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Bacteria associated with leaf-cutter ants drive natural antibiotic resistance in soil bacteria

Published online by Cambridge University Press:  18 July 2022

Sophia Simon ,
Kelsey Chai ,
Matthew Drescher  and
Johel Chaves-Campos Open the ORCID record for Johel Chaves-Campos [Opens in a new window]
Sophia Simon
Affiliation:
Department of Biology, University of Pennsylvania, 433 S University Ave, Philadelphia, PA19104, USA
Kelsey Chai
Affiliation:
Department of Chemistry, Haverford College, 370 Lancaster Ave, Haverford, PA19041, USA
Matthew Drescher
Affiliation:
College of Veterinary Medicine, Cornell University, Ithaca, NY14853-6401, USA
Johel Chaves-Campos*
Affiliation:
Council on International Educational Exchange, Tropical Ecology and Conservation Study Abroad Program, Monteverde60109, Costa Rica Verto Education, Costa Rica Program, CATIE, Turrialba30501, Costa Rica
*
Author for correspondence: Johel Chaves-Campos, Email: [email protected]
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Abstract

Actinobacteria that live mutualistically with leaf-cutter ants secrete antibiotics that may induce antibiotic resistance in nearby soil bacteria. We tested for the first time whether soil bacteria near and inside Atta cephalotes nests in Costa Rica show higher levels of antibiotic resistance than bacteria collected farther away. We collected soil samples 0 m to 50 m away from ant nests and grew bacteria from them on agar with paper discs treated with antibiotics of common veterinary use. As a proxy for antibiotic resistance, we measured the distance from the edge of each disc to the closest bacterial colonies. In general, resistance to oxytetracycline increased with proximity to leaf-cutter ant nests. Antibiotic resistance to oxytetracycline was also higher in samples collected inside the nest than in samples from the nest mound; not all antibiotics demonstrated the same trend. A preliminary exploratory morphological analysis suggests bacterial communities between 0 m and 50 m from ant nests were similar in diversity and abundance, indicating the pattern of antibiotic resistance described above may not be caused by differences in community composition. We conclude that actinobacteria living mutualistically with A. cephalotes drive natural antibiotic resistance to tetracycline in proximal bacterial communities.

Keywords

antibiotic resistancemutualismactinobacteriaAtta cephalotesleaf-cutter ants
Type
Research Article
Information
Journal of Tropical Ecology , Volume 38 , Issue 6 , November 2022 , pp. 410 - 415
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Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Allen, HK, Donato, J, Wang, HH, Cloud-Hansen, KA, Davies, J and Handelsman, J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nature Reviews Microbiology 8, 251–259.CrossRefGoogle ScholarPubMed
Aminov, RI (2009) The role of antibiotics and antibiotic resistance in nature. Environmental Microbiology 11, 2970–2988.CrossRefGoogle ScholarPubMed
Balestra, GM and Misaghi, IJ (1997) Increasing the efficiency of the plate counting method for estimating bacterial diversity. Journal of Microbiological Methods 30, 111–117.CrossRefGoogle Scholar
Benson, HJ (2001). Microbiological Applications Lab Manual, Eighth Edition. New York: The McGraw-Hill Companies.Google Scholar
Bot, ANM, Ortius-Lechner, D, Finster, K, Maile, R and Boomsma, JJ (2002) Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insectes Sociaux 49, 363–370.CrossRefGoogle Scholar
Cafaro, MJ and Currie, CR (2005) Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants. Canadian Journal of Microbiology 51, 441–446.CrossRefGoogle ScholarPubMed
Cafaro, MJ, Poulsen, M, Little, AE, Price, SL, Gerardo, NM, Wong, B, Stuart, AE, Larget, B, Abbot, P and Currie, CR (2011) Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria. Proceedings of the Royal Society B: Biological Sciences 278, 1814–1822.CrossRefGoogle ScholarPubMed
Carr, G, Derbyshire, ER, Caldera, E, Currie, CR and Clardy, J (2012) Antibiotic and antimalarial quinones from fungus-growing ant associated Pseudonocardia sp. Journal of Natural Products 75, 1806–1809.CrossRefGoogle ScholarPubMed
Currie, CR, Scott, JA, Summerbell, RC and Malloch, D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398, 701–704.CrossRefGoogle Scholar
D’Costa, VM, McGrann, KM, Hughes, DW and Wright, GD (2006) Sampling the antibiotic resistome. Science 311, 374–377.CrossRefGoogle ScholarPubMed
Fahrenfeld, N, Knowlton, K, Krometis, LA, Hession, WC, Xia, K, Lipscomb, E, Libuit, K, Green, BL, and Pruden, A (2014) Effect of manure application on abundance of antibiotic resistance genes and their attenuation rates in soil: field-scale mass balance approach. Environmental Science and Technology 48, 2643–2650.CrossRefGoogle ScholarPubMed
Forsberg, KJ, Reyes, A, Wang, B, Selleck, EM, Sommer, MO and Dantas, G (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107–1111.CrossRefGoogle ScholarPubMed
Ghosh, S and Lapara, TM (2007) The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. The International Society for Microbial Ecology Journal 1, 191–203.Google ScholarPubMed
Gullberg, E, Cao, S, Berg, OG, Ilbäck, C, Sandegren, L, Hughes, D and Andersson, DI (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathogens 7. doi: 10.1371/journal.ppat.1002158 CrossRefGoogle ScholarPubMed
Haber, W (2000) Plants and vegetation. In Nadkarni NM & Wheelwright NT, eds., Monteverde, Ecology and Conservation of a Tropical Cloud Forest. New York City, USA: Oxford University Press, pp. 39–94.Google Scholar
Hart, AG and Ratnieks, FL (2001) Task partitioning, division of labour and nest compartmentalisation collectively isolate hazardous waste in the leafcutting ant Atta cephalotes. Behavioral Ecology and Sociobiology 49, 387–392.CrossRefGoogle Scholar
Herigstad, B, Hamilton, M and Heersink, J (2001) How to optimize the drop plate method for enumerating bacteria. Journal of Microbiological Methods 44, 121–129.CrossRefGoogle ScholarPubMed
Hughes, WOH, Bot, ANM and Boomsma, JJ (2010) Caste-specific expression of genetic variation in the size of antibiotic-producing glands of leaf-cutting ants. Proceedings of the Royal Society B: Biological Sciences 277, 609–615.CrossRefGoogle ScholarPubMed
Huys, G, D’Haene, K and Swings, J (2002) Influence of the culture medium on antibiotic susceptibility testing of food-associated lactic acid bacteria with the agar overlay disc diffusion method. Letters in Applied Microbiology 34, 402–406.CrossRefGoogle ScholarPubMed
Jaffe, K and Vilela, E (1989) On nest densities of the leaf-cutting ant Atta cephalotes in tropical primary forest. Biotropica 21, 234–236.CrossRefGoogle Scholar
Lee, J, Lee, SY, Han, S, Seong, D, Wijesinghe, RE, Kim, P, Jeon, M, Jung, HY and Kim, J (2020) Multi-directional morphological assessment of single bacterial colonies through non-invasive optical imaging. Annals of Biomedical Engineering 48, 3014–3023.CrossRefGoogle ScholarPubMed
Matarrita-Carranza, B, Moreira-Soto, RD, Murillo-Cruz, C, Mora, M, Currie, CR and Pinto-Tomas, AA (2017) Evidence for widespread associations between neotropical hymenopteran insects and Actinobacteria. Frontiers in Microbiology 8. doi: 10.3389/fmicb.2017.02016 CrossRefGoogle ScholarPubMed
Mueller, UG, Dash, D, Rabeling, C and Rodrigues, A (2008) Coevolution between attine ants and actinomycete bacteria: a reevaluation. The Society for the Study of Evolution 62, 2894–2912.Google Scholar
Mueller, UG, Rehner, SA and Schultz, TR (1998) The evolution of agriculture in ants. Science. doi: 10.1126/science.281.5385.2034 CrossRefGoogle ScholarPubMed
Nguyen, D, Joshi-Datar, A, Lepine, F, Bauerle, E, Olakanmi, O, Beer, K, McKay, G, Siehnel, R, Schafhauser, J, Wang, Y and Britigan, BE (2011) Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334, 982–986.CrossRefGoogle ScholarPubMed
Ortius-Lechner, D, Maile, R, David Morgan, E and Boomsma, JJ (2000) Metapleural gland secretion of the leaf-cutter ant Acromyrmex octospinosus: new compounds and their functional significance. Journal of Chemical Ecology 26, 1667–1683.CrossRefGoogle Scholar
Piddock, LJV (1990) Techniques used for the determination of antimicrobial resistance and sensitivity in bacteria. Journal of Applied Bacteriology 68, 307–318.CrossRefGoogle ScholarPubMed
Poulsen, M, Erhardt, DP, Molinaro, DJ, Lin, TL and Currie, CR (2007) Antagonistic bacterial interactions help shape host-symbiont dynamics within the fungus-growing ant-microbe mutualism. PLoS ONE 9. doi: 10.1371/journal.pone.0000960 Google Scholar
R Core Team (2020) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Schoenian, I, Spiteller, M, Ghaste, M, Wirth, R, Herz, H and Spiteller, D (2011) Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proceedings of the National Academy of Sciences of the United States of America 108, 1955–1960.CrossRefGoogle ScholarPubMed
Seipke, RF, Barke, J, Brearley, C, Hill, L, Yu, DW, Goss, RJ and Hutchings, MI (2011) A single streptomyces symbiont makes multiple antifungals to support the fungus farming ant acromyrmex octospinosus. PLoS ONE 6. doi: 10.1371/journal.pone.0022028 CrossRefGoogle ScholarPubMed
Sen, R, Ishak, HD, Estrada, D, Dowd, SE, Hong, E and Mueller, UG (2009) Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proceedings of the National Academy of Sciences 106, 17805–17810.CrossRefGoogle ScholarPubMed
Sousa, AM, Machado, I, Nicolau, A and Pereira, MO (2013) Improvements on colony morphology identification towards bacterial profiling. Journal of Microbiological Methods 95, 327–335.CrossRefGoogle ScholarPubMed
Spielmeyer, A (2018) Occurrence and fate of antibiotics in manure during manure treatments: a short review. Sustainable Chemistry and Pharmacy 9, 76–86.CrossRefGoogle Scholar
Swanson, AC, Schwendenmann, L, Allen, MF, Aronson, EL, Artavia-León, A, Dierick, D, Fernandez-Bou, AS, Harmon, TC, Murillo-Cruz, C, Oberbauer, SF, Pinto-Tomás, AA (2019) Welcome to the Atta world: a framework for understanding the effects of leaf-cutter ants on ecosystem functions. Functional Ecology 33, 1386–1399.CrossRefGoogle Scholar
Walsh, F and Duffy, B (2013) The culturable soil antibiotic resistome: a community of multi-drug resistant bacteria. PLoS ONE 8. doi: 10.1371/journal.pone.0065567 CrossRefGoogle ScholarPubMed
Wilson, EO (1983) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). Behavioral Ecology and Sociobiology 7, 157–165.CrossRefGoogle Scholar
Yek, SH and Mueller, UG (2011) The metapleural gland of ants. Biological Reviews 86, 774–791.CrossRefGoogle ScholarPubMed
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