Insights of organic fertilizer micro flora of bovine manure and their useful potentials in sustainable agriculture

Autoři: Dalaq Aiysha aff001;  Zakia Latif aff001
Působiště autorů: Department of Microbiology and Molecular Genetics, University of the Punjab, Lahore, Pakistan aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226155


Exploration of diverse environmental samples for plant growth-promoting microbes to fulfill the increasing demand for sustainable agriculture resulted in increased use of bacterial biofertilizer. We aimed for the isolation of plant growth-promoting as well as antibiotic sensitive bacteria from bovine manure samples. The basic theme of our study is to highlight potentials of bacteria in manure and the unchecked risk associated with the application of manure i.e. introducing antibiotic-resistant microbial flora, as fertilizer. Fifty-two, morphologically distinct isolates; from eight different manure samples, were subjected to plant growth-promoting parametric tests along with antibiotic resistance. Thirteen antibiotic sensitive bacterial strains with potentials of plant growth promotion further characterized by 16S rRNA ribotyping and the identified genera were Stenotrophomonas, Achromobacter, Pseudomonas, and Brevibacillus. Successful radish seeds germination under sterile in-vitro conditions showed the potential of selected bacterial isolates as plant growth-promoting bacteria. The results of this study confirmed plant growth-promoting characteristics of bovine manures’ bacterial strains along with an alarming antibiotic resistance load which comprises 75% of bacterial isolated population. Our study showed distinct results of un-explored manure bacterial isolates for plant growth promotion and flagged ways associated with unchecked manure application in agriculture soil through high load of antibiotic resistant bacteria.

Klíčová slova:

Antibiotic resistance – Antibiotics – Bacteria – Fertilizers – Magnesium – Plant growth and development – Seed germination – Radish


1. Menzi H, Oenema O, Burton C, Shipin O, Gerber P, Robinson T, et al. Impacts of intensive livestock production and manure management on the environment. Livestock in a Changing Landscape. 2010; 1:139–63.

2. Parodi A, Leip A, De Boer IJ, Slegers PM, Ziegler F, Temme EH, et al. The potential of future foods for sustainable and healthy diets. Nature Sustainability. 2018; 1(12):782.

3. Steinfeld H, Gerber P, Wassenaar TD, Castel V, Rosales M, Rosales M, et al. Livestock’s long shadow: environmental issues and options. Food & Agriculture Org.; 2006.

4. Jarvie HP, Sharpley AN, Flaten D, Kleinman PJ, Jenkins A, Simmons T. The pivotal role of phosphorus in a resilient water–energy–food security nexus. Journal of Environmental Quality. 2015; 44(4):1049–62. doi: 10.2134/jeq2015.01.0030 26437086

5. Subaedah S, Aladin A. Fertilization of nitrogen, phosphor and application of green manure of Crotalaria juncea in increasing yield of maize in marginal dry land. Agriculture and Agricultural Science Procedia. 2016; 9:20–5.

6. Cai A, Zhang W, Xu M, Wang B, Wen S, Shah SA. Soil fertility and crop yield after manure addition to acidic soils in South China. Nutrient Cycling In Agroecosystems. 2018; 111(1):61–72.

7. Zhang Y, Shen H, He X, Thomas BW, Lupwayi NZ, Hao X, et al. Fertilization shapes bacterial community structure by alteration of soil pH. Frontiers in Microbiology. 2017; 8:1325. doi: 10.3389/fmicb.2017.01325 28769896

8. Chinnadurai C, Gopalaswamy G, Balachandar D. Long term effects of nutrient management regimes on abundance of bacterial genes and soil biochemical processes for fertility sustainability in a semi-arid tropical Alfisol. Geoderma. 2014; 232:563–72.

9. Francioli D, Schulz E, Lentendu G, Wubet T, Buscot F, Reitz T. Mineral vs. organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Frontiers in Microbiology. 2016; 7:1446. doi: 10.3389/fmicb.2016.01446 27683576

10. Hartmann M, Frey B, Mayer J, Mäder P, Widmer F. Distinct soil microbial diversity under long-term organic and conventional farming. The ISME Journal. 2015; 9(5):1177. doi: 10.1038/ismej.2014.210 25350160

11. Erhunmwunse AS, Olayinka A, Atoloye IA. Nutrient mineralization from nitrogen-and phosphorus-enriched poultry manure compost in an ultisol. Communications in Soil Science and Plant Analysis. 2019; 50(2):185–97.

12. Tule A, Hassani U. Colonization with antibiotic-resistant E. coli in commensal fecal flora of newborns. International Journal of Current Microbiology and Applied Science. 2017; 6:1623–9.

13. Mottet A, de Haan C, Falcucci A, Tempio G, Opio C, Gerber P. Livestock: On our plates or eating at our table? A new analysis of the feed/food debate. Global Food Security. 2017; 14:1–8.

14. McKenna M. The coming cost of superbugs: 10 Million Deaths per Year.

15. Sobur MA, Sabuj AA, Sarker R, Rahman AT, Kabir SL, Rahman MT. Antibiotic-resistant Escherichia coli and Salmonella spp. associated with dairy cattle and farm environment having public health significance. Veterinary World. 2019; 12(7):984. doi: 10.14202/vetworld.2019.984-993 31528022

16. Pérez-Valera E, Kyselková M, Ahmed E, Sladecek FX, Goberna M, Elhottová D. Native soil microorganisms hinder the soil enrichment with antibiotic resistance genes following manure applications. Scientific Reports. 2019; 9(1):6760. doi: 10.1038/s41598-019-42734-5 31043618

17. Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K. Fate and effects of veterinary antibiotics in soil. Trends in Microbiology. 2014; 22(9):536–45. doi: 10.1016/j.tim.2014.05.005 24950802

18. Li B, Webster TJ. Bacteria antibiotic resistance: New challenges and opportunities for implant‐associated orthopedic infections. Journal of Orthopaedic Research. 2018; 36(1):22–32. doi: 10.1002/jor.23656 28722231

19. Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin YF, Yannarell AC, et al. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. Journal of Environmental Quality. 2009; 38(3):1086–108. doi: 10.2134/jeq2008.0128 19398507

20. Unc A, Goss MJ. Transport of bacteria from manure and protection of water resources. Applied Soil Ecology. 2004; 25(1):1–8.

21. Durso LM, Cook KL. Impacts of antibiotic use in agriculture: what are the benefits and risks? Current Opinion in Microbiology. 2014; 19:37–44. doi: 10.1016/j.mib.2014.05.019 24997398

22. Zhang Y, Hao X, Alexander TW, Thomas BW, Shi X, Lupwayi NZ. Long-term and legacy effects of manure application on soil microbial community composition. Biology and Fertility of Soils. 2018; 54(2):269–83.

23. Long CM, Muenich RL, Kalcic MM, Scavia D. Use of manure nutrients from concentrated animal feeding operations. Journal of Great Lakes Research. 2018; 44(2):245–52.

24. Gao J, Luo Y, Wei Y, Huang Y, Zhang H, He W, et al. Screening of plant growth promoting bacteria (PGPB) from rhizosphere and bulk soil of Caragana microphylla in different habitats and their effects on the growth of Arabidopsis seedlings. Biotechnology & Biotechnological Equipment. 2019; 33(1):921–30.

25. Habibi S, Djedidi S, Ohkama-Ohtsu N, Sarhadi WA, Kojima K, Rallos RV, et al. Isolation and screening of indigenous plant growth-promoting rhizobacteria from different rice cultivars in Afghanistan soils. Microbes and Environments. 2019:ME18168.

26. Dhama K, Chauhan RS, Singhal L. Anti-cancer activity of cow urine: current status and future directions. International Journal of Cow Science. 2005; 1(2):1–25.

27. Randhawa GK, Kullar JS. Bioremediation of pharmaceuticals, pesticides, and petrochemicals with gomeya/cow dung. ISRN Pharmacology. 2011; 2011.

28. Sawant AA, Hegde NV, Straley BA, Donaldson SC, Love BC, Knabel SJ, et al. Antimicrobial-resistant enteric bacteria from dairy cattle. Applied Environmental Microbiology. 2007; 73(1):156–63. doi: 10.1128/AEM.01551-06 17098918

29. Heberle H, Meirelles GV, da Silva FR, Telles GP, Minghim R. InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics. 2015; 16(1):169.

30. Kumar A, Maurya BR, Raghuwanshi R. Isolation and characterization of PGPR and their effect on growth, yield and nutrient content in wheat (Triticum aestivum L.). Biocatalysis and Agricultural Biotechnology. 2014; 3(4):121–8.

31. Kumar A, Bahadur I, Maurya BR, Raghuwanshi R, Meena VS, Singh DK, et al. Does a plant growth-promoting rhizobacteria enhance agricultural sustainability? Journal of Pure and Applied Microbiology. 2015; 9(1):715–24.

32. Siddiqui ZA. PGPR: prospective biocontrol agents of plant pathogens. In PGPR: biocontrol and biofertilization 2005 (pp. 111–142). Springer, Dordrecht.

33. Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and Soil. 2009; 321(1–2):305–39.

34. Narayanan CM. Production of Phosphate-Rich Biofertiliser Using Vermicompost and Anaerobic Digestor Sludge—A Case Study.

35. Castagno LN, Estrella MJ, Sannazzaro AI, Grassano AE, Ruiz OA. Phosphate‐solubilization mechanism and in vitro plant growth promotion activity mediated by Pantoea eucalypti isolated from Lotus tenuis rhizosphere in the Salado River Basin (Argentina). Journal of Applied Microbiology. 2011; 110(5):1151–65. doi: 10.1111/j.1365-2672.2011.04968.x 21299771

36. Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N. Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microbial Cell Factories. 2014; 13(1):66.

37. Glick BR. Plant growth-promoting bacteria: mechanisms and applications. Scientifica. 2012; 2012.

38. Archana DS, Nandish MS, Savalagi VP, Alagawadi AR. Characterization of potassium solubilizing bacteria (KSB) from rhizosphere soil. Bioinfolet-A Quarterly Journal of Life Sciences. 2013; 10(1b):248–57.

39. Teo KC, Teoh SM. Preliminary biological screening of microbes isolated from cow dung in Kampar. African Journal of Biotechnology. 2011; 10(9):1640–5.

40. Dobereiner J, Baldani VL. Biological nitrogen fixation by endophytic diazotrophs in non-leguminous crops in the tropics. In Nitrogen fixation with non-legumes 1998 (pp. 3–7). Springer, Dordrecht.

41. Glickmann E, Dessaux Y. A critical examination of the specificity of the salkowski’s reagent for indolic compounds produced by phytopathogenic bacteria. Applied Environmental Microbiology. 1995; 61(2):793–6. 16534942

42. Castric KF, Castric PA. Method for rapid detection of cyanogenic bacteria. Applied Environmental Microbiology.1983; 45(2):701–2. 16346217

43. Nautiyal CS. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters. 1999; 170(1):265–70. doi: 10.1111/j.1574-6968.1999.tb13383.x 9919677

44. Aleksandrov VG, Il’ev IP. Phosphorus acid isolation from apatite produced by silicate bacteria. Mikrobiolohichnyi Zhurnal. 1967; 29(2):111–4. 4308691

45. Rana G, Mandal T, Mandal NK, Sakha D, Meikap BC. Calcite solubilization by bacteria: A novel method of environment pollution control. Geomicrobiology Journal. 2015; 32(9):846–52.

46. Mumtaz MZ, Ahmad M, Jamil M, Hussain T. Zinc solubilizing Bacillus spp. potential candidates for biofortification in maize. Microbiological Research. 2017; 202:51–60. doi: 10.1016/j.micres.2017.06.001 28647123

47. Resende JA, Silva VL, de Oliveira TL, de Oliveira Fortunato S, da Costa Carneiro J, Otenio MH, et al. Prevalence and persistence of potentially pathogenic and antibiotic resistant bacteria during anaerobic digestion treatment of cattle manure. Bioresource Technology. 2014; 153:284–91. doi: 10.1016/j.biortech.2013.12.007 24374028

48. Normand P. Utilisation des séquences 16S pour le positionnement phylétique d’un organisme inconnu. Oceanis. 1995;21:31–56.

49. Yildrim E, Donmez MF, Turan M. Use of bioinoculants in ameliorative effects on radish plants under salinity stress. Journal of plant nutrition. 2008; 31(12):2059–74.

Článek vyšel v časopise


2019 Číslo 12