Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter July 20, 2020

Development, spread and persistence of antibiotic resistance genes (ARGs) in the soil microbiomes through co-selection

  • Anand Prakash Maurya , Jina Rajkumari , Amitabha Bhattacharjee and Piyush Pandey EMAIL logo

Abstract

Bacterial pathogens resistant to multiple antibiotics are emergent threat to the public health which may evolve in the environment due to the co-selection of antibiotic resistance, driven by poly aromatic hydrocarbons (PAHs) and/or heavy metal contaminations. The co-selection of antibiotic resistance (AMR) evolves through the co-resistance or cross-resistance, or co-regulatory mechanisms, present in bacteria. The persistent toxic contaminants impose widespread pressure in both clinical and environmental setting, and may potentially cause the maintenance and spread of antibiotic resistance genes (ARGs). In the past few years, due to exponential increase of AMR, numerous drugs are now no longer effective to treat infectious diseases, especially in cases of bacterial infections. In this mini-review, we have described the role of co-resistance and cross-resistance as main sources for co-selection of ARGs; while other co-regulatory mechanisms are also involved with cross-resistance that regulates multiple ARGs. However, co-factors also support selections, which results in development and evolution of ARGs in absence of antibiotic pressure. Efflux pumps present on the same mobile genetic elements, possibly due to the function of Class 1 integrons (Int1), may increase the presence of ARGs into the environment, which further is promptly changed as per environmental conditions. This review also signifies that mutation plays important role in the expansion of ARGs due to presence of diverse types of anthropogenic pollutants, which results in overexpression of efflux pump with higher bacterial fitness cost; and these situations result in acquisition of resistant genes. The future aspects of co-selection with involvement of systems biology, synthetic biology and gene network approaches have also been discussed.


Corresponding author: Dr. Piyush Pandey, Professor and Head, Department of Microbiology, Assam University, Silchar, 788011, Assam, India, E-mail:

  1. Research funding: Authors acknowledge the Department of Biotechnology (DBT), Ministry of Science and Technology, Govt. of India for financial support.

  2. Author contributions: APM, JR and PP: manuscript writing and compilation; PP and AB: Manuscript checking and comments. PP: Overall conceptualization, supervision and finalizing the manuscript.

  3. Competing interests: Authors declare no conflict of interest.

  4. Informed consent: Not applicable.

  5. Ethical approval: Not applicable.

References

1. Wright, GD. Opportunities for natural products in 21st century antibiotic discovery. Nat Prod Rep 2017;34:694–701. https://doi.org/10.1039/c7np00019g.Search in Google Scholar PubMed

2. Bassetti, M, Peghin, M, Vena, A, Giacobbe, DR. Treatment of infections due to MDR Gram-negative bacteria. Front Med 2019;6:74. https://doi.org/10.3389/fmed.2019.00074.Search in Google Scholar PubMed PubMed Central

3. Sultan, I, Rahman, S, Jan, AT, Siddiqui, MT, Mondal, AH, Haq, QMR. Antibiotics, resistome and resistance mechanisms: a bacterial perspective. Front Microbiol 2018;9:2066. https://doi.org/10.3389/fmicb.2018.02066.Search in Google Scholar PubMed PubMed Central

4. Canton, R, Garbajosa, PR. Co-resistance: an opportunity for the bacteria and resistance genes. Curr Opin Pharmacol 2011;11:477–85. https://doi.org/10.1016/j.coph.2011.07.007.Search in Google Scholar PubMed

5. Durao, P, Balbontin, R, Gordo, I. Evolutionary mechanisms shaping the maintenance of antibiotic resistance. Trends Microbiol 2018;26:677–91. https://doi.org/10.1016/j.tim.2018.01.005.Search in Google Scholar PubMed

6. Yelin, I, Kishony, R. Antibiotic resistance. Cell 2018;172:1136.e1. https://doi.org/10.1016/j.cell.2018.02.018.Search in Google Scholar PubMed

7. Perry, JA, Westman, EL, Wright, GD. The antibiotic resistome: what’s new? Curr Opin Microbiol 2014;21:45–50. https://doi.org/10.1016/j.mib.2014.09.002.Search in Google Scholar PubMed

8. Webber, MA, Whitehead, RN, Mount, M, Loman, NJ, Pallen, MJ, Piddock, LJ. Parallel evolutionary pathways to antibiotic resistance selected by biocide exposure. J Antimicrob Chemother 2015;70:2241–8. https://doi.org/10.1093/jac/dkv109.Search in Google Scholar PubMed PubMed Central

9. Palme, JB, Kristiansson, E, Larsson, DGJ. Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiol Rev 2018;42:68–80. http://dx.doi.org/10.1093/femsre/fux053.10.1093/femsre/fux053Search in Google Scholar PubMed PubMed Central

10. Rodgers, K, McLellan, L, Peshkur, T, Williams, R, Tonner, R, Hursthouse, AS, et al.. Can the legacy of industrial pollution influence antimicrobial resistance in estuarine sediments? Environ Chem Lett 2019;17:595–607. https://doi.org/10.1007/s10311-018-0791-y.Search in Google Scholar

11. Seiler, C, Berendonk, TU. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol 2012;3:399. https://doi.org/10.3389/fmicb.2012.00399.Search in Google Scholar PubMed PubMed Central

12. Wang, R, Lai, TP, Gao, P, Zhang, H, Ho, PL, Woo, PC, et al.. Bismuth antimicrobial drugs serve as broad spectrum metallo-β-lactamase inhibitors. Nat Commun 2018;9:439. https://doi.org/10.1038/s41467-018-02828-6.Search in Google Scholar PubMed PubMed Central

13. Gisbert, JP. Helicobacter pylori eradication: a new, single-capsule bismuth-containing quadruple therapy. Nat Rev Gastroenterol Hepatol 2011;8:307–9. https://doi.org/10.1038/nrgastro.2011.84.Search in Google Scholar PubMed

14. Chey, WD, Leontiadis, GI, Howden, CW, Moss, SF. ACG clinical guideline: treatment of Helicobacter pylori infection. Am J Gastroenterol 2017;112:212–39. https://doi.org/10.1038/ajg.2016.563.Search in Google Scholar PubMed

15. Austin, CB, Wright, MS, Stepanauskas, R, McArthur, JV. Co-selection of antibiotic and metal resistance. TRENDS Microbiol 2006;14:176–82. https://doi.org/10.1016/j.tim.2006.02.006.Search in Google Scholar PubMed

16. Chen, B, He, R, Yuan, K, Chen, E, Lin, L, Chen, X, et al.. Polycyclic aromatic hydrocarbons (PAHs) enriching antibiotic resistance genes (ARGs) in the soils. Environm Poll 2016;6(Pt B):1–9. http://dx.doi.org/10.1016/j.envpol.2016.11.047.10.1016/j.envpol.2016.11.047Search in Google Scholar PubMed

17. Yazdankhah, S, Skjerve, E, Wasteson, Y. Antimicrobial resistance due to the content of potentially toxic metals in soil and fertilizing products. Microb Eco Health Dis 2018;29:1548248. https://doi.org/10.1080/16512235.2018.1548248.Search in Google Scholar PubMed PubMed Central

18. Chen, J, Li, J, Zhang, H, Shi, W, Liu, Y. Bacterial Heavy-Metal and Antibiotic resistance genes in a copper tailing dam area in northern China. Front Microbiol 2019;10:1916. https://doi.org/10.3389/fmicb.2019.01916.Search in Google Scholar PubMed PubMed Central

19. Palme, JB, Milakovic, M, Svecova, H, Ganjto, M, VJonsson, V, Grabic, R, et al.. Industrial wastewater treatment plant enriches antibiotic resistance genes and alters the structure of microbial communities. Water Res 2019;162:437–45. https://doi.org/10.1016/j.watres.2019.06.073.Search in Google Scholar PubMed

20. Bazzi, W, Abou Fayad, AG, Nasser, A, Haraoui, L-P, Dewachi, O, Abou-Sitta, G, et al.. Heavy metal toxicity in armed conflicts potentiates AMR in A. baumannii by selecting for antibiotic and heavy metal co-resistance mechanisms. Front Microbiol 2020;11:68. https://doi.org/10.3389/fmicb.2020.00068.Search in Google Scholar PubMed PubMed Central

21. Poole, K. At the nexus of antibiotics and metals: the impact of Cu and Zn on antibiotic activity and resistance. Trends Microbiol 2017;25:820–32. https://doi.org/10.1016/j.tim.2017.04.010.Search in Google Scholar PubMed

22. Cycon, M, Mrozik, A, Piotrowska-Seget, Z. Antibiotics in the soil environment-degradation and their impact on microbial activity and diversity. Front Microbiol 2019;10:338. https://doi.org/10.3389/fmicb.2019.00338.Search in Google Scholar PubMed PubMed Central

23. Almakki, A, Bilak, EJ, Marchandin, H, Fajardo, PL. Antibiotic resistance in urban runoff. Sci Total Environ 2019;667:64–76. https://doi.org/10.1016/j.scitotenv.2019.02.183.Search in Google Scholar PubMed

24. Chen, B, He, R, Yuan, K, Chen, E, Lin, L, Chen, X, et al.. Polycyclic aromatic hydrocarbons (PAHs) enriching antibiotic resistance genes (ARGs) in the soils. Environ Pollut 2017;220(Pt B):1005–13. https://doi.org/10.1016/j.envpol.2016.11.047.Search in Google Scholar PubMed

25. Gorovtsov, AV, Sazykin, IS, Sazykina, MA. The influence of heavy metals, polyaromatic hydrocarbons, and polychlorinated biphenyls pollution on the development of antibiotic resistance in soils. Environ Sci Pollut Res Int 2018;25:9283–92. https://doi.org/10.1007/s11356-018-1465-9.Search in Google Scholar PubMed

26. Wang, J, Wang, J, Zhao, Z, Chen, J, Lu, H, Liu, G, et al.. PAHs accelerate the propagation of antibiotic resistance genes in coastal water microbial community. Environ Pollut 2017;231(Pt 1):1145–52. https://doi.org/10.1016/j.envpol.2017.07.067.Search in Google Scholar PubMed

27. Grenni, P, Ancona, V, Barra Caracciolo, A. Ecological effects of antibiotics on natural ecosystems: a review. Microchem J 2018;136:25–39. https://doi.org/10.1016/j.microc.2017.02.006.Search in Google Scholar

28. Lister, PD, Wolter, DJ, Hanson, ND. Antibacterial resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin Microbiol Rev 2009;22:582–610. https://doi.org/10.1128/cmr.00040-09.Search in Google Scholar

29. Yang, QE, Agouri, SR, Tyrrell, JM, Walsh, TR. Heavy metal resistance genes are associated with blaNDM-1 and blaCTX-M-15 carrying Enterobacteriaceae. Antimicrob Agents Chemother 2018;62:e02642-17. https://doi.org/10.1128/aac.02642-17.Search in Google Scholar PubMed PubMed Central

30. Liu, P, Chen, X, Huang, Q, Chen, W. The Role of CzcRS Two-component systems in the heavy metal resistance of Pseudomonas putida X4. Int J Mol Sci 2015;16:17005–17. https://doi.org/10.3390/ijms160817005.Search in Google Scholar PubMed PubMed Central

31. Buffet-Bataillon, S, Tattevin, P, Maillard, J-Y, Bonnaure-Mallet, M, Jolivet-Gougeon, A. Efflux pump induction by quaternary ammonium compounds and fluoroquinolone resistance in bacteria. Fut Microbiol 2016;11:81–92. https://doi.org/10.2217/fmb.15.131.Search in Google Scholar PubMed

32. Xu, YB, Hou, MY, Li, YF, Huang, L, Ruan, JJ, Zheng, L, et al.. Distribution of tetracycline resistance genes and AmpC β-lactamase genes in representative non-urban sewage plants and correlations with treatment processes and heavy metals. Chemosphere 2017;170:274–81. https://doi.org/10.1016/j.chemosphere.2016.12.027.Search in Google Scholar PubMed

33. Li, L-G, Xia, Y, Zhang, T. Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME J 2017;11:651–62. https://doi.org/10.1038/ismej.2016.155.Search in Google Scholar PubMed PubMed Central

34. Eduardo-Correia, B, Morales-Filloy, H, Abad, JP. Bacteria from the multi-contaminated tinto river estuary (SW, Spain) show high multi-resistance to antibiotics and point to Paenibacillus spp. as antibiotic-resistance-dissemination players. Front Microbiol 2020;10:3071. https://doi.org/10.3389/fmicb.2019.03071.Search in Google Scholar PubMed PubMed Central

35. Abdulazeez, TL. Polycyclic aromatic hydrocarbons. A review. Cogent Environ Sci 2017;3:1339841. https://doi.org/10.1080/23311843.2017.1339841.Search in Google Scholar

36. Yao, X, Tao, F, Zhang, K, Tang, H, Xu, P. Multiple roles for two efflux pumps in the polycyclic aromatic hydrocarbon-degrading Pseudomonas putida strain B6-2 (DSM 28064). Appl Environ Microbiol 2017;83:01882-17. https://doi.org/10.1128/aem.01882-17.Search in Google Scholar PubMed PubMed Central

37. Summers, AO. Genetic linkage and horizontal gene transfer, the roots of the antibiotic multi-resistance problem. Anim Biotechnol 2006;17:125–35. https://doi.org/10.1080/10495390600957217.Search in Google Scholar PubMed

38. Farias, P, Espírito Santo, C, Branco, R, Francisco, R, Santos, S, Hansen, L, et al.. Natural hot spots for gain of multiple resistances: arsenic and antibiotic resistances in heterotrophic, aerobic bacteria from marine hydrothermal vent fields. Appl Environ Microbiol 2015;81:2534–43. https://doi.org/10.1128/aem.03240-14.Search in Google Scholar

39. Ghosh, A, Singh, A, Ramteke, PW, Singh, VP. Characterization of large plasmids encoding resistance to toxic heavy metals in Salmonella abortus equi. Biochem Biophys Res Commun 2000;272:6–11. https://doi.org/10.1006/bbrc.2000.2727.Search in Google Scholar PubMed

40. Huijbers, PMC, Flach, CF, Larsson, DJG. A conceptual framework for the environmental surveillance of antibiotics and antibiotic resistance. Environ Intern 2019;130:104880. https://doi.org/10.1016/j.envint.2019.05.074.Search in Google Scholar PubMed

41. Campos, J, Cristino, L, Peixe, L, Antunes, P. MCR-1 in multidrug-resistant and copper-tolerant clinically relevant Salmonella 1,4,[5],12:i:- and S. Rissen clones in Portugal, 2011 to 2015. Euro Surveill 2016;21:30270. https://doi.org/10.2807/1560-7917.es.2016.21.26.30270.Search in Google Scholar PubMed

42. Melnyk, AH, Wong, A, Kasse, R. The fitness costs of antibiotic resistance mutations. Evol Appl 2015;8:273–83. https://doi.org/10.1111/eva.12196.Search in Google Scholar PubMed PubMed Central

43. Wales, AD, Daves, RH. Co-selection of resistance to antibiotics, biocides and heavy metals, and its relevance to foodborne pathogens. Antibiotics 2015;4:567–604. https://doi.org/10.3390/antibiotics4040567.Search in Google Scholar PubMed PubMed Central

44. Santos-Lopez, A, Marshall, CW, Scribner, MR, Snyder, DJ, Cooper, VS. Evolutionary pathways to antibiotic resistance are dependent upon environmental structure and bacterial lifestyle. ELife 2019;8:47612. https://doi.org/10.7554/eLife.47612.Search in Google Scholar PubMed PubMed Central

45. Vogwill, T, Maclean, RC. The genetic basis of the fitness costs of antimicrobial resistance: a meta-analysis approach. Evol Appl 2015;8:284–95. https://doi.org/10.1111/eva.12202.Search in Google Scholar PubMed PubMed Central

46. Krishnamurthy, M, Moore, RT, Rajamani, S, Panchal, RG. Bacterial genome engineering and synthetic biology: combating pathogens. BMC Microbiol 2016;16:258. https://doi.org/10.1186/s12866-016-0876-3.Search in Google Scholar PubMed PubMed Central

47. Baker, SJ, Payne, DJ, Rappuoli, R, Gregorio, ED. Technologies to address antimicrobial resistance. Proc Natl Acad Sci 2018;115:12887–95. https://doi.org/10.1073/pnas.1717160115.Search in Google Scholar PubMed PubMed Central

48. Chowdhury, AS, Call, DR, Broschat, SR. Antimicrobial resistance prediction for gram-negative bacteria via game theory-based feature evaluation. Sci Rep 2019;9:14487. https://doi.org/10.1038/s41598-019-50686-z.Search in Google Scholar PubMed PubMed Central

49. Lee, M, Pinto, NA, Kim, CY, Yang, S, D’Souza, R, Yong, D, et al. Network integrative genomic and transcriptomic analysis of carbapenem-resistant Klebsiella pneumoniae strains identifies genes for antibiotic resistance and virulence. mSystems 2019;4:e00202-19. https://doi.org/10.1128/msystems.00202-19.Search in Google Scholar PubMed PubMed Central

50. Grimes, T, Potter, SST, Datta, S. Integrating gene regulatory pathways into differential network analysis of gene expression data. Sci Rep 2019;9:5479. https://doi.org/10.1038/s41598-019-41918-3.Search in Google Scholar PubMed PubMed Central

51. Boolchandani, M, D’Souza, AW, Dantas, G. Sequencing-based methods and resources to study antimicrobial resistance. Nat Rev 2019;20:356–70. https://doi.org/10.1038/s41576-019-0108-4.Search in Google Scholar PubMed PubMed Central

52. Su, M, Satola, SW, Read, TD. Genome-based prediction of bacterial antibiotic resistance. J Clin Microbiol 2019;57:e01405-18. https://doi.org/10.1128/jcm.01405-18.Search in Google Scholar

53. Martin-Galiano, AJ, McConnell, MJ. Using OMICS technologies and systems biology to identify epitope targets for the development of monoclonal antibodies against antibiotic-resistant bacteria. Front Immunol 2019;10:2841. https://doi.org/10.3389/fimmu.2019.02841.Search in Google Scholar PubMed PubMed Central

54. Camp, PV, Haslam, DB, Porollo, A. Bioinformatics approaches to the understanding of molecular mechanisms in antimicrobial resistance. Int J Mol Sci 2020;21:1363.https://doi.org/10.3390/ijms21041363.Search in Google Scholar PubMed PubMed Central

55. Zampieri, M, Enke, T, Chubukov, V, Ricci, V, Piddock, L, Sauer, U. Metabolic constraints on the evolution of antibiotic resistance. Mol Syst Biol 2017;13:917. https://doi.org/10.15252/msb.20167028.Search in Google Scholar PubMed PubMed Central

56. Rodrigo, G, Bajic, D, Elola, I, Poyatos, JF. Deconstructing a multiple antibiotic resistance regulation through the quantification of its input function. NPJ Syst Biol Applic 2017;3:30. https://doi.org/10.1038/s41540-017-0031-2.Search in Google Scholar PubMed PubMed Central

Received: 2020-03-29
Accepted: 2020-06-13
Published Online: 2020-07-20
Published in Print: 2020-11-18

© 2020 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 10.12.2023 from https://www.degruyter.com/document/doi/10.1515/reveh-2020-0035/html
Scroll to top button