Extended disease resistance emerging from the faecal nest of a subterranean termite

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1770, 2013, Pages

  Chouvenc, Thomas ^a   Efstathion, Caroline A ^a   Elliott, Monica L ^a   Su, Nan Yao ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Actinobacteria; Entomopathogens; Nesting behaviour; Symbiosis; Termites

Indexed keywords

EID: 84902649878     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.1885     Document Type: Article

References (65)

1. Rust MK, Su N-Y. 2012 Managing social insects of urban importance. Annu. Rev. Entomol. 57, 355-375. (doi:10.1146/annurevento-120710-100634)
2. Grassé P-P. 1982 Termitologia, vol. I. Paris, France: Masson.
3. Eggleton P. 2006 The termite gut habitat: its evolution and co-evolution. In Intestinal microorganisms of termites and other invertebrates (eds H König, A Varma), pp. 373-404. Berlin, Germany: Springer.
4. Wood TG. 1988 Termites and the soil environment. Biol. Fertil. Soils 6, 228-236. (doi:10.1007/BF00260819)
5. Chouvenc T, Elliott ML, Su N-Y. 2011 Rich microbial community associated with the nest material of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Fla. Entomol. 94, 115-116. (doi:10.1653/024.094.0117)
6. Schmid-Hempel P. 1998 Parasites in social insects. Princeton, NJ: Princeton University Press.
7. Chouvenc T, Su N-Y. 2010 Apparent synergy among defense mechanisms in subterranean termites (Rhinotermitidae) against epizootic events: Limits and potential for biological control. J. Econ. Entomol. 103, 1327-1337. (doi:10.1603/EC09407)
8. Rosengaus RB, Traniello JF, Bulmer MS. 2011 Ecology, behavior and evolution of disease resistance in termites. In Biology of termites: a modern synthesis (eds DE Bignell, Y Roisin, N Lo), pp. 165-192. New York, NY: Spinger.
9. Chouvenc T, Su N-Y, Robert A. 2009 Cellular encapsulation in the eastern subterranean termite, Reticulitermes flavipes (Isoptera), against infection by the entomopathogenic fungus Metarhizium anisopliae. J. Invertebr. Pathol. 101, 234-241. (doi:10.1016/j.jip.2009.05.008)
10. Bulmer MS, Lay F, Hamilton C. 2010 Adaptive evolution in subterranean termite antifungal peptides. Insect Mol. Biol. 19, 669-674. (doi:10.1111/j.1365-2583.2010.01023.x)
11. Traniello JFA, Rosengaus RB, Savoie K. 2002 The development of immunity in a social insect: evidence for group facilitation of disease resistance. Proc. Natl Acad. Sci. USA 99, 6838-6842. (doi:10.1073/pnas.102176599)
12. Yanagawa A, Shimizu S. 2007 Resistance of the termite Coptotermes formosanus Shiraki to Metarhizium anisopliae due to grooming. BioControl 52, 75-85. (doi:10.1007/s10526-006-9020-x)
13. Cremer S, Armitage SA, Schmid-Hempel P. 2007 Social immunity. Curr. Biol. 17, R693-R702. (doi:10.1016/j.cub.2007.06.008)
14. Chouvenc T, Su N-Y. 2012 When subterranean termites challenge the rules of fungal epizootics. PLoS ONE 7, e34484. (doi:10.1371/journal. pone.0034484)
15. Rosengaus RB, Lefebvre ML, Traniello JFA. 2000 Inhibition of fungal spore germination by Nasutitermes: evidence for a possible antiseptic role of soldier defensive secretions. J. Chem. Ecol. 26, 21-39. (doi:10.1023/A:1005481209579)
16. Rosengaus RB, Traniello JFA, Lefebvre ML, Maxmen AB. 2004 Fungistatic activity of the sternal gland secretion of the dampwood termite Zootermopsis angusticollis. Insect. Soc. 51, 259-264. (doi:10. 1007/s00040-004-0749-x)
17. Bulmer MS, Bachelet I, Raman R, Rosengaus RB, Sasisekharan R. 2009 Targeting an antimicrobial effector function in insect immunity as a pest control strategy. Proc. Natl Acad. Sci. USA 106, 12 652-12 657. (doi:10.1073/pnas.0904063106)
18. Chouvenc T, Su N-Y, Robert A. 2009 Inhibition of Metarhizium anisopliae in the alimentary tract of the eastern subterranean termite Reticulitermes flavipes. J. Invertebr. Pathol. 101, 130-136. (doi:10.1016/j.jip.2009.04.005)
19. Hamilton C, Lay F, Bulmer MS. 2011 Subterranean termite prophylactic secretions and external antifungal defenses. J. Insect. Physiol. 57, 1259-1266. (doi:10.1016/j.jinsphys.2011.05.016)
20. Chouvenc T, Efstathion CA, Elliott ML, Su N-Y. 2012 Resource competition between two fungal parasites in subterranean termites. Naturwissenschaften 99, 949-958. (doi:10.1007/s00114-012-0977-2)
21. Poulsen M, Little AEF, Currie CR. 2009 Fungusgrowing ant-microbe symbiosis: using microbes to defend beneficial associations within symbiotic communities. In Defensive mutualism in microbial symbiosis (eds JF White, MS Torres), pp. 149-166. Boca Raton, FL: CRC Press.
22. Caldera EJ, Poulsen M, Suen G, Currie CR. 2009 Insect symbioses: a case study of past, present, and future fungus-growing ant research*. Environ. Entomol. 38, 78-92. (doi:10.1603/022.038.0110)
23. Kaltenpoth M. 2009 Actinobacteria as mutualists: general healthcare for insects? Trends Microbiol. 17, 529-535. (doi:10.1016/j.tim.2009.09.006)
24. Currie CR, Scott JA, Summerbell RC, Malloch D. 1999 Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398, 701-704. (doi:10.1038/19519)
25. Currie CR, Wong B, Stuart AE, Schultz TR, Rehner SA, Mueller UG, Sung GH, Spatafora JW, Straus NA. 2003 Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299, 386-388. (doi:10.1126/science.1078155)
26. Haeder S, Wirth R, Herz H, Spiteller D. 2009 Candicidin-producing Streptomyces support leafcutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc. Natl Acad. Sci. USA 106, 4742-4746. (doi:10.1073/pnas. 0812082106)
27. Barke J et al. 2010 A mixed community of Actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol. 8, 109. (doi:10.1186/1741-7007-8-109)
28. Seipke RF, Barke J, Brearley C, Hill L, Douglas WY, Goss RJ, Hutchings MI. 2011 A single Streptomyces symbiont makes multiple antifungals to support the fungus farming ant Acromyrmex octospinosus. PLoS ONE 6, e22028. (doi:10.1371/journal.pone.0022028)
29. Schoenian I, Spiteller M, Ghaste M, Wirth R, Herz H, Spiteller D. 2011 Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc. Natl Acad. Sci. USA 108, 1955-1960. (doi:10.1073/pnas.1008441108)
30. Kaltenpoth M, Goettler W, Dale C, Stubblefield JW, Herzner G, Roeser-Mueller K, Strohm E. 2006 'Candidatus Streptomyces philanthi', an endosymbiotic Streptomycete in the antennae of Philanthus digger wasps. Int. J. Syst. Evol. Microbiol. 56, 1403-1411. (doi:10.1099/ijs.0.64117-0)
31. Kroiss J, Kaltenpoth M, Schneider B, Schwinger MG, Hertweck C, Maddula RK, Strohm E, Svatos A. 2010 Symbiotic Streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat. Chem. Biol. 6, 261-263. (doi:10.1038/ nchembio.331)
32. Poulsen M, Oh DC, Clardy J, Currie CR. 2011 Chemical analyses of wasp-associated Streptomyces bacteria reveal a prolific potential for natural products discovery. PLoS ONE 6, e16763. (doi:10. 1371/journal.pone.0016763)
33. Scott JJ, Ho DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR. 2008 Bacterial protection of beetle-fungus mutualism. Science 322, 63. (doi:10.1126/ science.1160423)
34. Hulcr J, Adams AS, Raffa K, Hofstetter RW, Klepzig KD, Currie CR. 2011 Presence and diversity of Streptomyces in Dendroctonus and sympatric bark beetle galleries across North America. Microb. Ecol. 61, 759-768. (doi:10.1007/s00248-010-9797-0)
35. Poulsen M. 2010 Biomedical exploitation of the fungus-growing ant symbiosis. Drug News Perspect. 23, 203-210. (doi:10.1358/dnp.2010.23.3.1489981)
36. Jouquet P, Traoré S, Choosai C, Hartmann C, Bignell DE. 2011 Influence of termites on ecosystem functioning. Ecosystem services provided by termites. Eur. J. Soil Biol. 47, 215-222. (doi:10.1016/j.ejsobi.2011.05.005)
37. Chouvenc T, Su N-Y, Grace JK. 2011 Fifty years of attempted biological control of termites: analysis of a failure. Biol. Control 59, 69-82. (doi:10.1016/j. biocontrol.2011.06.015)
38. Chouvenc T, Su N-Y, Robert A. 2009 Susceptibility of seven termite species (Isoptera) to the entomopathogenic fungus Metarhizium anisopliae. Sociobiology 54, 723-748.
39. Su N-Y, Scheffrahn RH. 1986 A method to access, trap, and monitor field populations of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in the urban environment. Sociobiology 12, 299-304.
40. Kaeberlein T, Lewis K, Epstein SS. 2002 Isolating 'uncultivable' microorganisms in pure culture in a simulated natural environment. Science 296, 1127-1129. (doi:10.1126/science.1070633)
41. Shlatter DA, Fubuh A, Xiao K, Hernandez D, Hobbie S, Kinkel L. 2009 Resource amendments influence density and competitive phenotypes of Streptomyces in soil. Microbiol. Ecol. 57, 413-420. (doi:10.1007/s00248-008-9433-4)
42. Levy SB, Marshall B. 2004 Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 10, S122-S129. (doi:10.1038/nm1145)
43. Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST. 1994 Bergey's manual of determinative bacteriology, 9th edn. Baltimore, MD: Williams and Wilkins.
44. Chouvenc T, Su N-Y, Elliott ML. 2008 Interaction between the subterranean termite Reticulitermes flavipes (Isoptera: Rhinotermitidae) and the entomopathogenic fungus Metarhizium anisopliae in foraging arenas. J. Econ. Entomol. 101, 885-893. (doi:10.1603/0022-0493(2008)101[885:IBTSTR]2.0.CO;2)
45. Waksman SA, Lechevalier HA. 1962 The Actinomycetes, vol. III. Antibiotics of Actinomycetes. Baltimore, MD: Williams & Wilkins.
46. Tamashiro M, Fujii JK, Lai P-Y. 1973 A simple method to observe, trap, and prepare large numbers of subterranean termites for laboratory and field experiments. Environ. Entomol. 2, 721-722.
47. Chouvenc T, Bardunias PM, Li HF, Elliott ML, Su N-Y. 2011 Planar arenas for use in laboratory bioassay studies of subterranean termites (Rhinotermitidae). Fla. Entomol. 94, 817-826. (doi:10.1653/024.094.0413)
48. Begon M, Harper JL, Townsend CR. 1996 Ecology. Individuals, populations and communities, 2nd edn. Oxford, UK: Blackwell.
49. Mattoso TC, Moreira DD, Samuels RI. 2012 Symbiotic bacteria on the cuticle of the leaf-cutting ant Acromyrmex subterraneus subterraneus protect workers from attack by entomopathogenic fungi. Biol. Lett. 8, 461-464. (doi:10.1098/rsbl.2011.0963)
50. de Souza DJ, Lenoir A, Kasuya MCM, Ribeiro MMR, Devers S, Couceiro JDC, Lucia TMCD. 2012 Ectosymbionts and immunity in the leaf-cutting ant Acromyrmex subterraneus subterraneus. Brain. Behav. Immun. 28, 182-187. (doi:10.1016/j.bbi.2012.11.014)
51. Dawkins R. 2004 Extended phenotype-but not too extended. A reply to Laland, Turner and Jablonka. Biol. Philos. 19, 377-396.
52. Bignell DE. 2000 Introduction to symbiosis. In Termites: evolution, sociality, symbiosis, ecology (eds T Abe, DE Bignell, M Higashi), pp. 189-208. Dordrecht, The Netherlands: Kluwer Academic Publishers.
53. Bignell DE. 2006 Termites as soil engineers and soil processors. In Intestinal microorganisms of termites and other invertebrates (eds H König, A Varma), pp. 183-220. Berlin, Germany: Springer.
54. Lo N, Eggleton P. 2011 Termite phylogenetics and co-cladogenesis with symbionts. In Biology of termites: a modern synthesis (eds DE Bignell, Y Roisin, N Lo), pp. 27-50. New York, NY: Spinger.
55. Oliver KM, Moran NA. 2009 Defensive symbionts in aphids and other insects. In Defensive mutualism in microbial symbiosis (eds JF White, MS Torres), pp. 129-148. Boca Raton, FL: CRC Press.
56. Cafaro MJ et al. 2011 Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria. Proc. R. Soc. B 278, 1814-1822. (doi:10.1098/rspb.2010.2118)
57. Caldera EJ, Currie CR. 2012 The population structure of antibiotic-producing bacterial symbionts of Apterostigma dentigerum ants: impacts of coevolution and multipartite symbiosis. Am. Nat. 180, 604-617. (doi:10.1086/667886)
58. Currie CR, Bot AN, Boomsma JJ. 2003 Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites. Oikos 101, 91-102. (doi:10.1034/j.1600-0706.2003.12036.x)
59. Currie CR, Poulsen M, Mendenhall J, Boomsma JJ, Billen J. 2006 Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311, 81-83. (doi:10.1126/science. 1119744)
60. Mueller UG. 2012 Symbiont recruitment versus antsymbiont co-evolution in the attine ant-microbe symbiosis. Curr. Opin. Microbiol. 15, 269-277. (doi:10.1016/j.mib.2012.03.001)
61. Kost C, Lakatos T, Böttcher I, Arendholz WR, Redenbach M, Wirth R. 2007 Non-specific association between filamentous bacteria and fungus-growing ants. Naturwissenschaften 94, 821-828. (doi:10.1007/s00114-007-0262-y)
62. Mueller UG, Dash D, Rabeling C, Rodrigues A. 2008 Coevolution between attine ants and Actinomycete bacteria: a reevaluation. Evolution 62, 2894-2912. (doi:10.1111/j.1558-5646.2008.00501.x)
63. Sen R, Ishak HD, Estrada D, Dowd SE, Hong E, Mueller UG. 2009 Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc. Natl Acad. Sci. USA 106, 17 805-17 810. (doi:10.1073/pnas.0904827106)
64. Mueller UG, Ishak H, Lee JC, Sen R, Gutell RR. 2010 Placement of attine ant-associated Pseudonocardia in a global Pseudonocardia phylogeny (Pseudonocardiaceae, Actinomycetales): a test of two symbiont-association models. Antonie van Leeuwenhoek 98, 195-212. (doi:10.1007/s10482-010-9427-3)
65. Husseneder C, Ho HY, Blackwell M. 2010 Comparison of the bacterial symbiont composition of the Formosan subterranean termite from its native and introduced range. Open Microbiol. J. 4, 53-66. (doi:10.2174/ 1874285801004010053)