Exploring the Potential for Actinobacteria as Defensive Symbionts in Fungus-Growing Termites

Microbial Ecology

Volumn 63, Issue 4, 2012, Pages 975-985

  Visser, Anna A ^a,d   Nobre, Tânia ^a   Currie, Cameron R ^b   Aanen, Duur K ^a   Poulsen, Michael ^b,c  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d Physiology Wageningen   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); FUNGI; ISOPTERA; MACROTERMITINAE; TERMITOMYCES;

EID: 84864327090     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-011-9987-4     Document Type: Article

References (53)

1. Aanen DK, de Fine Licht HH, Debets AJM, Kerstes NAG, Hoekstra RF, Boomsma JJ (2009) High symbiont relatedness stabilizes mutualistic cooperation in fungus-growing termites. Science 326: 1103-1106.
2. Aanen DK, Ros VID, de Fine Licht HH, Mitchell J, de Beer ZW, Slippers B, Rouland-Lefèvre C, Boomsma JJ (2007) Patterns of interaction specificity of fungus-growing termites and Termitomyces symbionts in South Africa. BMC Evol Biol 7: 115. doi: 10. 1186/1471-2148-7-115.
3. Boomsma JJ, Aanen DK (2009) Rethinking crop-disease management in fungus-growing ants. Proc Natl Acad Sci U S A 106: 17611-17612.
4. Cafaro MJ, Poulsen M, Little AE, Price SL, Gerardo NM, Wong B, Stuart AE, Larget B, Abbot P, Currie CR (2011) Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria. Proc R Soc B 278(1713): 1814-1822.
5. 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.
6. Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: 701-704.
7. Fields MW, Yan TF, Rhee SK, Carroll SL, Jardine PM, Watson DB, Criddle CS, Zhou JZ (2005) Impacts on microbial communities and cultivable isolates from groundwater contaminated with high levels of nitric acid-uranium waste. FEMS Microbiol Ecol 53: 417-428.
8. Fuller CA (2007) Fungistatic activity of freshly killed termite, Nasutitermes acajutlae, soldiers in the Caribbean. J Insect Sci 7: 1-8.
9. Goodfellow M, Williams ST (1983) Ecology of Actinomycetes. Annu Rev Microbiol 37: 189-216.
10. Grubbs KJ, Biedermann PH, Suen G, Adams SM, Moeller JA, Klassen JL, Goodwin LA, Woyke T, Munk AC, Bruce D, Detter C, Tapia R, Han CS, Currie CR (2011) Genome sequence of Streptomyces griseus strain XylebKG-1, an Ambrosia beetle-associated actinomycete. J Bacteriol 193: 2890-2891.
11. Guedegbe HJ, Miambi E, Pando A, Houngnandan P, Rouland-Lefèvre C (2009) Molecular diversity and host specificity of termite-associated Xylaria. Mycologia 101: 686-691.
12. Hsieh HM, Lin CR, Fang MJ, Rogers JD, Fournier J, Lechat C, Ju YM (2010) Phylogenetic status of Xylaria subgenus Pseudoxylaria among taxa of the subfamily Xylarioideae (Xylariaceae) and phylogeny of the taxa involved in the subfamily. Mol Phylogenet Evol 54: 957-969.
13. Hsu SC, Lockwood JL (1975) Powdered chitin as a selective medium for enumeration of actinomycetes in water and soil. Appl Microbiol 29: 422-426.
14. 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.
15. Jones JA (1990) Termites, soil fertility and carbon cycling in dry tropical Africa: a hypothesis. J Trop Ecol 6: 291-305.
16. Kaltenpoth M (2009) Actinobacteria as mutualists: general healthcare for insects? Trends Microbiol 17: 529-535.
17. Kaltenpoth M, Göttler W, Herzner G, Strohm E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15: 475-479.
18. Katoh H, Miura T, Maekawa K, Shinzato N, Matsumoto T (2002) Genetic variation of symbiotic fungi cultivated by the macrotermitine termite Odontotermes formosanus (Isoptera: Termitidae) in the Ryukyu Archipelago. Mol Ecol 11: 1565-1572.
19. Konaté S, Le Roux X, Verdier B, Lepage M (2003) Effect of underground fungus-growing termites on carbon dioxide emission at the point- and landscape-scales in an African savanna. Funct Ecol 17: 305-314.
20. 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.
21. Lamberty M, Zachary D, Lanot R, Bordereau C, Robert A, Hoffmann JA, Bulet P (2001) Insect Immunity. Constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J Biol Chem 276: 4085-4092.
22. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115-175.
23. Lepage M (1984) Distribution, density and evolution of Macrotermes bellicosus nests (Isoptera, Macrotermitinae) in the northeast of Ivory-Coast. J Anim Ecol 53: 107-117.
24. Leuthold RH, Badertscher S, Imboden H (1989) The inoculation of newly formed fungus comb with Termitomyces in Macrotermes colonies (Isoptera, Macrotermitinae). Insectes Sociaux 36: 328-338.
25. Mando A, Brussaard L (1999) Contribution of termites to the breakdown of straw under Sahelian conditions. Biol Fertil Soils 29: 332-334.
26. Moriya S, Inoue T, Ohkuma M, Yaovapa T, Johjima T, Suwanarit P, Sangwanit U, Vongkaluang C, Noparatnaraporn N, Kudo T (2005) Fungal community analysis of fungus gardens in termite nests. Microb Environ 20: 243-252.
27. Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Annu Rev Ecol Evol Syst 36: 563-595.
28. Nobre T, Kone NA, Konate S, Linsenmair KE, Aanen DK (2011) Dating the fungus-growing termites' mutualism shows a mixture between ancient codiversification and recent symbiont dispersal across divergent hosts. Mol Ecol 20: 2619-2627.
29. Nobre T, Rouland-Lefevre C, Aanen D (2011) Comparative biology of fungus cultivation in termites and ants. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, New York, p 576.
30. Oh DC, Poulsen M, Currie CR, Clardy J (2009) Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis. Nat Chem Biol 5: 391-393.
31. Poulsen M, Cafaro MJ, Erhardt DP, Little AEF, Gerardo NM, Tebbets B, Klein BS, Currie CR (2010) Variation in Pseudonocardia antibiotic defence helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants. Environ Microbiol Rep 2: 534-540.
32. Poulsen M, Currie CR (2010) Symbiont interactions in a tripartite mutualism: exploring the presence and impact of antagonism between two fungus-growing ant mutualists. PLoS One 5: e8748.
33. Poulsen M, Erhardt DP, Molinaro DJ, Lin TL, Currie CR (2007) Antagonistic bacterial interactions help shape host-symbiont dynamics within the fungus-growing ant-microbe mutualism. PLoS One 2: e960.
34. Riesenfeld CS, Schloss PD, Handelsman J (2004) Metagenomics: genomic analysis of microbial communities. Annu Rev Genet 38: 525-552.
35. Rogers JD (2000) Thoughts and musings on tropical Xylariaceae. Mycol Res 104: 1412-1420.
36. Rogers JD, Ju YM, Lehmann J (2005) Some Xylaria species on termite nests. Mycologia 97: 914-923.
37. Saitou N, Nei M (1987) The neighbor-joining method-a new method for reconstructing phylogenetic tress. Mol Biol Evol 4: 406-425.
38. Sands WA (1960) The initiation of fungus comb construction in laboratory colonies of Ancistrotermes guineensis (Silvestri). Insectes Sociaux 7: 251-259.
39. Sands WA (1969) The association of termites and fungi. In: Krishna K, Weesner FM (eds) Biology of termites. Vol. 1. Academic, New York, pp 495-524.
40. Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR (2008) Bacterial protection of beetle-fungus mutualism. Science 322: 63.
41. Sen R, Ishak HD, Estrada D, Dowd SE, Hong EK, Mueller UG (2009) Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci U S A 106: 17805-17810.
42. Shinzato N, Muramatsu M, Watanabe Y, Matsui T (2005) Termite-regulated fungal monoculture in fungus combs of a macrotermitine termite Odontotermes formosanus. Zool Sci 22: 917-922.
43. Staley JT (2006) The bacterial species dilemma and the genomic-phylogenetic species concept. Phil Trans R Soc B 361: 1899-1909.
44. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) Mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
45. Thomas RJ (1987) Distribution of Termitomyces Heim and other fungi in the nests and major workers of Macrotermes bellicosus (Smeathman) in Nigeria. Soil Biol Biochem 19: 329-333.
46. van Valen L (1973) A new evolutionary law. Evol Theory 1: 1-30.
47. Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of 'unculturable' bacteria. FEMS Microbiol Lett 309: 1574-6968.
48. Visser AA (2011) On the ecology and evolution of microorganisms associated with fungus-growing termites. PhD-thesis. university of Wageningen, 176 pp.
49. Visser AA, Kooij P, Debets AJM, Kuyper TW, Aanen DK (2011) Pseudoxylaria as stowaway of the fungus-growing termite nest: interaction asymmetry between Pseudoxylaria, Termitomyces and free-living relatives. Fungal Ecol 4: 322-332.
50. Visser AA, Ros VID, de Beer ZW, Debets AJM, Hartog E, Kuyper TW, Læssøe T, Slippers B, Aanen DK (2009) Levels of specificity of Xylaria species associated with fungus-growing termites: a phylogenetic approach. Mol Ecol 18: 553-567.
51. Waksman SA, Schatz A (1945) Strain specificity and production of antibiotic substances. VI. Strain variation and production of streptothricin by Actinomyces lavendulae. Proc Natl Acad Sci U S A 31: 208-214.
52. Waksman SA, Schatz AR, Reynolds DM (2010) Production of antibiotic substances by Actinomycetes. Ann N Y Acad Sci 1213: 112-124.
53. Wood TG, Thomas RJ (1989) The mutualistic association between Macrotermitinae and Termitomyces. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic, London, pp 69-92.