Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1713, 2011, Pages 1814-1822

  Cafaro, Matías J ^a,b   Poulsen, Michael ^a   Little, Ainslie E F ^a,c   Price, Shauna L ^d   Gerardo, Nicole M ^e   Wong, Bess ^f,g   Stuart, Alison E ^h   Larget, Bret ^a,i   Abbot, Patrick ^j   Currie, Cameron R ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^c Quarles and Brady LLP   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e EMORY UNIVERSITY   (United States)

^f UNIVERSITY OF TORONTO   (Canada)

^g Sporometrics Inc   (Canada)

^h Calgary Board of Education   (Canada)

ⁱ University of Wisconsin Madison   (United States)

^j VANDERBILT UNIVERSITY   (United States)

more..

Author keywords

Fungus growing ants; Microbial interaction; Mutualism; Pseudonocardia; Symbiosis

Indexed keywords

BACTERIAL PROTEIN; ELONGATION FACTOR TU; RNA 16S;

ANT; ANTIBIOTICS; BIOASSAY; CHEMICAL ANALYSIS; EVOLUTIONARY BIOLOGY; FUNGUS; INHIBITION; MUTUALISM; PHYLOGENETICS; PHYLOGENY;

ACTINOMYCETALES; ANIMAL; ANT; ARTICLE; BIODIVERSITY; CLASSIFICATION; DNA SEQUENCE; EVOLUTION; GENETICS; HYPOCREALES; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; SPECIES DIFFERENCE; SYMBIOSIS;

ACTINOMYCETALES; ANIMALS; ANTS; BACTERIAL PROTEINS; BIODIVERSITY; BIOLOGICAL EVOLUTION; HYPOCREALES; PEPTIDE ELONGATION FACTOR TU; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS;

ACTINOBACTERIA; ATTINI; ESCOVOPSIS; FORMICIDAE; FUNGI; PSEUDONOCARDIA;

EID: 79955758518     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.2118     Document Type: Article

References (49)

1. Margulis, L. & Fester, R. 1991 Symbiosis as a source of evolutionary innovation, p 454. Cambridge, UK: MIT Press.
2. Moran, N. A. 2007 Symbiosis as an adaptive process and source of phenotypic complexity. Proc. Natl Acad. Sci. USA 104, 8627-8633. (doi:10.1073/pnas.0611659104)
3. Geurts, R., Fedorova, E. & Bisseling, T. 2005 Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr. Opin. Plant Biol. 8, 346-352. (doi:10.1016/j.pbi.2005.05.013)
4. Fraune, S. & Bosch, T. C. G. 2007 Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc. Natl Acad. Sci. USA 104, 13 146-13 151. (doi:10.1073/pnas.0703375104)
5. Nyholm, S. V., Stewart, J. J., Ruby, E. G. & McFall-Ngai, M. J. 2009 Recognition between symbiotic Vibrio fischeri and the hemocytes of Euprymna scolopes. Environ. Microbiol. 11, 483-493. (doi:10.1111/j.1462-2920.2008.01788.x)
6. Ridenhour, B. J. 2005 Identification of selective sources: partitioning selection based on interactions. Am. Nat. 166, 12-25. (doi:10.1086/430524)
7. Strauss, S. Y., Sahli, H. & Conner, J. K. 2005 Toward a more trait-centered to diffuse (co)evolution. New Phytol. 165, 81-90. (doi:10.1111/j.1469-8137.2004.01228.x)
8. Janzen, D. H. 1980 When is it coevolution? Evolution 34, 611-612. (doi:10.2307/2408229)
9. Mikheyev, A. S., Mueller, U. G. & Abbot, P. 2010 Comparative dating of attine ant and lepiotaceous cultivar phylogenies reveals coevolutionary synchrony and discord. Am. Nat. 175, 126-133. (doi:10.1086/652472)
10. Chapela, I. H., Rehner, S. A., Schultz, T. R. & Mueller, U. G. 1994 Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266, 1691-1694. (doi:10.1126/science.266.5191.1691)
11. Schultz, T. R. & Brady, S. 2008 Major evolutionary transitions in ant agriculture. Proc. Natl Acad. Sci. USA 105, 5435-5440. (doi:10.1073/pnas.0711024105)
12. Currie, C. R., Mueller, U. G. & Malloch, D. 1999 The agricultural pathology of ant fungus gardens. Proc. Natl Acad. Sci. USA 96, 7998-8002. (doi:10.1073/pnas.96.14.7998)
13. Currie, C. R., Wong, B., Stuart, A. E., Schultz, T. R., Rehner, S. A., Mueller, U. G., Sung, G.-H., Spatafora, J. W. & Straus, N. A. 2003 Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299, 386-388. (doi:10.1126/science.1078155)
14. Gerardo, N. M., Mueller, U. G. & Currie, C. R. 2006 Complex host-pathogen coevolution in the Apterostigma fungus-growing ant-microbe symbiosis. BMC Evol. Biol. 6, 88. (doi:10.1186/1471-2148-6-88)
15. Taerum, S. J., Cafaro, M. J., Little, A. E. F., Schultz, T. R. & Currie, C. R. 2007 Low host-pathogen specificity in the leaf-cutting ant-microbe symbiosis. Proc. R. Soc. B 274, 1971-1978. (doi:10.1098/rspb.2007.0431)
16. Gerardo, N. M. & Caldera, E. J. 2007 Labile associations between fungus-growing ant cultivars and their garden pathogens. Int. Soc. Micr. Ecol. J. 1, 373-384.
17. Currie, C. R. & Stuart, A. E. 2001 Weeding and grooming of pathogens in agriculture by ants. Proc. R. Soc. Lond. B 268, 1033-1039. (doi:10.1098/rspb.2001.1605)
18. Poulsen, M. & Currie, C. R. 2006 Complexity of insect-fungal associations: exploring the influence of microorganisms on attine ant-fungus symbiosis. In Insect symbiosis vol. 2, (eds K. Bourtzis & T. A. Miller), pp. 57-77. FL, USA: CRC.
19. Fernández-Marín, H., Zimmerman, J. K., Nash, D. R., Boomsma, J. J. & Wcislo, W. T. 2009 Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proc. R. Soc. B 276, 2263-2269. (doi:10.1098/rspb.2009.0184)
20. Currie, C. R., Scott, J. A., Summerbell, R. C. & Malloch, D. 1999 Fungus-growing ants use antibiotic producing bacteria to control garden parasites. Nature 398, 701-704. (doi:10.1038/19519)
21. Currie, C. R., Bot, A. N.M. & Boomsma, J. J. 2003 Experimental evidence of a tripartite mutualism: bacteria protect ant fungal gardens from specialized parasites. Oikos 101, 91-102. (doi:10.1034/j.1600-0706.2003.12036.x)
22. Poulsen, M., Cafaro, M. J., Erhardt, D. P., Little, A. E. F., Gerardo, N. M. & Currie, C. R. 2010 Variation in Pseudonocardia antibiotic defense governs parasiteinduced morbidity in Acromyrmex leaf-cutting ants. Environ. Microbiol. Rep. 2, 534-540. (doi:10.1111/j.1758-2229.2009.00098.x)
23. Currie, C. R., Poulsen, M., Mendenhall, J., Boomsma, J. J. & Billen, J. 2006 Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311, 81-83. (doi:10.1126/science.1119744)
24. Oh, D.-C., Poulsen, M., Currie, C. R. & Clardy, J. 2009 Dentigerumycin, the bacterially produced molecular mediator of a fungus-growing ant symbiosis. Nat. Chem. Biol. 5, 391-393. (doi:10.1038/nchembio.159)
25. Little, A. E. F. & Currie, C. R. 2008 Black yeast symbionts compromise the efficiency of antibiotic defences in fungus-growing ants. Ecology 89, 1216-1222. (doi:10.1890/07-0815.1)
26. Currie, C. R., Schultz, T. R. & Engel, M. In preparation. Presence of Actinobacteria on an attine ant in Dominican amber.
27. Cafaro, M. J. & Currie, C. R. 2005 Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants. Can. J. Microbiol. 51, 441-446. (doi:10.1139/w05-023)
28. Poulsen, M., Cafaro, M. J., Boomsma, J. J. & Currie, C. R. 2005 Specificity of the mutualistic association between actinomycete bacteria and two sympatric species of Acromyrmex leaf-cutting ants. Mol. Ecol. 14, 3597-3604. (doi:10.1111/j.1365-294X.2005.02695.x)
29. Mikheyev, A. S., Vo, T. & Mueller, U. G. 2008 Phylogeography of post-Pleistocene population expansion in a fungus-gardening ant and its microbial mutualists. Mol. Ecol. 17, 4480-4488. (doi:10.1111/j.1365-294X.2008.03940.x)
30. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmou-gin, F. & Higgins, D. G. 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24, 4876-4882. (doi:10.1093/nar/25.24.4876)
31. Maddison, D. R. & Maddison, W. P. 2005 MacClade 4.07 Mac OS X. Sunderland, MA: Sinauer Associates, Inc.
32. Huelsenbeck, J. P. & Ronquist, F. 2001 MRBAYES: Bayesian inference of phylogeny. Bioinformatics (Oxf.) 17, 754-755. (doi:10.1093/bioinformatics/17.8.754)
33. Sukumaran, J. & Holder, M. T. 2009. SumTrees: summarization of split support on phylogenetic trees, version 1.0.2. Part of the DendroPy phylogenetic computation library, version 2.6.1. See http://packages.python.org/DendroPy.
34. Zwickl, D. J. 2006 Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis, The University of Texas at Austin, TX, USA.
35. Haeder, S., Wirth, R., Herz, H. & Spiteller, D. 2009 Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc. Natl Acad. Sci. USA 106, 4742-4746. (doi:10.1073/pnas.0812082106)
36. Sen, R., Ishak, H. D., Estrada, D., Dowd, S. E., Hong, E. & Mueller, U. G. 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)
37. Barke, J., Seipke, R. F., Grüschow, S., Heavens, D., Drou, N., Bibb, M. J., Goss, R. J. M., Yu, D. W. & Hutchings, M. I. 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)
38. Tarkka, M. T. & Hampp, R. 2008 Secondary metabolites of soil streptomycetes in biotic interactions. In Soil biology: secondary metabolites in soil ecology (ed. P. Karlovsy), pp. 107-126. Heidelberg, Germany: Springer.
39. Strobel, G. A. 2002 Rainforest endophytes and bioactive products. Crit. Rev. Biotech. 22, 315-333. (doi:10.1080/07388550290789531)
40. Kost, C., Lakatos, T., Böttcher, I., Arendholz, W.-R., 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)
41. Mueller, U. G., 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)
42. Ciche, T. A. & Goffredi, S. K. 2007 General methods to investigate microbial synthesis. In Methods for general and molecular microbiology (eds C. A. Reddy, T. J. Beveridge, J. A. Breznak, G. M. Arzluf, T. M. Schmidt & L. R. Synder), 3rd edn, pp. 394-419. Washington, DC: ASM Press.
43. Caldera, E. J., Poulsen, M., Suen, G. & Currie, C. R. 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)
44. Van Borm, S., Billen, J. & Boomsma, J. J. 2002 The diversity of microorganisms associated with Acromyrmex leafcutter ants. BMC Evol. Biol. 2, 9. (doi:10.1186/1471-2148-2-9)
45. Pinto-Tomás, A. A., Anderson, M. A., Suen, G., Stevenson, D. M., Chu, F. S. T., Wallace Cleland, W., Weimer, P. J. & Currie, C. R. 2009 Symbiotic nitrogen fixation in the fungus gardens of leafcutter ants. Science 326, 1120-1123. (doi:10.1126/science.1173036)
46. Suen, G. et al. 2010 An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genet. 6, e1001129. (doi:10.1371/journal.pgen.1001129)
47. Zhang, M., Poulsen, M. & Currie, C. R. 2007 Symbiont recognition of mutualistic bacteria in Acromyrmex leafcutting ants. Int. Soc. Micr. Ecol. J. 1, 313-320.
48. Tanaka, Y. & Omura, S. 1987 Metabolism and products of actinomycetes: an introduction. Actinomycetologica 4, 13-14. (doi:10.3209/saj.4_13)
49. Kaltenpoth, M. 2009 Actinobacteria as mutualists: general healthcare for insects? Trends Microbiol. 17, 529-535. (doi:10.1016/j.tim.2009.09.006)