Advertisement

Exploration of Soil Resistome Through a Metagenomic Approach

  • Sankalp Misra
  • Vijay Kant Dixit
  • Swapnil Pandey
  • Shashank Kumar Mishra
  • Nikita Bisht
  • Puneet Singh ChauhanEmail author
Chapter

Abstract

Resistance toward antibiotics in microbes is considered to be one of the most significant challenges to modern medicine. The sum total of resistance genes against antibiotics in microorganism present in the soil is called the soil resistome and could serve as a source of resistance in microbes that can ultimately serve as a sink for drug discoveries. A deep knowledge of soil resistome and its multilateral interaction with advancement in drug development is essential for implementing suitable actions reducing spread of resistance in an efficient way. However, the soil resistome and its evolution are still in their infancy. The amalgamation of metagenomics with next-generation sequencing technology proved to be a robust methodological approach for exploring the soil microbiome, along with other related factors, especially the resistome. In this chapter, we have tried to incorporate the current knowledge on how the soil resistome is designed and discuss application of metagenomics to decipher hidden processes, particularly in respect to novel findings for medical diagnostics, controlling infections, and improving public health.

Keywords

Metagenomics Antibiotic resistome Rhizosphere Microbial diversity 

Notes

Acknowledgments

The authors acknowledge Director, CSIR-National Botanical Research Institute, for providing facilities and support during the study. The authors also acknowledge the financial assistance from CSIR-Network project (MLP022; OLP 0105). The authors have no conflict of interest.

References

  1. Allen, H. K., An, R., Handelsman, J., & Moe, L. A. (2015). A response regulator from a soil metagenome enhances resistance to the β-lactam antibiotic carbenicillin in Escherichia coli. PLoS One, 10, e0120094.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alnoch, R. C., Martini, V. P., Glogauer, A., Costa, A. C., Piovan, L., Muller-Santos, M., de Souza, E. M., de Oliveira, P. F., Mitchell, D. A., & Krieger, N. (2015). Immobilization and characterization of a new regioselective and enantioselective lipase obtained from a metagenomic library. PLoS One, 10, e0114945.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Amos, G. C., Zhang, L., Hawkey, P. M., Gaze, W. H., & Wellington, E. M. (2014). Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Veterinary Microbiology, 171, 441–447.PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bengtsson-Palme, J., & Larsson, D. G. J. (2015). Antibiotic resistance genes in the environment: Prioritizing risks. Nature Reviews. Microbiology, 13, 396.PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bérdy, J. (2005). Bioactive microbial metabolites. The Journal of Antibiotics, 58, 1–26.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Berthold, T., Centler, F., Hubschmann, T., Remer, R., Thullner, M., Harms, H., & Wick, L. Y. (2016). Mycelia as a focal point for horizontal gene transfer among soil bacteria. Scientific Reports, 6, 36390.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Cox, G., & Wright, G. D. (2013). Intrinsic antibiotic resistance: Mechanisms, origins, challenges and solutions. International Journal of Medical Microbiology, 303, 287–292.PubMedCrossRefPubMedCentralGoogle Scholar
  8. D’Costa, V. M., McGrann, K. M., Hughes, D. W., & Wright, G. D. (2006). Sampling the antibiotic resistome. Science, 311, 374–377.PubMedCrossRefPubMedCentralGoogle Scholar
  9. D’Costa, V. M., Griffiths, E., & Wright, G. D. (2007). Expanding the soil antibiotic resistome: Exploring environmental diversity. Current Opinion in Microbiology, 10, 481–489.Google Scholar
  10. Davies, J. (2006). Are antibiotics naturally antibiotics? Journal of Industrial Microbiology & Biotechnology, 33, 496–499.CrossRefGoogle Scholar
  11. Davies, J., & Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews, 74, 417–433.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Donato, J. J., Moe, L. A., Converse, B. J., Smart, K. D., Berklein, F. C., McManus, P. S., & Handelsman, J. (2010). Metagenomic analysis of apple orchard soil reveals antibiotic resistance genes encoding predicted bifunctional proteins. Applied and Environmental Microbiology, 76, 4396–4401.PubMedPubMedCentralCrossRefGoogle Scholar
  13. dos Santos, D. F., Istvan, P., Noronha, E. F., Quirino, B. F., & Kruger, R. H. (2015). New dioxygenase from metagenomic library from Brazilian soil: Insights into antibiotic resistance and bioremediation. Biotechnology Letters, 37, 1809–1817.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Forsberg, K. J., Patel, S., Gibson, M. K., Lauber, C. L., Knight, R., Fierer, N., & Dantas, G. (2014). Bacterial phylogeny structures soil resistomes across habitats. Nature, 509, 612–616.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Gaze, W. H., Krone, S. M., Larsson, D. G. J., Li, X.-Z., Robinson, J. A., Simonet, P., Smalla, K., Timinouni, M., Topp, E., Wellington, E. M., Wright, G. D., & Zhu, Y. G. (2013). Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerging Infectious Diseases, 19, e120871.PubMedCentralCrossRefGoogle Scholar
  16. Gillings, M. R. (2014). Integrons: Past, present, and future. Microbiology and Molecular Biology Reviews, 78, 257–277.PubMedCrossRefPubMedCentralGoogle Scholar
  17. Hamidian, M., Holt, K. E., & Hall, R. M. (2015). Genomic resistance island AGI1 carrying a complex class 1integron in a multiply antibiotic-resistant ST25 Acinetobacter baumannii isolate. The Journal of Antimicrobial Chemotherapy, 70, 2519–2523.PubMedCrossRefPubMedCentralGoogle Scholar
  18. Hug, L. A., Baker, B. J., Anantharaman, K., Brown, C. T., Probst, A. J., Castelle, C. J., Butterfield, C. N., Hernsdorf, A. W., Amano, Y., Ise, K., Suzuki, Y., Dudek, N., Relman, D. A., Finstad, K. M., Amundson, R., Thomas, B. C., & Banfield, J. F. (2016). A new view of the tree of life. Nature Microbiology, 1, 1–6.CrossRefGoogle Scholar
  19. Inglis, D. O., Binkley, J., Skrzypek, M. S., Arnaud, M. B., Cerqueira, G. C., Shah, P., Wymore, F., Wortman, J. R., & Sherlock, G. (2013). Comprehensive annotation of secondary metabolite biosynthetic genes and gene clusters of Aspergillus nidulans, A. fumigatus, A. niger and A. oryzae. BMC Microbiology, 13, 91.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Jones, C., & Stanley, J. (1992). Salmonella plasmids of the pre-antibiotic era. Journal of General Microbiology, 138, 189–197.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Katz, L., & Baltz, R. H. (2016). Natural product discovery: Past, present, and future. Journal of Industrial Microbiology & Biotechnology, 43, 155–176.CrossRefGoogle Scholar
  22. Kim, H. J., Jeong, Y. S., Jung, W. K., Kim, S. K., Lee, H. W., Kahng, H. Y., Kim, J., & Kim, H. (2015). Characterization of novel family IV esterase and family I.3 lipase from an oil-polluted mud flat metagenome. Molecular Biotechnology, 57, 781–792.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Lewis, K. (2013). Platforms for antibiotic discovery. Nature Reviews Drug Discovery, 12, 371.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Li, X., Rui, J., Xiong, J., Li, J., He, Z., Zhou, J., Yannarell, A. C., & Mackie, R. I. (2014). Functional potential of soil microbial communities in the maize rhizosphere. PLoS One, 9, e112609.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Li, L. G., Xia, Y., & Zhang, T. (2016). Co-occurrence of antibiotic and metal resistance genes revealed incomplete genome collection. The ISME Journal, 11, 651–662.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Linares, J. F., Gustafsson, I., Baquero, F., & Martinez, J. L. (2006). Antibiotics as intermicrobial signaling agents instead of weapons. Proceedings of the National Academy of Sciences, 103, 19484–19489.Google Scholar
  27. Ling, L. L., Schneider, T., Peoples, A. J., Spoering, A. L., Engels, I., Conlon, B. P., Mueller, A., Schaberle, T. F., Hughes, D. E., Epstein, S., Jones, M., Lazarides, L., Steadman, V. A., Cohen, D. R., Felix, C. R., Fetterman, K. A., Millett, W. P., Nitti, A. G., Zullo, A. M., Chen, C., & Lewis, K. (2015). A new antibiotic kills pathogens without detectable resistance. Nature, 517, 455–459.PubMedCrossRefPubMedCentralGoogle Scholar
  28. Liu, B., & Pop, M. (2008). ARDB—Antibiotic resistance genes database. Nucleic Acids Research, 37, D443–D447.Google Scholar
  29. Manaia, C. M. (2016). Assessing the risk of antibiotic resistance transmission from the environment to humans: Non-direct proportionality between abundance and risk. Trends in Microbiology, 25, 173–181.PubMedCrossRefPubMedCentralGoogle Scholar
  30. Marshall, C. G., Lessard, I. A., Park, I., & Wright, G. D. (1998). Glycopeptide antibiotic resistance genes in glycopeptide-producing organisms. Antimicrobial Agents and Chemotherapy, 42, 2215–2220.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Martinez, J. L. (2008). Antibiotics and antibiotic resistance genes in natural environments. Science, 321, 365–367.PubMedCrossRefPubMedCentralGoogle Scholar
  32. Martínez, J. L., Baquero, F., & Andersson, D. I. (2007). Predicting antibiotic resistance. Nature Reviews. Microbiology, 5, 958–965.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Martínez, J. L., Coque, T. M., & Baquero, F. (2015). What is a resistance gene? Ranking risk in resistomes. Nature Reviews. Microbiology, 13, 116–123.PubMedCrossRefPubMedCentralGoogle Scholar
  34. McArthur, A. G., Waglechner, N., Nizam, F., Yan, A., Azad, M. A., Baylay, A. J., Bhullar, K., Canova, M. J., De Pascale, G., Ejim, L., Kalan, L., King, A. M., Koteva, K., Morar, M., Mulvey, M. R., O’Brien, J. S., Pawlowski, A. C., Piddock, L. J., Spanogiannopoulos, P., Sutherland, A. D., Tang, I., Taylor, P. L., Thaker, M., Wang, W., Yan, M., Yu, T., & Wright, G. D. (2013). The comprehensive antibiotic resistance database. Antimicrobial Agents and Chemotherapy, 57, 3348–3357.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Misra, S., Pandey, S., Dixit, V., Mishra, S. K., Khan, M. H., Agarwal, L., & Chauhan, P. S. (2017). Soil microbiome for enhanced crop productivity. In V. Kalia, Y. Shouche, H. Purohit, & P. Rahi (Eds.), Mining of Microbial Wealth and MetaGenomics (pp. 227–247). Singapore: Springer.Google Scholar
  36. Miyazaki, K., & Kitahara, K. (2018). Functional metagenomic approach to identify overlooked antibiotic resistance mutations in bacterial rRNA. Scientific Reports, 8, 5179.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Nagayama, H., Sugawara, T., Endo, R., Ono, A., Kato, H., Ohtsubo, Y., Nagata, Y., & Tsuda, M. (2015). Isolation of oxygenase genes for indigo-forming activity from an artificially polluted soil metagenome by functional screening using Pseudomonas putida strains as hosts. Applied Microbiology and Biotechnology, 99, 4453–4470.PubMedCrossRefPubMedCentralGoogle Scholar
  38. Nesme, J., Cécillon, S., Delmont, T. O., Monier, J. M., Vogel, T. M., & Simonet, P. (2014). Large-scale metagenomic-based study of antibiotic resistance in the environment. Current Biology, 24, 1096–1100.PubMedCrossRefPubMedCentralGoogle Scholar
  39. O’Brien, J., & Wright, G. D. (2011). An ecological perspective of microbial secondary metabolism. Current Opinion in Biotechnology, 22, 552–558.PubMedCrossRefPubMedCentralGoogle Scholar
  40. O’Mahony, M. M., Henneberger, R., Selvin, J., Kennedy, J., Doohan, F., Marchesi, J. R., & Dobson, A. D. (2015). Inhibition of the growth of Bacillus subtilis DSM10 by a newly discovered antibacterial protein from the soil metagenome. Bioengineered, 6, 89–98.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Perry, J. A., & Wright, G. D. (2014). Forces shaping the antibiotic resistome. BioEssays, 36, 1179–1184.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Perry, J. A., Westman, E. L., & Wright, G. D. (2014). The antibiotic resistome: What’s new? Current Opinion in Microbiology, 21, 45–50.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Poirel, L., Rodriguez-Martinez, J. M., Mammeri, H., Liard, A., & Nordmann, P. (2005). Origin of plasmid-mediated quinolone resistance determinant Qnr A. Antimicrobial Agents and Chemotherapy, 49, 3523–3525.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Rodriguez, M. M., Power, P., Radice, M., Vay, C., Famiglietti, A., Galleni, M., Ayala, J. A., & Gutkind, G. (2004). Chromosome-encoded CTX-M-3 from Kluyvera ascorbata: A possible origin of plasmid-borne CTX-M-1-derived cefotaximases. Antimicrobial Agents and Chemotherapy, 48, 4895–4897.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Sharon, I., Kertesz, M., Hug, L. A., Pushkarev, D., Blauwkamp, T. A., Castelle, C. J., Amirebrahimi, M., Thomas, B. C., Burstein, D., Tringe, S. G., Williams, K. H., & Banfield, J. F. (2015). Accurate, multi-kb reads resolve complex populations and detect rare microorganisms. Genome Research, 25, 534–543.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Soucy, S. M., Huang, J., & Gogarten, J. P. (2015). Horizontal gene transfer: Building the web of life. Nature Reviews. Genetics, 16, 472–482.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Su, J., Zhang, F., Sun, W., Karuppiah, V., Zhang, G., Li, Z., & Jiang, Q. (2015). A new alkaline lipase obtained from the metagenome of marine sponge Ircinia sp. World Journal of Microbiology and Biotechnology, 31, 1093–1102.PubMedCrossRefPubMedCentralGoogle Scholar
  48. Surette, M. G. (2013). Concentration-dependent activity of antibiotics in natural environments. Frontiers in Microbiology, 4, 20.PubMedPubMedCentralGoogle Scholar
  49. Surette, M., & Wright, G. D. (2017). Lessons from the environmental antibiotic resistome. Annual Review of Microbiology, 71, 309–329.PubMedCrossRefPubMedCentralGoogle Scholar
  50. Torres-Cortes, G., Millan, V., Ramirez-Saad, H. C., Nisa-Martinez, R., Toro, N., & Martinez-Abarca, F. (2011). Characterization of novel antibiotic resistance genes identified by functional metagenomics on soil samples. Environmental Microbiology, 13, 1101–1114.PubMedCrossRefPubMedCentralGoogle Scholar
  51. Traxler, M. F., Watrous, J. D., Alexandrov, T., Dorrestein, P. C., & Kolter, R. (2013). Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. MBio, 4, e00459–e00413.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Truman, A. W., Kwun, M. J., Cheng, J., Yang, S. H., Suh, J. W., & Hong, H. J. (2014). Antibiotic resistance mechanisms inform discovery: Identification and characterization of a novel amycolatopsis strain producing ristocetin. Antimicrobial Agents and Chemotherapy, 58, 5687–5695.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Udikovic-Kolic, N., Wichmann, F., Broderick, N. A., & Handelsman, J. (2014). Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. PNAS, 111, 15202–15207.PubMedCrossRefPubMedCentralGoogle Scholar
  54. Waksman, S. A. (1941). Antagonistic relations of microorganisms. Bacteriological Reviews, 5, 231–291.PubMedPubMedCentralGoogle Scholar
  55. Waksman, S. A. (1945). Microbial antagonisms and antibiotic substances. New York: Commonwealth Fund.Google Scholar
  56. Walsh, F., & Duffy, B. (2013). The culturable soil antibiotic resistome: A community of multi-drug resistant bacteria. PLoS One, 8, e65567.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Wang, J. H., Lu, J., Zhang, Y. X., Wu, J., Luo, Y., & Liu, H. (2018). Metagenomic analysis of antibiotic resistance genes in coastal industrial mariculture systems. Bioresource Technology, 18, 30042–30047.Google Scholar
  58. Wright, G. D. (2007). The antibiotic resistome: The nexus of chemical and genetic diversity. Nature Reviews. Microbiology, 5, 175–186.PubMedCrossRefPubMedCentralGoogle Scholar
  59. Xiao, K. Q., Li, B., Ma, L., Bao, P., Zhou, X., Zhang, T., & Zhu, Y. G. (2016). Metagenomic profiles of antibiotic resistance genes in paddy soils from South China. FEMS Microbiology Ecology, 92, fiw023.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Sankalp Misra
    • 1
    • 2
  • Vijay Kant Dixit
    • 1
  • Swapnil Pandey
    • 1
    • 2
  • Shashank Kumar Mishra
    • 1
    • 2
  • Nikita Bisht
    • 1
    • 2
  • Puneet Singh Chauhan
    • 1
    • 2
    Email author
  1. 1.Microbial Technologies DivisionCSIR-National Botanical Research Institute (CSIR-NBRI)LucknowIndia
  2. 2.Academy of Scientific and Innovative Research (AcSIR)GhaziabadIndia

Personalised recommendations