosystems of the Arabian Peninsula,” In: Sabkha Ecosystems, Tasks for Vegetation Science VI, Gul, B., Böer, B., Ajmal Khan, M., Clüsener-Godt, M., and Hameed, A. (Eds.). Springer Nature, Switzerland AG 2019 55. https://doi.org/10.1007/978-3-030-04417-6_5, 2019.
22. A. Bhatt, N. R. Bhat, M. K. Suleiman, and H. Al-Mansour, “Prioritization of potential native plants from Arabian Peninsula based on economic and ecological values: Implication for restoration,”Sustainability, vol. 15, 6139. https://doi.org/10.3390/su150761339, 2023.
23. G. M. Fahmy, and R. F. Al-Thani, “Ecology of Halophytes and their bacterial inhabitants in the coastal salt marsh of Al-Dhakhira, Qatar,” Environmental Studies Centre (ESC), University of Qatar, Doha, Qatar, 2006.
24. B. R. Glick, “Bacteria with ACC deaminase can promote plant growth and help to feed the world,” Microbiol. Res., vol. 169, pp. 30–9 B. R. doi: 10.1016/j.micres.2013.09.009, 2014.
25. M. Hanin, C. Ebel, M. Ngom, L. Laplaze, K. Masmoiudi, “New insights on plant salt tolerance mechanisms and their potential use for breeding,” Front. Plant Sci., vol. 7, 1787. https://doi.org/10.3389/fpls.2016.01787, 2016.
26. S. Zewdu, K. V. Suryabhagavan, and M. Balakrishnan,” Geo-spatial approach for soil salinity mapping in Sego Irrigation Farm, South Ethiopia,” J. Saudi Soc Agric. Sci., vol. 16 (1), pp. 16–24. doi: 10.1016/j.jssas.2014.12.003, 2017.
27. A. Ali, D. Guo, A. Mahar, F. Ma, R. Li, F. Shen, P. Wang, and Z. Zhang,”Streptomyces pactum assisted phytoremediation in Zn/Pb smelter contaminated soil of Feng County and its impact on enzymatic activities,” Sci. Rep., vol. 7, 46087. https://doi.org/10.1038/srep46087, 2017.
28. O. Y. A. Costa, J. M. Raaijmakers, and E. E. Kuramae,”Microbial extracellular polymeric substances: Ecological function and impact on soil aggregation,” Front. Microbiol., vol. 9, 1636. doi: 10.3389/fmicb.2018.01636, 2018.
29. H. Baoune, J. D. Aparicio, A. Acuña, A. O. El Hadj-khelil, L. Sanchez, M. A. Polti, and A. Alvarez,” Effectiveness of the Zea mays-Streptomyces association for the phytoremediation of petroleum hydrocarbons impacted soils,” Ecotoxicology and Environmental Safety, vol. 184, 109591. https://doi.org/10.1016/j.ecoenv.2019.109591, 2019.
30. O. S. Olanrewaju, and O. O. Babalola, “Streptomyces: implications and interactions in plant growth promotion,” Appl. Microbiol. Biotechnol., vol. 103 (3), pp. 1179–1188. doi: 10.1007/s00253-018-09577-y, 2019.
31. N. Romano-Armada, M. F. Yañez-Yazlle, V. P. Irazusta, V. B. Rajal, and N. B. Moraga,” Potential of bioremediation and PGP traits in Streptomyces as strategies for bio-reclamation of salt-affected soils for agriculture,” Pathogens, vol. 9 (2), 117. https://doi.org/10.3390/pathogens9020117, 2020.
32. S. F. Worsley, J. Newitt, J. Rassbach, S. F. D. Batey, N. A. Holmes, J. C. Murrell, B. Wilkinson, and M. I. Hutchings,” Streptomyces endophytes promote host health and enhance growth across plant species,” Appl. Environ. Microbiol., vol. 86 (16). e01053-20. doi: 10.1128/AEM.01053-20, 2020.
33. W. Chemoh, W. Bin-Ismail, and S. Dueramae,” Antagonistic potential of soil Streptomyces isolates from Southern Thailand to inhibit foodborne bacterial pathogens,” Int. J. Microbiol., vol. 30, 2545441. doi: 10.1155/2021/2545441, 2021.
34. N. Nonthakaew, W. Panbangred, W. Songnuan, and B. Intra, ”Plant growth-promoting properties of Streptomyces spp. isolates and their impact on mung bean plantlets’ rhizosphere microbiome,” Front. Microbiol., vol. 13, 967415. doi: 10.3389/fmicb.2022.967415, 2022.
35. F. Pang, M. K. Solanki, and Z. Wang, “Streptomyces can be an excellent plant growth manager,” World Journal of Microbiology and Biotechnology, vol. 38 (11). doi: 10.1007/s11274-022-03380-8, 2022.
36. K. Alam, A. Mazumder, S. Sikdar, Y-M. Zhao, J. Hao, C. Song, Y. Wang, R. Sarkar, S. Islam, Y. Zhang, and A. Li, “Streptomyces: The biofactory of secondary metabolites,” Front. Microbiol., vol.13, 968053. doi: 10.3389/fmicb.2022.968053, 2022.
37. M. M. Ashore,” Sabkhas in the peninsula of Qatar - geomorphologic and geological and biological studies,” University of Qatar, Doha, Qatar, Centre of Documentation and Humanitarian Studies, 1991.
38. B. Dahal, G. NandaKafle, L. Perkins, and V. S. Brözel,”Diversity of free-living nitrogen fixing Streptomyces in soils of the badlands of South Dakota,” Microbiol. Res., vol. 195, pp. 31-39. doi: 10.1016/j.micres.2016.11.004, 2017.
39. W. Alsharif, M. M. Saad, and H. Hirt,”Desert microbes for boosting sustainable agriculture in extreme environments,” Frontiers in Microbiology, vol. 11, 1666. doi: 10.3389/fmicb.2020.01666, 2020.
40. R. F. Al-Thani, B. T. Yasseen, and P. Balakrishnan, “Soil properties in the north-east of Qatar attract halophytes and microorganisms for potential phytoremediation: Al Ghariya case study,” Int. J. Phytoremediat., (Under publication), 2023.
41. H. A. Abulfatih, E. M. Abdel-Bari, A. Alsubaey, Y. M. Ibrahim, “Vegetation of Qatar,” Scientific and Applied Research Center (SARC), University of Qatar, Doha, Qatar, 2001.
42. J. Norton, S. Abdul Majid, D. Allan, M. Al Safran, B. Böer, and R. Richer, “An illustrated checklist of the flora of Qatar,” United Nations Educational, Scientific and Cultural Organization, UNESCO Office in Doha, Qatar Foundation, MAERSK OIL QATAR AS. Doha, Qatar, 2009.
43. E. M. Abdel-Bari, B. T. Yasseen, and R. F. Al-Thani, “Halophytes in the State of Qatar,” Environmental Studies Center, University of Qatar, Doha, Qatar, ISBN.99921-52-98-2, 2007.
44. A. Elnaggar, A. El-Keblawy, K. A. Mosa, and S. Soliman, “Drought tolerance during germination depends on light and temperature of incubation in Salsola imbricata, a desert shrub of Arabian deserts,” Flora, vol. 249, pp. 156-163, 2018.
45. S. Afsar, L. Aziz, M. Qasim, A. H. Baloch, M. S. Noman, and S. Gulzar, “Salt tolerance of a leaf succulent halophyte Salsola imbricata Forssk–Growth and water relations perspective,” Int. J. Biol. Biotechnol., vol. 18, pp. 499-507, 2021.
46. Z. Hanif, H. H. Ali, G. Rasool, A. Tanveer, and B. S. Chauhan, “Genus Salsola: its benefits, uses, environmental perspectives and future aspects-a review,” Journal of Rangeland Science, vol. 8 (3), pp. 315-328, 2018.
47. K. H. Batanouny, “Ecology and flora of Qatar,” Centre for Scientific and Applied Research, University of Qatar, Qatar, 1981.
48. K. H. Batanouny, and A. A. Turki, “Vegetation of south-western Qatar, “Arab Gulf J. Scient. Res., vol. 1 (1), pp. 5–19, 1983.
49. N. K. Mishra, and A. Sangwan, “Phytoremediation of salt-affected soils: A review of processes, applicability, and the impact on soil health in hisar, Haryana,” Int. J. Eng. Sci. Inven. Res. Develop. II, 2349e6185, www.ijesird.com.e., 2016.
50. C. J. De Loach, “Tamarix aphylla,” Crop protection compendium database CAB International, pp. 505-513, 2004.
51. T. M. Jasiem, N. M. Nasser, and H. K. Al-Bazaz, “Tamarix aphylla L.: A review,” Research Journal of Pharmacy and Technology, vol. 12 (7), pp. 3219-3222, 2019.
52. S. A. Alshehri, S. Wahab, S. S. Abullais, G. Das, U. Hani, W. Ahmad, M. Amir, A. Ahmad, G. Kandasamy, and R. Vasudevan, “Pharmacological Efficacy of Tamarix aphylla. A Comprehensive Review, “Plants, vol. 11 (1), 118. doi: 10.3390/plants11010118, 2021.
53. Q. A. Mandeel, “Microfungal community associated with rhizosphere soil of Zygophyllum qatarense in arid habitats of Bahrain,”Journal of Arid Environments,” vol. 50 (4), pp. 665–681. doi: 10.1006/jare.2001.0864, 2002.
54. F. Bibi, G. A. Strobel, M. I. Naseer, M. Yasir, A. A. K. Al-Ghamdi, E. I. Azhar, “Halophytes-associated endophytic and rhizospheric bacteria: Diversity, antagonism, and metabolite production,” Biocon. Sci. Technol., vol. 28, pp. 192-213, 2018.
55. K. L. Gartley, “Recommended methods for measuring soluble salts in soils, Chapter 10. In: Recommended Soil Testing Procedures for the Northeastern United States Last Revised Cooperative, Bulletin No. 493, pp. 87-94, 2022.
56. S. Gaudino, C. Galas, M. Belli, S. Barbizzi, P. de Zorzi, R. Jacimovic, Z. Jeran, A. Pati, and U. Sansone, “The role of different soil sample digestion methods on trace elements analysis: a comparison of ICP-MS and INAA measurement results,” Accred. Qual. Assur., vol. 12, pp. 84-93. https://doi.org/10.1007/s00769-006-0238-1, 2007.
57. P. Sarojam, “Trace Metal Characterization of Soils Using the Optima 7300 DV ICP-OES,” PerkinElmer, Inc., Shelton, CT 06484 USA, 2010-2012.
58. E. Bassiri, “Biology 275 online laboratory manual,” http://www. sas. upenn. edu/Lab Manuals/select. Dept. of Biology, Univ. of Pennsylvania. http://www.sas.upenn.edu/LabManuals/biol275/Table_of_Contents_fil es/10-Antibiotics-New.pdf, 2014.
59. A. Al-Mohannadi, “Screening and isolation of Streptomyces bacteria from rhizosphere of two shrubs Caroxylon imbricata and Tamarisk aphylla. Al-Ghariya Sabkhas, Qatar,” Final Report, Department of Biological and Environmental Sciences, College of Arts and Sciences, Qatar University, BIOL 497, ID: 201802595, 2022-2023.
60. D. Deyab, “Screening and isolation of Streptomyces bacteria from rhizosphere of two shrubs Tetraena qatarensis and Sporobolus ioclados. Al-Ghariya Sabkhas, Qatar,” Final Report, Department of Biological and Environmental Sciences, College of Arts and Sciences, Qatar University, BIOL 497, ID: 201801378, 2022-2023.
61. A. O. Ogundare, F. O. Ekundayo, and F. Banji- Onisile, “Antimicrobial activities of Streptomyces species isolated from various soil samples in Federal University of Technology, Akure Environment,” IOSR Journal of Pharmacy and Biological Sciences (IOSR-JPBS), vol. 10 (4), Ver. III, pp. 22-30. e-ISSN: 2278-3008, p-ISSN: 2319-7676, 2015.
62. A. E. Saleh, “Hydrocarbon degrading candidate bacteria isolated from Qatar polluted soil and molecular identification of key enzymes coding genes, “MSc. Thesis, Qatar University, College of Arts and Sciences, Department of Biological and Environmental Sciences, 2021.
63. M. Y. Ashfaq D. A. Da’na, and M. A. Al-Ghouti,”Application of MALDI-TOF MS for identification of environmental bacteria; a review,” J. Environ. Manage., vol. 305, 114359. doi: 10.1016/j.jenvman.2021.114359, 2022.
64. H. D. Chapman, and P. F. Pratt, “Methods of analysis for soils, plants, and waters,” California, Berkeley, Div. Agr. Sci. University of California, 1961.
65. H. Chenchouni,“Edaphic factors controlling the distribution of inland halophytes in an ephemeral Salt Lake “Sabkha Ecosystem” at North African semi-arid lands, “ Science of the Total Environment, vol. 575, pp. 660-671, 2017.
66. A. Kawasaki, P. G. Dennis, C. Forstner, A. K. H. Raghavendra, U. Mathesius, A. E. Richardson, E. Delhaize, M. Gilliham, M. Watt, P. R. Ryan, “Manipulating exudate composition from root apices shapes the microbiome throughout the root system,” Plant Physiol, vol. 187 (4), pp. 2279-2295. doi: 10.1093/plphys/kiab337, 2021.
67. R. F. Al-Thani, and B. T. Yasseen, “Phytoremediation of polluted soils and waters by native Qatari plants: future perspectives,” Environmental Pollution, vol. 259, 113694. https://doi.org/10.1016/j.envpol.2019.113694, 2020.
68. M. I. Mhlongo, L. A. Piater, N. E. Madala, N. Labuschagne, and I. A. Dubery, “The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance,” Front. Plant Sci., vol. 9, 112. doi: 10.3389/fpls.2018.00112, 2018.
69. N. Baeshen, L. Baz, A. Y. Shami, R. Ashy, R. Jalal, A. A. Abulfaraj, M. Refai, M. A. Majeed, S. S. Abuzahrah, H. A. Abdelkader, N. Baeshen, M. Baeshen, “Composition, abundance, and diversity of the soil microbiome associated with the halophytic plants Tamarix aphylla and Halopeplis perfoliata on Jeddah Seacoast, “Saudi Arabia. Plants, vol. 12 (11), 2176. doi: 10.3390/plants12112176, 2023.
70. P. J. Hogarth, “The Biology of mangroves,” Oxford, Oxford University Press, 228, 1999.
71. H. H. Zahran, “Diversity, adaptation, and activity of the bacterial flora in saline environments,” Biol. Fertil. Soils, vol. 25, pp. 211–223. doi: 10.1007/s003740050306, 1999.
72. A. Khan, M. Fiaz, R. Ali khan, J. Khan, F. Ullah khan, and Z. Wahab, “Antimicrobial efficacy of Tamarix dioca (L.) leaves and flowers,”Science Heritage Journal, vol. 2 (1), pp. 1-3. doi: 10.26480/gws.01.2018.01.03, 2018.
73. A. Frostegård, and E. Bååth,” The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil,” Biol Fert Soils, vol. 22, pp. 59-65. https://doi.org/10.1007/BF00384433, 1996.
74. S. C. Becerra, D. C. Roy, C. J. Sanchez, R. J. Christy, and D. M.Burmeister, “An optimized staining technique for the detection of Gram-positive and Gram-negative bacteria within tissue,” BMC Res Notes, vol. 9, 216. https://doi.org/10.1186/s13104-016-1902-0, 2016.
75. L. G. Oates, H. W. Read, J. L. M. Gutknecht, D. S. Duncan, T. B. Balser, and R. D. Jackson, “ A lipid extraction and analysis method for characterizing soil microbes in experiments with many samples,” J. Vis. Exp., vol. 125, 55310. doi: 10.3791/55310, 2017.
76. A. S. Sharmili, and P. Rasmasamy, “Fatty acid methyl ester (FAME) analysis of moderately thermophilic bacteria isolated from the Coramandal coast, Chennai, Tamilnadu,” European J. Exp. Biol., vol. 6 (6: 5), pp. 1-7, 2017.
77. R. Franco-Duarte, L. Černáková, S. Kadam, K. S. Kaushik, B. Salehi, A. Bevilacqua, M. R. Corbo, H. Antolak, K. Dybka-Stępień, M. Leszczewicz, S. Relison Tintino, V. C. Alexandrino de Souza, J. Sharifi-Rad, H. D. M. Coutinho, N. Martins, and C. F. Rodrigues, “Advances in chemical and biological methods to identify microorganisms-from past to present,” Microorganisms, vol. 7 (5), E 130. https://doi.org/10.3390/microorganisms7050130, 2019.
78. V. Solntceva, M. Kostrzewa, and G. Larrouy-Maumus, “Detection of species-specific lipids by routine MALDI TOF Mass spectrometry to unlock the challenges of microbial identification and antimicrobial susceptibility testing,” Front. Cell Infect. Microbiol., vol. 10, 621452. doi: 10.3389/fcimb.2020.621452, 2021.
79. I. Saadoun, F. Al-Momani, H. I. Malkawi, and M. J. Mohammad, “Isolation, identification, and analysis of antibacterial activity of soil Streptomycetes isolates from north Jordan,” Microbios, vo. 100 (395), pp. 41-46, 1999.
80. S. Rammali, L. Hilali, K. Dari, B. Bencharki, A. Rahim, M. Timinouni, F. Gaboune, M. El Aalaoui, and A. Khattabi, “Antimicrobial and antioxidant activities of Streptomyces species from soils of three different cold sites in the Fez-Meknes region Morocco,” Sci. Rep., vol. 12 (1), 17233. doi: 10.1038/s41598-022-21644-z, 2022.
81. A. Kumar, and J. P. Verma, “Does plant-microbe interaction confer stress tolerance in plants: A review?,” Microbiol. Res., vol. 207, pp. 41–52. doi: 10.1016/j.micres.2017.11.004, 2018.
82. A. Meena, and K. S. Rao,”Assessment of soil microbial and enzyme activity in the rhizosphere zone under different land use/cover of a semiarid region, India,” Ecol. Process, vol. 10: https://doi.org/10.1186/s13717-021-00288-3, 2021.
83. G. Shukla, and A. Varma, (Eds.), “Soil enzymology,” Springer: Berlin/Heidelberg, Germany, pp. 1–392, 2011.
84. A. T. Adetunji, F. B. Lewu, Mulidzi, R., and B. Ncube, “The biological activities of β-glucosidase, phosphatase, and urease as soil quality indicators: a review, “J. Soil Sci. Plant Nutr., vol. 17 (3), Temuvo set. http://dx.doi.org/10.4067/S0718-95162017000300018, 2017.
85. S. Ullah, C. Ai, S. Huang, J. Zhang, L. Jia, J. Ma, W. Zhou, and P. He, “The responses of extracellular enzyme activities and microbial community composition under nitrogen addition in an upland soil,” PLoS One, vol. 14 (9), e0223026. doi: 10.1371/journal.pone.0223026, 2019.
86. L. Loucif, E. Bendjama, D. Gacemi-Kirane, and J. M. Rolain, “Rapid identification of Streptomyces isolates by MALDI-TOF MS, “Microbiological research, vol. 169 (12), pp. 940–947. https://doi.org/10.1016/j.micres.2014.04.004, 2014.
87. M. L. Yarbrough, W. Lainhart, and C. D. Burnham, “Identification of Nocardia, Streptomyces, and Tsukamurella using MALDI-TOF MS with the Bruker Biotyper,” Diagnostic microbiology and infectious disease, vol. 89 (2), pp. 92–97. https://doi.org/10.1016/j.diagmicrobio.2017.06.019, 2017.
88. T. M. Farhat, Z. A. Al Disi, M. Y. Ashfaq, and N. Zouari, “Study of diversity of mineral-forming bacteria in Sabkha mats and sediments of mangrove forest in Qatar,” Biotechnology reports (Amsterdam, Netherlands), vol. 39, e00811. https://doi.org/10.1016/j.btre.2023.e00811, 2023.