Skip to main content
SpringerLink
Log in

Exploration of Soil Resistome Through a Metagenomic Approach

  • Chapter
  • First Online:
Antibacterial Drug Discovery to Combat MDR

  • 948 Accesses

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bengtsson-Palme, J., & Larsson, D. G. J. (2015). Antibiotic resistance genes in the environment: Prioritizing risks. Nature Reviews. Microbiology, 13, 396.

    Article  CAS  PubMed  Google Scholar 

  • Bérdy, J. (2005). Bioactive microbial metabolites. The Journal of Antibiotics, 58, 1–26.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cox, G., & Wright, G. D. (2013). Intrinsic antibiotic resistance: Mechanisms, origins, challenges and solutions. International Journal of Medical Microbiology, 303, 287–292.

    Article  CAS  PubMed  Google Scholar 

  • D’Costa, V. M., McGrann, K. M., Hughes, D. W., & Wright, G. D. (2006). Sampling the antibiotic resistome. Science, 311, 374–377.

    Article  PubMed  Google Scholar 

  • 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 

  • Davies, J. (2006). Are antibiotics naturally antibiotics? Journal of Industrial Microbiology & Biotechnology, 33, 496–499.

    Article  CAS  Google Scholar 

  • Davies, J., & Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews, 74, 417–433.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed Central  Google Scholar 

  • Gillings, M. R. (2014). Integrons: Past, present, and future. Microbiology and Molecular Biology Reviews, 78, 257–277.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones, C., & Stanley, J. (1992). Salmonella plasmids of the pre-antibiotic era. Journal of General Microbiology, 138, 189–197.

    Article  CAS  PubMed  Google Scholar 

  • Katz, L., & Baltz, R. H. (2016). Natural product discovery: Past, present, and future. Journal of Industrial Microbiology & Biotechnology, 43, 155–176.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Lewis, K. (2013). Platforms for antibiotic discovery. Nature Reviews Drug Discovery, 12, 371.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, B., & Pop, M. (2008). ARDB—Antibiotic resistance genes database. Nucleic Acids Research, 37, D443–D447.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez, J. L. (2008). Antibiotics and antibiotic resistance genes in natural environments. Science, 321, 365–367.

    Article  CAS  PubMed  Google Scholar 

  • Martínez, J. L., Baquero, F., & Andersson, D. I. (2007). Predicting antibiotic resistance. Nature Reviews. Microbiology, 5, 958–965.

    Article  PubMed  CAS  Google Scholar 

  • Martínez, J. L., Coque, T. M., & Baquero, F. (2015). What is a resistance gene? Ranking risk in resistomes. Nature Reviews. Microbiology, 13, 116–123.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Miyazaki, K., & Kitahara, K. (2018). Functional metagenomic approach to identify overlooked antibiotic resistance mutations in bacterial rRNA. Scientific Reports, 8, 5179.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • O’Brien, J., & Wright, G. D. (2011). An ecological perspective of microbial secondary metabolism. Current Opinion in Biotechnology, 22, 552–558.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perry, J. A., & Wright, G. D. (2014). Forces shaping the antibiotic resistome. BioEssays, 36, 1179–1184.

    Article  PubMed  Google Scholar 

  • Perry, J. A., Westman, E. L., & Wright, G. D. (2014). The antibiotic resistome: What’s new? Current Opinion in Microbiology, 21, 45–50.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soucy, S. M., Huang, J., & Gogarten, J. P. (2015). Horizontal gene transfer: Building the web of life. Nature Reviews. Genetics, 16, 472–482.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Surette, M. G. (2013). Concentration-dependent activity of antibiotics in natural environments. Frontiers in Microbiology, 4, 20.

    PubMed  PubMed Central  Google Scholar 

  • Surette, M., & Wright, G. D. (2017). Lessons from the environmental antibiotic resistome. Annual Review of Microbiology, 71, 309–329.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waksman, S. A. (1941). Antagonistic relations of microorganisms. Bacteriological Reviews, 5, 231–291.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waksman, S. A. (1945). Microbial antagonisms and antibiotic substances. New York: Commonwealth Fund.

    Google Scholar 

  • Walsh, F., & Duffy, B. (2013). The culturable soil antibiotic resistome: A community of multi-drug resistant bacteria. PLoS One, 8, e65567.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Wright, G. D. (2007). The antibiotic resistome: The nexus of chemical and genetic diversity. Nature Reviews. Microbiology, 5, 175–186.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Microbial Technologies Division, CSIR-National Botanical Research Institute (CSIR-NBRI), Lucknow, Uttar Pradesh, India

    Sankalp Misra, Vijay Kant Dixit, Swapnil Pandey, Shashank Kumar Mishra, Nikita Bisht & Puneet Singh Chauhan

  2. Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, Uttar Pradesh, India

    Sankalp Misra, Swapnil Pandey, Shashank Kumar Mishra, Nikita Bisht & Puneet Singh Chauhan

Authors
  1. Sankalp Misra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vijay Kant Dixit
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Swapnil Pandey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shashank Kumar Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nikita Bisht
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Puneet Singh Chauhan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Puneet Singh Chauhan .

Editor information

Editors and Affiliations

  1. Agricultural Microbiology, Faculty of Agricultural Sciences, Aligarh Muslim University, Aligarh, Uttar Pradesh, India

    Iqbal Ahmad

  2. Institute of Ophthalmology, JN Medical College, Aligarh Muslim University, Aligarh, Uttar Pradesh, India

    Shamim Ahmad

  3. School of Medicine, Texas Tech University Health Sciences Center, Lubbock, TX, USA

    Kendra P. Rumbaugh

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Misra, S., Dixit, V.K., Pandey, S., Mishra, S.K., Bisht, N., Chauhan, P.S. (2019). Exploration of Soil Resistome Through a Metagenomic Approach. In: Ahmad, I., Ahmad, S., Rumbaugh, K. (eds) Antibacterial Drug Discovery to Combat MDR. Springer, Singapore. https://doi.org/10.1007/978-981-13-9871-1_15

Download citation

Publish with us

Policies and ethics

Search

Navigation