Abstract
Termites are usually associated with the decomposition of dead wood, although the diets of many species encompass other resources such as cactus, humus, feces, carcasses and lichens. Some components of their diets, however, may be associated with non-nutritional functions. The termite Constrictotermes cyphergaster has a varied diet, with dead wood being the main item consumed, but with lichens as secondary resources. The question concerning why lichens are consumed appears complicated, and needs careful study in a step-wise analysis. The present study was designed to examine and understand the effects of usnic acid, a secondary lichen metabolite, on the growth of bacteria associated with the gut microbiota of C. cyphergaster. Our results showed significant control of termite gut bacteria by usnic acid as compared with a treatment without it. Thus usnic acid appears to help the termite, possibly by controlling gut microbiota and avoiding diseases associated with entomopathogenic bacteria.
Similar content being viewed by others
Data Availability
Not applicable.
Code Availability
Not applicable.
References
Arango RA, Carlson CM, Currie CR et al (2016) Antimicrobial activity of actinobacteria isolated from the guts of subterranean termites. Environ Entomol 45:1415–1423. https://doi.org/10.1093/ee/nvw126
Araújo J (1998) In: Melo IS, Azevedo J (eds) Estratégias para isolamento seletivo de actinobactérias. Embrapa-CNPMA, Jaguariúna, pp 352–367
Araújo KD et al (2005) Analysis of meteorological conditions in São João do Cariri in thesemi-arid region of Paraíba. J Department Geosci 14:2
Araújo DA, H et al (2018) Toxicity of usnic acid from Cladonia substellata (lichen) to embryos and adults of Biomphalaria glabrata. Acta Trop v 179:39–43
Araújo KD, de Andrade AP, Raposo RWC et al (2010) Analysis of the weather conditions of São João do Cariri in the semi-arid region of Paraiba. Geogr (Londrina) 14:61–72. https://doi.org/10.5433/2447-1747.2005v14n1p61
Asahina Y, Shibata S (1954) Chemistry of Lichen Substances. Japan Society for Promotion of Science, Tokyo
Asplund J, Wardle DA (2013) The impact of secondary compounds and functional characteristics on lichen palatability and decomposition. J Ecol 101:689–700. https://doi.org/10.1111/1365-2745.12075
Barbosa M, De Lima I, Lima J et al (2007) Vegetation and Flora in Cariri Paraibano. Oecologia Brasiliensis 11:313–322. https://doi.org/10.4257/oeco.2007.1103.01
Barbosa-Silva AM, Silva AC, Pereira ECG et al (2019) Richness of Lichens consumed by Constrictotermes cyphergaster in the Semi-arid Region of Brazil. Sociobiology 66:154–160. https://doi.org/10.13102/sociobiology.v66i1.3665
Barbosa-Silva AM, Vasconcellos A (2019) Consumption rate of lichens by Constrictotermes cyphergaster (Isoptera): Effects of C, N, and P contents and ratios. Insects. https://doi.org/10.3390/insects10010023
Bourguignon T, Lo N, Dietrich C et al (2018) Rampant host switching shaped the Termite gut Microbiome. Curr Biol 28:649–654e2. https://doi.org/10.1016/j.cub.2018.01.035
Breznak JA (1982) Intestinal microbiota of Termites and other Xylophagous Insects. Annu Rev Microbiol 36:323–323. https://doi.org/10.1146/annurev.mi.36.100182.001543
Brune A (2013) The prokaryotes: Prokaryotic biology and symbiotic associations. In Symbiotic Associations Between Termites and Prokaryotes (pp. 545–570). https://doi.org/10.1007/978-3-642-30194-0
Brune A (2014) Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12:168–180. https://doi.org/10.1038/nrmicro3182
Brune A, Dietrich C (2015) The gut microbiota of Termites: digesting the diversity in the light of Ecology and Evolution. Annu Rev Microbiol 69:150720190645000. https://doi.org/10.1146/annurev-micro-092412-155715
Cetin H, Tufan-Cetin O, Turk AO et al (2008) Insecticidal activity of major lichen compounds, (-)- and (+)-usnic acid, against the larvae of house mosquito, Culex pipiens L. Parasitol Res 102:1277–1279. https://doi.org/10.1007/s00436-008-0905-8
Cocchietto M, Skert N, Nimis P, Sava G (2002) A review on usnic acid, an interesting natural compound. Naturwissenschaften 89:137–146. https://doi.org/10.1007/s00114-002-0305-3
Collins NM (1979) Observations on the foraging activity of Hospitalitermes umbrinus (haviland), (Isoptera: Termitidae) in the Gunong Mulu National Park, Sarawak. Ecol Entomol 4:231–238. https://doi.org/10.1111/j.1365-2311.1979.tb00580.x
Cos P, Vlietinck AJ, Berghe D, Vanden, Maes L (2006) Anti-infective potential of natural products: how to develop a stronger in vitro “proof-of-concept. J Ethnopharmacol 106:290–302. https://doi.org/10.1016/j.jep.2006.04.003
Edith MM, Nancy LMB, Zipporah LO et al (2016) Isolation and characterization of some gut microbial symbionts from fungus-cultivating termites (macrotermes and Odontotermes spp). Afr J Microbiol Res 10:994–1004. https://doi.org/10.5897/ajmr2016.8060
Eutick ML, O’Brien RW, Slaytor M (1978) Bacteria from the gut of australian termites. Appl Environ Microbiol 35:823–828. https://doi.org/10.1128/aem.35.5.823-828.1978
Falcão EPdS, Da Silva NH, De Gusmão NB et al (2002) Atividade antimicrobiana de compostos fenólicos do líquen Heterodermia leucomela (L.) Poelt. Acta Farm Bonaer 21:43–49
Fox J, Sanford W (2019) An R Companion to Applied Regression
Francolini I, Norris P, Piozzi A et al (2004) Usnic Acid, a natural Antimicrobial Agent able to inhibit bacterial biofilm formation on Polymer Surfaces. Antimicrob Agents Chemother 48:4360–4365. https://doi.org/10.1128/AAC.48.11.4360-4365.2004
Gupta VK, Verma S, Gupta S et al (2012) Membrane-damaging potential of natural L-(-)-usnic acid in Staphylococcus aureus. Eur J Clin Microbiol Infect Dis 31:3375–3383. https://doi.org/10.1007/s10096-012-1706-7
Hiraishi A (1992) Direct automated sequencing of 16S rDNA amplified by polymerase chain reaction from bacterial culture without DNA purification. Lett Appl Microbiol 15:210–213
König H (2006) Bacillus species in the intestine of termites and other soil invertebrates. J Appl Microbiol 101:620–627. https://doi.org/10.1111/j.1365-2672.2006.02914.x
Lawrey JD Lichen Secondary Compounds: Evidence for a Correspondence between Antiherbivore and Antimicrobial Function Author (s):, James D (1989). Lawrey Published by: American Bryological and Lichenological Society Lichen Secondary Compounds: Evidence for a Correspon. The Bryologist, 92(3), 326–328
Luzina OA, Salakhutdinov NF (2016) Biological activity of usnic acid and its derivatives: part 1. Activity against unicellular organisms. Russ J Bioorganic Chem 42:115–132. https://doi.org/10.1134/S1068162016020084
Martins MCB, Silva MC, Silva LRS et al (2014) Usnic acid potassium salt: an alternative for the control of Biomphalaria glabrata (say, 1818). PLoS ONE 9:1–6. https://doi.org/10.1371/journal.pone.0111102
Martins MCB, Lopes RS, Barbosa PS et al (2018) Effects of Usnic, Barbatic and Fumarprotocetraric acids on survival of Nasutitermes corniger (Isoptera: Termitidae: Nasutitermitinae). Sociobiology 65:79–87. https://doi.org/10.13102/sociobiology.v65i1.1840
Mikaelyan A, Meuser K, Brune A (2017) Microenvironmental heterogeneity of gut compartments drives bacterial community structure in wood- and humus-feeding higher termites. FEMS Microbiol Ecol 93:1–13. https://doi.org/10.1093/femsec/fiw210
Menezes L, Alvarez TM, Persinoti GF, Franco JP, Squina F, Moreira EA, Arab A (2018) Food Storage by the Savanna Termite Cornitermes cumulans (Syntermitinae): a strategy to Improve Hemicellulose Digestibility? Microb Ecol 76(2):492–505. https://doi.org/10.1007/s00248-017-1128-2
Mikaelyan A, Dietrich C, Köhler T, Poulsen M, Sillam-Dussès D, Brune A (2015) Diet is the primary determinant of bacterial community structure in the guts of higher termites. Mol Ecol 24(20):5284–5295. https://doi.org/10.1111/mec.13376
Moura FMS, Vasconcellos A, Araújo VFP, Bandeira AG (2006) Seasonality in foraging behaviour of Constrictotermes cyphergaster (Termitidae, Nasutitermitinae) in the caatinga of northeastern Brazil. Insectes Soc 53:472–479. https://doi.org/10.1007/s00040-005-0899-0
Moura FMDS, Vasconcellos A, De Araújo VPP, Bandeira AG (2008) Consumption of Vegetal Organic Matter by Constrictotermes cyphergaster (Isoptera, Termitidae, Nasutitermitinae) in an area of Caatinga, northeastern Brazil. Sociobiology 51:181–189
Odabasoglu F, Cakir A, Suleyman H, Aslan A, Bayir Y et al (2006) Gastroprotective and antioxidant effects of usnic acid on indomethacin-indiced gastric ulcer in rats. J Ethnopharmacol 103:59–65
Ohkuma M, Brune A (2010) Diversity, structure, and evolution of the Termite Gut Microbial Community. Biology of Termites: a modern synthesis. Springer Netherlands, Dordrecht, pp 413–438
Pourramezan Z, Ghezelbash GR, Romani B et al (2012) Screening and identification of newly isolated cellulose-degrading bacteria from the gut of xylophagous termite Microcerotermes diversus (Silvestri). Microbiol (Russian Fed 81:736–742. https://doi.org/10.1134/S0026261712060124
Ribeiro SM, Pereira EC, Gusmão NB, Falcão EP, Da Silva NH (2006) Produção de metabólitos bioativos pelo líquen Cladonia substellata Vainio. Acta Bot Brasilica 20(2):265–272. https://doi.org/10.1590/S0102-33062006000200003
Sahib K, Kularatne NS, Kumar S, Karunaratne V (2008) Effect of (+)-usnic acid on the shot-hole borer (Xyleborus fornicatus Eichh.) Of tea. J Natl Sci Found Sri Lanka 36:335–336. https://doi.org/10.4038/jnsfsr.v36i4.274
Sanchez-Contreras M, Vlisidou I (2008) The diversity of insect-bacteria interactions and its applications for disease control. Biotechnol Genet Eng Rev 25:203–244. https://doi.org/10.5661/bger-25-203
Smith AC, Hussey MA (2005) Gram stain protocols. Am Soc Microbiol 1:14
Spribille T, Tuovinen V, Resl P et al (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Sci (80-) 353:488–492. https://doi.org/10.1126/science.aaf8287
Suzuki MT, Giovannoni SJ (1996) Bias caused by template annealing in the ampli¢cation of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62:625–630
Upadhyay V, Demmer U, Warkentin E et al (2012) Structure and catalytic mechanism of N5, N10- methenyl-tetrahydromethanopterin cyclohydrolase. Biochemistry 51:8435–8443. https://doi.org/10.1021/bi300777k
Funding
Received from the Brazilian National Research Council – CNPq and MHO received scholarships from the Coordination for the Improvement of Higher Education Personnel – CAPES, FAPESQ/PELD 23/2020.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics Approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
de Oliveira, M.H., Lacerda-Rolim, M.d.S., Barbosa-Silva, A.M. et al. Inhibitory effect of usnic acid on the gut microbiota of the termite Constrictotermes cyphergaster. Symbiosis 89, 329–335 (2023). https://doi.org/10.1007/s13199-023-00912-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-023-00912-0