Placement of attine ant-associated Pseudonocardia in a global Pseudonocardia phylogeny (Pseudonocardiaceae, Actinomycetales): A test of two symbiont-association models

Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology

Volumn 98, Issue 2, 2010, Pages 195-212

  Mueller, Ulrich G ^a   Ishak, Heather ^a   Lee, Jung C ^a   Sen, Ruchira ^a   Gutell, Robin R ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Antibiotic; Attine ant microbe symbiosis; Mutualism; Secondary rRNA structure

Indexed keywords

RNA 16S;

ANT; BACTERIAL COLONIZATION; BACTERIAL TRANSMISSION; BACTERIUM ISOLATION; CLADISTICS; COMMENSAL; CONFERENCE PAPER; CONTROLLED STUDY; CULTURE MEDIUM; ESCOVOPSIS; FUNGUS; MICROBIAL COMMUNITY; MOLECULAR EVOLUTION; MOLECULAR MODEL; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PSEUDONOCARDIA; PSEUDONOCARDIACEAE; RNA ANALYSIS; RNA STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SYMBIONT; SYMBIOSIS; UNINDEXED SEQUENCE; ACTINOMYCETALES; ANIMAL; BIOLOGICAL MODEL; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY;

ACTINOMYCETALES; ANIMALS; ANTS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; SYMBIOSIS;

ACTINOMYCETALES; ATTINI; BACTERIA (MICROORGANISMS); ESCOVOPSIS; FORMICIDAE; FUNGI; PSEUDONOCARDIA; PSEUDONOCARDIACEAE;

EID: 77955553995     PISSN: 00036072     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10482-010-9427-3     Document Type: Conference Paper

References (48)

1. SG Acinas R Sarma-Rupavtarm V Klepac-Ceraj MF Polz 2005 PCR-induced sequence artifacts and bias: insights from comparison of two 16S rRNA clone libraries constructed from the same sample Appl Environ Microbiol 71 8966 8969 10.1128/AEM.71.12.8966-8969.2005 1:CAS:528:DC%2BD2MXhtlehur7K 16332901 (Pubitemid 41804041)
2. M Bacci SB Ribeiro MEF Casarotto FC Pagnocca 1995 Biopolymer-degrading bacteria from nests of the leaf-cutting ant Atta sexdens rubropilosa Braz J Med Biol Res 28 79 82
3. JJ Boomsma DK Aanen 2009 Rethinking crop-disease management in fungus-growing ants Proc Natl Acad Sci USA 106 17611 17612 10.1073/pnas. 0910004106 1:CAS:528:DC%2BD1MXhsVSjsL3K 19826091
4. MJ Cafaro CR Currie 2005 Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants Can J Microbiol 51 441 446 10.1139/w05-023 1:CAS:528:DC%2BD2MXhtFygsbvN 16121221 (Pubitemid 41641227)
5. EJ Caldera M Poulsen G Suen CR Currie 2009 Insect symbioses: a case study of past, present, and future fungus-growing ant research Environ Entomol 38 78 92 10.1603/022.038.0110 19791600
6. JJ Cannone S Subramanian MN Schnare JR Collett LM D'Souza Y Du B Feng N Lin LV Madabusi KM Müller N Pande Z Shang N Yu RR Gutell 2002 The comparative RNA Web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs BioMed Cen Bioinformatics 3 2 10.1186/1471-2105-3-2 (Pubitemid 38751202)
7. SC Carreiro FC Pagnocca OC Bueno M Bacci MJA Hebling OA da Silva 1997 Yeasts associated with the nests of the leaf-cutting ant Atta sexdens rubropilosa Forel, 1908 Antonie van Leeuwenhoek 71 243 248 10.1023/A: 1000182108648 1:STN:280:DyaK2s3ms1Witw%3D%3D 9111918 (Pubitemid 27136181)
8. CR Currie 2001 A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis Annu Rev Microbiol 55 357 380 10.1146/annurev.micro.55.1.357 1:CAS:528:DC%2BD3MXnslKjtL4%3D 11544360 (Pubitemid 32978110)
9. CR Currie UG Mueller D Malloch 1999 The agricultural pathology of ant fungus gardens Proc Natl Acad Sci USA 96 7998 8002 10.1073/pnas.96.14.7998 1:CAS:528:DyaK1MXltVOku70%3D 10393936 (Pubitemid 29328396)
10. CR Currie JA Scott RC Summerbell D Malloch 1999 Fungus-growing ants use antibiotic-producing bacteria to control garden parasites Nature 398 701 704 10.1038/19519 1:CAS:528:DyaK1MXivVegtLk%3D (Pubitemid 29197647)
11. CR Currie ANM Bot JJ Boomsma 2003 Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites Oikos 101 91 102 10.1034/j.1600-0706.2003.12036.x (Pubitemid 36614722)
12. CR Currie M Poulsen J Mendenhall JJ Boomsma J Billen 2006 Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants Science 311 81 83 10.1126/science.1119744 1:CAS:528:DC%2BD28Xht1egsw%3D%3D 16400148 (Pubitemid 43063062)
13. S Dattagupta I Schaperdoth A Montanari S Mariani N Kita JW Valley JL Macalady 2009 A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod Int Soc Microb Ecol 3 935 943 1:CAS:528: DC%2BD1MXovFOgu7g%3D
14. Diamond J (2006) Virus and the whale: exploring evolution in creatures small and large. National Science Teachers Association Press, Arlington, VA
15. H Fernández-Marín JK Zimmerman DR Nash JJ Boomsma WT Wcislo 2009 Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants Proc R Soc Lond B 276 2236 2269 10.1098/rspb.2009.0184
16. M Goodfellow ST Williams 1983 Ecology of actinomycetes Annu Rev Microbiol 37 189 216 10.1146/annurev.mi.37.100183.001201 1:STN:280:DyaL2c%2FltV2ltA%3D%3D 6357051
17. SJ Gould RC Lewontin 1979 The spandrels of San Marco and the Panglossian Paradigm: a critique of the Adaptationist Programme Proc R Soc Lond B 205 581 598 10.1098/rspb.1979.0086 1:STN:280:DyaL3c%2FnvFyrsw%3D%3D 42062
18. RR Gutell B Weiser CR Woese HF Noller 1985 Comparative anatomy of 16S-like ribosomal RNA Prog Nucl Acid Res Mol Biol 32 155 216 10.1016/S0079-6603(08)60348-7 1:CAS:528:DyaL28XmsVelsQ%3D%3D
19. RR Gutell A Power G Hertz E Putz G Stormo 1992 Identifying constraints on the higher-order structure of RNA: continued development and application of comparative sequence analysis methods Nucleic Acids Res 20 5785 5795 10.1093/nar/20.21.5785 1:CAS:528:DyaK3sXhvVWgtg%3D%3D 1454539
20. RR Gutell N Larsen CR Woese 1994 Lessons from an evolving ribosomal RNA: 16S and 23S rRNA structure from a comparative perspective Microbiol Rev 58 10 26 1:CAS:528:DyaK2cXmsVylu74%3D 8177168
21. RR Gutell JC Lee JJ Cannone 2002 The accuracy of ribosomal RNA comparative structure models Curr Opin Struct Biol 12 301 310 10.1016/S0959-440X(02)00339-1 1:CAS:528:DC%2BD38Xlt1Siu7c%3D 12127448 (Pubitemid 34804611)
22. S Haeder R Wirth H Herz D Spiteller 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 10.1073/pnas.0812082106 1:CAS:528:DC%2BD1MXktFOgtLg%3D 19270078
23. M Hamady R Knight 2009 Microbial community profiling for human microbiome projects: tools, techniques, and challenges Genome Res 19 1141 1152 10.1101/gr.085464.108 1:CAS:528:DC%2BD1MXosVCktL8%3D 19383763
24. Huang Y, Goodfellow M (2011) Genus I. Pseudonocardia (Henssen 1957, 408AL) emend. Park, Park, Lee and Kim 2008, 2477VP. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo M, Suzuki K, Ludwig W, Whitman WB (eds) Bergey's manual of systematic bacteriology, 2nd ed., vol 5: the actinobacteria. Springer, New York (in press)
25. C Kost T Lakatos I Böttcher W-R Arendholz M Redenbach R Wirth 2007 Non-specific association between filamentous bacteria and fungus-growing ants Naturwissenschaften 94 821 828 10.1007/s00114-007-0262-y 1:CAS:528: DC%2BD2sXhtVSisLjO 17541536 (Pubitemid 47367669)
26. SD Lee ES Kim YC Hah 2000 Phylogenetic analysis of the genera Pseudonocardia and Actinobispora based on 16S ribosomal DNA sequences FEMS Microbiol Lett 182 125 129 10.1111/j.1574-6968.2000.tb08885.x 1:CAS:528:DC%2BD3cXotFWj 10612743
27. Maddison DR, Maddison WP (2000) MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MA
28. HP McVeigh J Munro TM Embley 1994 The phylogenetic position of Pseudoamycolata halophobica (Akimov et al. 1989) and a proposal to reclassify it as Pseudonocardia halophobica Int J Syst Bacteriol 44 300 302 10.1099/00207713-44-2-300 1:CAS:528:DyaK2cXlsFeitbk%3D 8186094
29. UG Mueller NM Gerardo DK Aanen DL Six TR Schultz 2005 The evolution of agriculture in insects Ann Rev Ecol Evol Sys 36 563 595 10.1146/annurev.ecolsys. 36.102003.152626 (Pubitemid 43068871)
30. UG Mueller D Dash C Rabeling A Rodrigues 2008 Coevolution between attine ants and actinomycete bacteria: a reevaluation Evolution 62 2894 2912 10.1111/j.1558-5646.2008.00501.x 1:CAS:528:DC%2BD1cXhsVeqsLzM 18752608
31. D-C Oh M Poulsen CR Currie J Clardy 2009 Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis Nat Chem Biol 5 391 393 10.1038/nchembio.159 1:CAS:528:DC%2BD1MXjsl2ns7k%3D 19330011
32. GJ Olsen R Overbeek N Larsen TL Marsh MJ McCaughey MA Maciukenas WM Kuan TJ Macke Y Xing CR Woese 1992 The ribosomal database project Nucleic Acids Res 20 suppl 2199 2200 1:STN:280:DyaK383osFWktA%3D%3D 1598241
33. SW Park ST Park JE Lee YM Kim 2008 Pseudonocardia carboxydivorans sp. nov., a carbon monoxide-oxidizing actinomycete, and an emended description of the genus Pseudonocardia Int J Syst Evol Microbiol 58 2475 2478 10.1099/ijs.0.65765-0 1:CAS:528:DC%2BD1MXjvVOitQ%3D%3D 18984679
34. DK Posada A Crandall 1998 Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests Bioinformatics 14 817 818 10.1093/bioinformatics/14.9.817 1:CAS:528:DyaK1MXktlCltw%3D%3D 9918953
35. M Poulsen DP Erhardt DJ Molinaro L Ting-Li CR Currie 2007 Antagonistic bacterial interactions help shape host-symbiont dynamics within the fungus-growing ant-microbe mutualism PLoS ONE 2 e960 10.1371/journal.pone. 0000960 17896000 (Pubitemid 351472231)
36. Poulsen M, Little AEF, Currie CR (2009) Fungus-growing ant-microbe symbiosis: using microbes to defend beneficial associations with symbiotic communities. In: White JF, Torres MS (eds) Defensive mutualism in microbial symbiosis. CRC Press, Boca Raton, pp 149-162
37. A Rodrigues M Bacci UG Mueller A Ortiz FC Pagnocca 2008 Microfungal "weeds" in the leafcutter ant symbiosis Microb Ecol 56 604 614 10.1007/s00248-008-9380-0 1:STN:280:DC%2BD1cnks1aksQ%3D%3D 18369523
38. A Rodrigues RN Cable UG Mueller M Bacci FC Pagnocca 2009 Antagonistic interactions between garden yeasts and microfungal garden pathogens of leaf-cutting ants Antonie Leeuwenhook 96 331 342 10.1007/s10482-009-9350-7
39. AV Santos RJ Dillon VM Dillon SE Reynolds RI Samuels 2004 Occurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa FEMS Microbiol Lett 239 319 323 10.1016/j.femsle.2004.09.005 1:CAS:528:DC%2BD2cXot12isb0%3D 15476982 (Pubitemid 39346141)
40. R Sen HD Ishak D Estrada SE Dowd E Hong UG Mueller 2009 Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants Proc Natl Acad Sci USA 106 17805 17810 10.1073/pnas.0904827106 1:CAS:528:DC%2BD1MXhsVSjsLjF 19805175
41. F Stomeo MC Portillo JM Gonzalez L Laiz C Saiz-Jimenez 2008 Pseudonocardia in white colonizations in two caves with Paleolithic paintings Int Biodeterior Biodegradation 62 483 486 10.1016/j.ibiod.2007.12.011 1:CAS:528:DC%2BD1cXht1eitr%2FN
42. G Suen CR Currie 2008 Ancient fungal farmers of the insect world Microbiol Today 35 172 175
43. S Warwick T Bowen H McVeigh TM Embley 1994 A phylogenetic analysis of the family Pseudonocardiaceae and the genera Actinokineospora and Saccharothrix with 16S rRNA sequences and a proposal to combine the genera Amycolata and Pseudonocardia in an emended genus Pseudonocardia Int J Syst Bacteriol 44 293 299 10.1099/00207713-44-2-293 1:CAS:528:DyaK2cXlslCqtrg%3D 8186093
44. CR Woese 2000 Interpreting the universal phylogenetic tree Proc Natl Acad Sci USA 97 8392 8396 10.1073/pnas.97.15.8392 1:CAS:528:DC%2BD3cXlt1Ggtbc%3D 10900003 (Pubitemid 30639683)
45. CR Woese LJ Magrum R Gupta RB Siegel DA Stahl J Kop N Crawford R Brosius R Gutell JJ Hogan HF Noller 1980 Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence Nucleic Acids Res 8 2275 2294 10.1093/nar/8.10.2275 1:CAS:528:DyaL3cXlvVWhtro%3D 6159576
46. CR Woese R Gutell R Gupta HF Noller 1983 Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids Microbiol Rev 47 621 669 1:CAS:528:DyaL2cXhtlCgsbY%3D 6363901
47. M Zhang M Poulsen CR Currie 2007 Symbiont recognition of mutualistic bacteria in Acromyrmex leaf-cutting ants Int Soc Microb Ecol J 1 313 320
48. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, The University of Texas at Austin