Research article

Diversity and antimicrobial activity of the tropical ant-derived actinomycetes isolated from Thailand

  • Received: 02 November 2023 Revised: 30 December 2023 Accepted: 15 January 2024 Published: 22 January 2024
  • Antibiotic resistance is one of the most important global healthcare challenges and is responsible for the mortality of millions of people worldwide every year. It is a crisis attributed to misuse of antibiotics and a lack of new drug development. Actinomycetes constitute a group of Gram-positive bacteria known for their distinctive high guanine-cytosine (G+C) content in their genomic DNA. These microorganisms are widely recognized for their capability to generate a wide range of secondary metabolites with diverse biological activities. These versatile microorganisms are ubiquitous in diverse ecosystems, including soil, freshwater, marine sediments, and within the bodies of insects. A recent study has demonstrated that social insects, such as ants, host a diverse array of these bacteria. In this study, we involved the isolation and characterization of a total of 72 actinomycete strains obtained from 18 distinct ant species collected from various regions across Thailand. Utilizing 16S rRNA gene analysis, these isolated actinomycetes were classified into four distinct genera: Amycolatopsis (2 isolates), Micromonospora (1 isolate), Nocardia (8 isolates), and Streptomyces (61 isolates). Among the Streptomyces strains, 23 isolates exhibited antimicrobial activity against a panel of Gram-positive bacteria, including Bacillus subtilis ATCC 6633, Staphylococcus epidermidis ATCC 12228, Staphylococcus aureus ATCC 25923, Kocuria rhizophila ATCC 9341, and Methicillin-resistant Staphylococcus aureus (MRSA) DMST 20646. Additionally, two isolates displayed antifungal activity against Candida albicans TISTR 5554. Based on 16S rRNA gene sequence similarity studies, these two isolates, ODS25 and ODS28, were demonstrated to be closely related to Streptomyces lusitanus NBRC 13464T (98.07%) and Streptomyces haliclonae DSM 41970T (97.28%), respectively. The level of 16S rRNA gene sequence similarity below 98.65% cutoff indicates its potential as a novel actinomycete species. These findings underscore the potential of actinomycetes sourced from ants as a valuable reservoir of novel antimicrobials.

    Citation: Tuangrat Tunvongvinis, Weeyawat Jaitrong, Yudthana Samung, Somboon Tanasupawat, Wongsakorn Phongsopitanun. Diversity and antimicrobial activity of the tropical ant-derived actinomycetes isolated from Thailand[J]. AIMS Microbiology, 2024, 10(1): 68-82. doi: 10.3934/microbiol.2024005

    Related Papers:

  • Antibiotic resistance is one of the most important global healthcare challenges and is responsible for the mortality of millions of people worldwide every year. It is a crisis attributed to misuse of antibiotics and a lack of new drug development. Actinomycetes constitute a group of Gram-positive bacteria known for their distinctive high guanine-cytosine (G+C) content in their genomic DNA. These microorganisms are widely recognized for their capability to generate a wide range of secondary metabolites with diverse biological activities. These versatile microorganisms are ubiquitous in diverse ecosystems, including soil, freshwater, marine sediments, and within the bodies of insects. A recent study has demonstrated that social insects, such as ants, host a diverse array of these bacteria. In this study, we involved the isolation and characterization of a total of 72 actinomycete strains obtained from 18 distinct ant species collected from various regions across Thailand. Utilizing 16S rRNA gene analysis, these isolated actinomycetes were classified into four distinct genera: Amycolatopsis (2 isolates), Micromonospora (1 isolate), Nocardia (8 isolates), and Streptomyces (61 isolates). Among the Streptomyces strains, 23 isolates exhibited antimicrobial activity against a panel of Gram-positive bacteria, including Bacillus subtilis ATCC 6633, Staphylococcus epidermidis ATCC 12228, Staphylococcus aureus ATCC 25923, Kocuria rhizophila ATCC 9341, and Methicillin-resistant Staphylococcus aureus (MRSA) DMST 20646. Additionally, two isolates displayed antifungal activity against Candida albicans TISTR 5554. Based on 16S rRNA gene sequence similarity studies, these two isolates, ODS25 and ODS28, were demonstrated to be closely related to Streptomyces lusitanus NBRC 13464T (98.07%) and Streptomyces haliclonae DSM 41970T (97.28%), respectively. The level of 16S rRNA gene sequence similarity below 98.65% cutoff indicates its potential as a novel actinomycete species. These findings underscore the potential of actinomycetes sourced from ants as a valuable reservoir of novel antimicrobials.



    加载中

    Acknowledgments



    This work was supported by the 90th Anniversary of Chulalongkorn University Scholarship under the Ratchadaphisek, Somphot Fund. We thank the 100th Anniversary Chulalongkorn University Fund for Doctoral Scholarship, Graduated School, Chulalongkorn University to TT and the Pharmaceutical Research Instrument Center, Faculty of Pharmaceutical Sciences, Chulalongkorn University, for providing research facilities.

    Conflict of interest



    The authors declare no conflicts of interest.

    Author contributions:



    TT performed screening, isolation, genotypic and phenotypic characterization, identification, and manuscript writing. WJ and YS collected and identified the ant samples. ST and WP conducted and advised all experiments.

    [1] Bérdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65: 385-395. https://doi.org/10.1038/ja.2012.27
    [2] Paradkar A (2013) Clavulanic acid production by Streptomyces clavuligerus: biogenesis, regulation and strain improvement. J Antibiot 66: 411-420. https://doi.org/10.1038/ja.2013.26
    [3] Ghoname RM, Ghozlan HA, Sabry SAEF (2022) Novel research on Rapamycin analogue production by Streptomyces sp. strain RHS5. J Adv Biomed Pharm Sci 5: 88-95. https://doi.org/10.1186%2Fs40643-022-00554-y
    [4] Cragg GM, Pezzuto JM (2016) Natural products as a vital source for the discovery of cancer chemotherapeutic and chemopreventive agents. Med Princ Pract 25: 41-59. https://doi.org/10.1159/000443404
    [5] Hassan SS, Shaikh AL (2017) Marine actinobacteria as a drug treasure house. Biomed Pharmacother 87: 46-57. https://doi.org/10.1016/j.biopha.2016.12.086
    [6] Global Antimicrobial Resistance and Use Surveillance System (GLASS) Report: 2021: from Organization WH, 2021. Available from: https://www.who.int/publications/i/item/9789240027336
    [7] Tackling drug-resistant infections globally: Final report and recommendations by Jim O'Neill: from Government of the United Kingdom 2016, 19 May 2016. Available from: https://apo.org.au/node/63983
    [8] Kumar Y (2019) Antimicrobial Resistance-A Global Threat. London: EBook. https://www.intechopen.com/books/6978
    [9] Tiwari K, Gupta RK (2012) Rare actinomycetes: a potential storehouse for novel antibiotics. Crit Rev Biotechnol 32: 108-132. https://doi.org/10.3109/07388551.2011.562482
    [10] Donadio S, Maffioli S, Monciardini P, et al. (2010) Antibiotic discovery in the twenty-first century: current trends and future perspectives. J Antibiot 63: 423-430. https://doi.org/10.1038/ja.2010.62
    [11] Challinor VL, Bode HB (2015) Bioactive natural products from novel microbial sources. Ann N Y Acad Sci 1354: 82-97. https://doi.org/10.1111/nyas.12954
    [12] Ratcliffe NA, Mello CB, Garcia ES, et al. (2011) Insect natural products and processes: new treatments for human disease. Insect Biochem Mol Biol 41: 747-769. https://doi.org/10.1016/j.ibmb.2011.05.007
    [13] Berasategui A, Shukla S, Salem H, et al. (2016) Potential applications of insect symbionts in biotechnology. Appl Microbiol Biotechnol 100: 1567-1577. https://doi.org/10.1007/s00253-015-7186-9
    [14] Wu Q, Patočka J, Kuča K (2018) Insect antimicrobial peptides, a mini review. Toxins 10: 461. https://doi.org/10.3390/toxins10110461
    [15] Chevrette MG, Carlson CM, Ortega HE, et al. (2019) The antimicrobial potential of Streptomyces from insect microbiomes. Nat Commun 10: 1-11. https://doi.org/10.1038/s41467-019-08438-0
    [16] Bailey IW (1920) Some relations between ants and fungi. Ecology 1: 174-189. https://doi.org/10.2307/1929134
    [17] Van Arnam EB, Currie CR, Clardy J (2018) Defense contracts: molecular protection in insect-microbe symbioses. Chem Soc Rev 47: 1638-1651. https://doi.org/10.1039/C7CS00340D
    [18] Barka EA, Vatsa P, Sanchez L, et al. (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol 80: 1-43. https://doi.org/10.1128/mmbr.00019-15
    [19] Oh DC, Scott JJ, Currie CR, et al. (2009) Mycangimycin, a polyene peroxide from a mutualist Streptomyces sp. Org Lett 11: 633-636. https://doi.org/10.1021/ol802709x
    [20] Wang Z, Yu Z, Zhao J, et al. (2020) Community composition, antifungal activity and chemical analyses of ant-derived actinobacteria. Front Microbiol 11: 201. https://doi.org/10.3389/fmicb.2020.00201
    [21] Hayakawa M, Nonomura H (1987) Humic acid-vitamin agar, a new medium for the selective isolation of soil actinomycetes. J Ferment Technol 65: 501-509. https://doi.org/10.1016/0385-6380(87)90108-7
    [22] Küster E, Williams S (1964) Selection of media for isolation of streptomycetes. Nature 202: 928-929. https://doi.org/10.1038/202928a0
    [23] Inahashi Y, Matsumoto A, Ōmura S, et al. (2011) Streptosporangium oxazolinicum sp. nov., a novel endophytic actinomycete producing new antitrypanosomal antibiotics, spoxazomicins. J Antibiot 64: 297-302. https://doi.org/10.1038/ja.2011.18
    [24] Rao NSS (1995) Soil microorganisms and plant growth.Science Publishers, Inc, India: Book. https://www.cabidigitallibrary.org/
    [25] Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16: 313-340. https://doi.org/10.1099/00207713-16-3-313
    [26] Raeder U, Broda P (1985) Rapid preparation of DNA from filamentous fungi. Lett Appl Microbiol 1: 17-20. https://doi.org/10.1111/j.1472-765X.1985.tb01479.x
    [27] Suriyachadkun C, Chunhametha S, Thawai C, et al. (2009) Planotetraspora thailandica sp. nov., isolated from soil in Thailand. Int J Syst Evol Microbiol 59: 992-997. https://doi.org/10.1099/ijs.0.003228-0
    [28] Lane D (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematics. Nucleic acid techniques in bacterial systematic. New York: John Wiley and Sons 115-175.
    [29] Yoon SH, Ha SM, Kwon S, et al. (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67: 1613-1617. https://doi.org/10.1099%2Fijsem.0.001755
    [30] Kumar S, Stecher G, Li M, et al. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35: 1547-1549. https://doi.org/10.1093%2Fmolbev%2Fmsy096
    [31] Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368-376. https://doi.org/10.1007/BF01734359
    [32] Mearns-Spragg A, Bregu M, Boyd K, et al. (1998) Cross-species induction and enhancement of antimicrobial activity produced by epibiotic bacteria from marine algae and invertebrates, after exposure to terrestrial bacteria. Lett Appl Microbiol 27: 142-146. https://doi.org/10.1046/j.1472-765x.1998.00416.x
    [33] Esnard J, Potter TL, Zuckerman BM (1995) Streptomyces costaricanus sp. nov., isolated from nematode-suppressive soil. Int J Syst Bacteriol 45: 775-779. https://doi.org/10.1099/00207713-45-4-775
    [34] Ge M, Cai X, Wang D, et al. (2023) Efficacy of Streptomyces murinus JKTJ-3 in suppression of Pythium damping-off of watermelon. Microorganisms 11: 1360. https://doi.org/10.3390/microorganisms11061360
    [35] Samuels LD (1964) Actinomycin and its effects: Influence on an effector pathway for hormonal control. N Engl J Med 271: 1301-1308. https://doi.org/10.1056/NEJM196412102712408
    [36] Waksman SA, Katz E, Vining LC (1958) Nomenclature of the actinomycins. Proc Natl Acad Sci USA 44: 602-612. https://doi.org/10.1073/pnas.44.6.602
    [37] Alam K, Mazumder A, Sikdar S, et al. (2022) Streptomyces: The biofactory of secondary metabolites. Front Microbiol 13: 968053. https://doi.org/10.3389/fmicb.2022.968053
    [38] Avendano C, Menéndez JC (2008) Anticancer drugs acting via radical species, photosensitizers and photodynamic therapy of cancer. Anticancer Agents Med Chem : 93-138. http://dx.doi.org/10.1016/B978-0-444-52824-7.00004-4
    [39] Shetty PR, Buddana SK, Tatipamula VB, et al. (2014) Production of polypeptide antibiotic from Streptomyces parvulus and its antibacterial activity. Braz J Microbiol 45: 303-312. https://doi.org/10.1590/S1517-83822014005000022
    [40] Merkel O, Wacht N, Sifft E, et al. (2012) Actinomycin D induces p53-independent cell death and prolongs survival in high-risk chronic lymphocytic leukemia. Leukemia 26: 2508-2516. https://doi.org/10.1038/leu.2012.147
    [41] Somphong A, Poengsungnoen V, Buaruang K, et al. (2023) The lichen-derived Streptomyces isolated from Pyxine cocoes produces the antibiotic with potent antimicrobial and antitumor activities. Sci Asia 49: 328-336. http://dx.doi.org/10.2306/scienceasia1513-1874.2023.025
    [42] Chandrakar S, Gupta AK (2019) Actinomycin-producing endophytic Streptomyces parvulus associated with root of aloe vera and optimization of conditions for antibiotic production. Probiotics Antimicrob Proteins 11: 1055-1069. https://doi.org/10.1007/s12602-018-9451-6
    [43] Kim M, Oh HS, Park SC, et al. (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64: 346-351. https://doi.org/10.1099/ijs.0.059774-0
    [44] Mueller UG, Dash D, Rabeling C, et al. (2008) Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution 62: 2894-2912. https://doi.org/10.1111/j.1558-5646.2008.00501.x
    [45] Seipke RF, Barke J, Ruiz-Gonzalez MX, et al. (2012) Fungus-growing Allomerus ants are associated with antibiotic-producing actinobacteria. Antonie Van Leeuwenhoek 101: 443-447. https://doi.org/10.1007/s10482-011-9621-y
    [46] Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58: 1-26. https://doi.org/10.1038/ja.2005.1
    [47] Hanshew AS, McDonald BR, Díaz Díaz C, et al. (2015) Characterization of actinobacteria associated with three ant–plant mutualisms. Microb Ecol 69: 192-203. https://doi.org/10.1007/s00248-014-0469-3
    [48] Zucchi TD, Guidolin AS, Cônsoli FL (2011) Isolation and characterization of actinobacteria ectosymbionts from Acromyrmex subterraneus brunneus (Hymenoptera, Formicidae). Microbiol Res 166: 68-76. https://doi.org/10.1016/j.micres.2010.01.009
    [49] Haeder S, Wirth R, Herz H (2009) Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc Ntl cd Sci USA 106: 4742-4746. https://doi.org/10.1073/pnas.0812082106
    [50] Zakalyukina YV, Osterman IA, Wolf J, et al. (2022) Amycolatopsis camponoti sp. nov., new tetracenomycin-producing actinomycete isolated from carpenter ant Camponotus vagus. Antonie Van Leeuwenhoek 115: 533-544. https://doi.org/10.1007/s10482-022-01716-w
    [51] Jiang S, Piao C, Yu Y, et al. (2018) Streptomyces capitiformicae sp. nov., a novel actinomycete producing angucyclinone antibiotics isolated from the head of Camponotus japonicus Mayr. Int J Syst Evol Microbiol 68: 118-124. https://doi.org/10.1099/ijsem.0.002468
    [52] Li Y, Ye L, Wang X, et al. (2016) Streptomyces camponoticapitis sp. nov., an actinomycete isolated from the head of an ant (Camponotus japonicus Mayr). Int J Syst Evol Microbiol 66: 3855-3859. https://doi.org/10.1099/ijsem.0.001276
    [53] Bai L, Liu C, Guo L, et al. (2016) Streptomyces formicae sp. nov., a novel actinomycete isolated from the head of Camponotus japonicus Mayr. Antonie Van Leeuwenhoek 109: 253-261. https://doi.org/10.1007/s10482-015-0628-7
    [54] Liu C, Guan X, Li Y, et al. (2016) Nocardia camponoti sp. nov., an actinomycete isolated from the head of an ant (Camponotus japonicas Mayr). Int J Syst Evol Microbiol 66: 1900-1905. https://doi.org/10.1099/ijsem.0.000963
    [55] Guo L, Liu C, Zhao J, et al. (2016) Promicromonospora alba sp. nov., an actinomycete isolated from the cuticle of Camponotus japonicas Mayr. Int J Syst Evol Microbiol 66: 1340-1345. https://doi.org/10.1099/ijsem.0.000885
    [56] Zakalyukina YV, Birykov MV, Lukianov DA, et al. (2019) Nybomycin-producing Streptomyces isolated from carpenter ant Camponotus vagus. Biochimie 160: 93-99. https://doi.org/10.1016/j.biochi.2019.02.010
    [57] Shin B, Park SH, Kim BY, et al. (2017) Deinococcucins A–D, aminoglycolipids from Deinococcus sp., a gut bacterium of the carpenter ant Camponotus japonicus. J Nat Prod 80: 2910-2916. https://doi.org/10.1021/acs.jnatprod.7b00426
    [58] Liu SH, Xu MD, Zhang H, et al. (2016) New cytotoxic spectinabilin derivative from ant-associated Streptomyces sp. 1H-GS5. J Antibiot 69: 128-131. https://doi.org/10.1038/ja.2015.99
    [59] Qin Z, Munnoch JT, Devine R, et al. (2017) Formicamycins, antibacterial polyketides produced by Streptomyces formicae isolated from African Tetraponera plant-ants. Chem Sci 8: 3218-3227. https://doi.org/10.1039/C6SC04265A
    [60] An JS, Lee JY, Kim E, et al. (2020) Formicolides A and B, antioxidative and antiangiogenic 20-membered macrolides from a wood ant gut bacterium. J Nat Prod 83: 2776-2784. https://doi.org/10.1021/acs.jnatprod.0c00772
    [61] Hong SH, Ban YH, Byun WS, et al. (2019) Camporidines A and B: antimetastatic and anti-inflammatory polyketide alkaloids from a gut bacterium of Camponotus kiusiuensis. J Nat Prod 82: 903-910. https://doi.org/10.1021/acs.jnatprod.8b01000
  • microbiol-10-01-005-s001.pdf
  • Reader Comments
  • © 2024 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(1135) PDF downloads(263) Cited by(0)

Article outline

Figures and Tables

Figures(4)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog