Skip to main content

Advertisement

SpringerLink
Log in

Gut bacteria of animals living in polluted environments exhibit broad-spectrum antibacterial activities

  • Original Article
  • Published:
International Microbiology Aims and scope Submit manuscript

Abstract

Infectious diseases, in particular bacterial infections, are the leading cause of morbidity and mortality posing a global threat to human health. The emergence of antibiotic resistance has exacerbated the problem further. Hence, there is a need to search for novel sources of antibacterials. Herein, we explored gut bacteria of a variety of animals living in polluted environments for their antibacterial properties against multi-drug resistant pathogenic bacteria. A variety of species were procured including invertebrate species, Blaptica dubia (cockroach), Gromphadorhina portentosa (cockroach), Scylla serrata (crab), Grammostola rosea (tarantula), Scolopendra subspinipes (centipede) and vertebrate species including Varanus salvator (water monitor lizard), Malayopython reticulatus (python), Cuora amboinensis (tortoise), Oreochromis mossambicus (tilapia fish), Rattus rattus (rat), Gallus gallus domesticus (chicken) and Lithobates catesbeianus (frog). Gut bacteria of these animals were isolated and identified using microbiological, biochemical, analytical profiling index (API) and through molecluar identification using 16S rRNA sequencing. Bacterial conditioned media (CM) were prepared and tested against selected Gram-positive and Gram-negative pathogenic bacteria as well as human cells (HaCaT). The results revealed that CM exhibited significant broad-spectrum antibacterial activities. Upon heat inactivation, CM retained their antibacterial properties suggesting that this effect may be due to secondary metabolites or small peptides. CM showed minimal cytotoxicity against human cells. These findings suggest that gut bacteria of animals living in polluted environments produce broad-spectrum antibacterial molecule(s). The molecular identity of the active molecule(s) together with their mode of action is the subject of future studies which could lead to the rational development of novel antibacterial(s).

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdelmohsen UR, Bayer K, Hentschel U (2014) Diversity, abundance and natural products of marine sponge-associated actinomycetes. Nat Prod Rep 31:381–399

    Article  CAS  Google Scholar 

  • Adesanya, K., Adekoya, K. O., Ogunkanmi, L. & OBOH, B. 2017. Identification and characterization of Bacteria isolated from pipe-borne water samples in selected areas of Lagos using Api kits and RAPD-PCR

  • Akbar N, Siddiqui R, Iqbal M, Sagathevan K, Khan N (2018) Gut bacteria of cockroaches are a potential source of antibacterial compound (s). Lett Appl Microbiol 66:416–426

    Article  CAS  Google Scholar 

  • Akbar N, Siddiqui R, Sagathevan K, Khan NA (2019) Gut bacteria of animals/pests living in polluted environments are a potential source of antibacterials. Appl Microbiol Biotechnol 103:3955–3964

    Article  CAS  Google Scholar 

  • Ali SM, Siddiqui R, Ong S-K, Shah MR, Anwar A, Heard PJ, Khan NA (2017) Identification and characterization of antibacterial compound (s) of cockroaches (Periplaneta americana). Appl Microbiol Biotechnol 101:253–286

    Article  CAS  Google Scholar 

  • Anand P, Chellaram C, Shanthini F (2011) Isolation and screening of marine bacteria producing antibiotics against human pathogens. Int J Pharma Bio Sci 2:1–15

  • Anwar A, Masri A, Rao K, Rajendran K, Khan NA, Shah MR, Siddiqui R (2019) Antimicrobial activities of green synthesized gums-stabilized nanoparticles loaded with flavonoids. Sci Rep 9:3122

    Article  Google Scholar 

  • Ayuningrum D, Liu Y, Riyanti, Sibero MT, Kristiana R, Asagabaldan MA, Wuisan ZG, Trianto A, Radjasa OK, Sabdono A, Schäberle TF (2019) Tunicate-associated bacteria show a great potential for the discovery of antimicrobial compounds. PLoS One 14:e0213797

    Article  CAS  Google Scholar 

  • Bull AT, Stach JE (2007) Marine actinobacteria: new opportunities for natural product search and discovery. Trends Microbiol 15:491–499

    Article  CAS  Google Scholar 

  • Chevrette MG, Carlson CM, Ortega HE, Thomas C, Ananiev GE, Barns KJ, Book AJ, Cagnazzo J, Carlos C, Flanigan W (2019) The antimicrobial potential of Streptomyces from insect microbiomes. Nat Commun 10:516

    Article  CAS  Google Scholar 

  • Coates AR, Halls G, Hu Y (2011) Novel classes of antibiotics or more of the same? Br J Pharmacol 163:184–194

    Article  CAS  Google Scholar 

  • Elbendary AA, Hessain AM, El-Hariri MD, Seida AA, Moussa IM, Mubarak AS, Kabli SA, Hemeg HA, El Jakee JK (2018) Isolation of antimicrobial producing actinobacteria from soil samples. Saudi J Biol Sci 25:44–46

  • Ferris RA, Palmer BA, Borlee BR, Mccue PM (2017) Ability of chromogenic agar, MALDI-TOF, API 20E and 20 strep strips, and BBL crystal enteric and gram-positive identification kits to precisely identify common equine uterine pathogens. J Equine Vet Sci 57:35–40

    Article  Google Scholar 

  • Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74(8):2461–2470

    Article  CAS  Google Scholar 

  • Fredrickson AG, Stephanopoulos G (1981) Microbial competition. Science 213(4511):972–979

    Article  CAS  Google Scholar 

  • Garcia-Gonzalez E, Müller S, Ensle P, Süssmuth RD, Genersch E (2014) Elucidation of sevadicin, a novel non-ribosomal peptide secondary metabolite produced by the honey bee pathogenic bacterium . Environ Microbiol 16(5):1297–1309

  • Gislin D, Sudarsanam D, Raj GA, Baskar K (2018) Antibacterial activity of soil bacteria isolated from Kochi, India and their molecular identification. J Genet Eng Biotechnol 16:287–294

    Article  Google Scholar 

  • Hatha, A., Shubhankar Ghosh, A., Selvam, D., Neethu, C. & Saramma, A. 2014. Diversity and antimicrobial activity of lactic acid bacteria from the gut of marine fish Rastrelliger kanagurta against fish, shrimp and human pathogens

  • Hyronimus B, Le Marrec C, Urdaci MC (1998) Coagulin, a bacteriocin-like-inhibitory substance produced by Bacillus coagulans I. J Appl Microbiol 85(1):42–50

    Article  CAS  Google Scholar 

  • Iqbal J, Siddiqui R, Khan NA (2014) Acanthamoeba and bacteria produce antimicrobials to target their counterpart. Parasit Vectors 7:56–56

    Article  Google Scholar 

  • Jee Y, Carlson J, Rafai E, Musonda K, Huong TTG, Daza P, Sattayawuthipong W, Yoon T (2018) Antimicrobial resistance: a threat to global health. Lancet Infect Dis 18:939–940

    Article  Google Scholar 

  • Jeyamogan S, Khan NA, Siddiqui R (2017) Animals living in polluted environments are a potential source of anti-tumor molecule (s). Cancer Chemother Pharmacol 80:919–924

    Article  Google Scholar 

  • Khaled JM, Al-Mekhlafi FA, Mothana RA, Alharbi NS, Alzaharni KE, Sharafaddin AH, Kadaikunnan S, Alobaidi AS, Bayaqoob NI, Govindarajan M (2018) Brevibacillus laterosporus isolated from the digestive tract of honeybees has high antimicrobial activity and promotes growth and productivity of honeybee’s colonies. Environ Sci Pollut Res 25:10447–10455

  • Lau CH-F, Van Engelen K, Gordon S, Renaud J, Topp E (2017) Novel antibiotic resistance determinants from agricultural soil exposed to antibiotics widely used in human medicine and animal farming. Appl Environ Microbiol 83:e00989–e00917

    Article  CAS  Google Scholar 

  • Lee CR, Cho I, Jeong B, Lee S (2013) Strategies to minimize antibiotic resistance. Int J Environ Res Public Health 10(9):4274–4305

    Article  CAS  Google Scholar 

  • León-Palmero E, Joglar V, Álvarez PA, Martín-Platero A, Llamas I, Reche I (2018) Diversity and antimicrobial potential in sea anemone and holothurian microbiomes. Plos One 13 (5):e0196178

  • Liu Q, Ni X, Wang Q, Peng Z, Niu L, Xie M, Lin Y, Zhou Y, Sun H, Pan K (2018) Investigation of lactic acid bacteria isolated from giant panda feces for potential probiotics in vitro. Probiotics Antimicro 11(1):85–91

  • Masri A, Anwar A, Ahmed D, Siddiqui R, Raza Shah M, Khan N (2018) Silver nanoparticle conjugation-enhanced antibacterial efficacy of clinically approved drugs cephradine and vildagliptin. Antibiotics 7:100

    Article  CAS  Google Scholar 

  • Matobole R, Van Zyl L, Parker-Nance S, Davies-Coleman M, Trindade M (2017) Antibacterial activities of bacteria isolated from the marine sponges Isodictya compressa and Higginsia bidentifera collected from Algoa Bay, South Africa. Mar Drugs 15:47

  • Patil PB, Zeng Y, Coursey T, Houston P, Miller I, Chen S (2010) Isolation and characterization of a Nocardiopsis sp. from honeybee guts. FEMS Microbiol Lett 312(2):110–118

  • Pavunraj M, Ramasubbu G, Baskar K (2017) Leucas aspera (wild.) L.: antibacterial, antifungal and mosquitocidal activities. Trends Phytochem Res 1:135–142

  • Pidot SJ, Coyne S, Kloss F, Hertweck C (2014) Antibiotics from neglected bacterial sources. Int J Med Microbiol 304:14–22

    Article  CAS  Google Scholar 

  • Ranjan R, Jadeja V (2017) Isolation, characterization and chromatography based purification of antibacterial compound isolated from rare endophytic actinomycetes Micrococcus yunnanensis. J Pharm Anal 7:343–347

  • Siddiqui R, Jeyamogan S, Ali SM, Abbas F, Sagathevan K, Khan NA (2017) Crocodiles and alligators: Antiamoebic and antitumor compounds of crocodiles. Exp Parasitol 183:194–200

    Article  CAS  Google Scholar 

  • Spellberg B, Shlaes D (2014) Prioritized current unmet needs for antibacterial therapies. Clin Pharmacol Ther 96:151–153

    Article  CAS  Google Scholar 

  • World Health Organization (2018) The top 10 causes of death. https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death. Accessed 11 Jan 2019

  • Zheng W, Zhang Y, Lu HM, Li DT, Zhang ZL, Tang ZX, Shi LE (2015) Antimicrobial activity and safety evaluation of Enterococcus faecium KQ 2.6 isolated from peacock feces. BMC Biotechnol 15(1):30

    Article  Google Scholar 

  • Zipperer A, Konnerth MC, Laux C, Berscheid A, Janek D, Weidenmaier C, Burian M, Schilling NA, Slavetinsky C, Marschal M (2016) Human commensals producing a novel antibiotic impair pathogen colonization. Nature 535:511

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Sunway University, Malaysia and American University of Sharjah, UAE for supporting this work.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, School of Science and Technology, Sunway University, Bandar Sunway, 47500, Petaling Jaya, Selangor, Malaysia

    Noor Akbar & K. Sagathevan

  2. Department of Biology, Chemistry and Environmental Sciences, College of Arts and Sciences, American University of Sharjah, University City, 26666, Sharjah, United Arab Emirates

    Ruqaiyyah Siddiqui & Naveed Ahmed Khan

Authors
  1. Noor Akbar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruqaiyyah Siddiqui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Sagathevan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naveed Ahmed Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NA carried out all experiments under the supervision of KS, RS and NAK. KS and NA sourced the animals and carried out dissections. NA prepared the first draft of the manuscript. NAK and RS conceived the idea, obtained results and corrected the manuscript.

Corresponding author

Correspondence to Naveed Ahmed Khan.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval and consent to participate

This article does not contain any studies with human participants. The use of animals was approved by the Sunway University Research Ethics Committee, SUNREC042. We also confirm that all experiments were performed in accordance with applicable rules and regulations.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akbar, N., Siddiqui, R., Sagathevan, K. et al. Gut bacteria of animals living in polluted environments exhibit broad-spectrum antibacterial activities. Int Microbiol 23, 511–526 (2020). https://doi.org/10.1007/s10123-020-00123-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10123-020-00123-3

Keywords

Search

Navigation