Sequence conservation and functional constraint on intergenic spacers in reduced genomes of the obligate symbiont Buchnera

PLoS Genetics

Volumn 7, Issue 9, 2011, Pages

  Degnan, Patrick H ^a   Ochman, Howard ^a   Moran, Nancy A ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; NUCLEOTIDE; SPACER DNA; SMALL UNTRANSLATED RNA;

ACYRTHOSIPHON KONDOI; APHID; ARTICLE; BACTERIAL GENOME; BINDING SITE; BUCHNERA; DNA FOOTPRINTING; DNA SEQUENCE; GENE SEQUENCE; GENETIC CONSERVATION; GENOME ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PSEUDOGENE; SEQUENCE ALIGNMENT; SYMBIONT; TRANSCRIPTION TERMINATION; UROLEUCON AMBROSIAE; ANIMAL; GENETICS; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; REGULATORY SEQUENCE; SYMBIOSIS;

ACYRTHOSIPHON KONDOI; APHIDIDAE; BACTERIA (MICROORGANISMS); BUCHNERA (PROTEOBACTERIA); UROLEUCON AMBROSIAE;

ANIMALS; APHIDS; BASE SEQUENCE; BUCHNERA; CONSERVED SEQUENCE; DNA, INTERGENIC; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; PSEUDOGENES; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, SMALL UNTRANSLATED; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 80053458871     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002252     Document Type: Article

References (53)

1. McCutcheon JP, (2010) The bacterial essence of tiny symbiont genomes. Curr Opin Microbiol 13: 73-78.
2. Tamas I, Klasson L, Näslund K, Canbäck B, Eriksson AS, et al. (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376-2379.
3. van Ham RCHJ, Kamerbeek J, Palacios C, Rausell C, Abascal F, et al. (2003) Reductive evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 100: 581-586.
4. Degnan PH, Lazarus AB, Wernegreen JJ, (2005) Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res 15: 1023-1033.
5. McCutcheon JP, Moran NA, (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol Evol 2: 708-718.
6. Mira A, Ochman H, Moran NA, (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17: 589-596.
7. Kuo C-H, Moran NA, Ochman H, (2009) The consequences of genetic drift for bacterial genome complexity. Genome Res 19: 1450-1454.
8. Zientz E, Dandekar T, Gross R, (2004) Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol Mol Biol Rev 68: 745-770.
9. McCutcheon JM, Moran NA, (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci U S A 104: 19392-19397.
10. Moran NA, McCutcheon JP, Nakabachi A, (2008) Evolution and genomics of heritable bacterial symbionts. Annu Rev Genet 42: 165-190.
11. Moran NA, Mira A, (2001) The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol 2: RESEARCH0054.
12. Dunbar HE, Wilson AC, Ferguson NR, Moran NA, (2007) Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol 5: e96 doi:10.1371/journal.pbio.0050096.
13. Wilcox JL, Dunbar HE, Wolfinger RD, Moran NA, (2003) Consequences of reductive evolution for gene expression in an obligate endosymbiont. Mol Microbiol 48: 1491-1500.
14. Moran NA, Dunbar HE, Wilcox J, (2005) Regulation of transcription in a reduced bacterial genome: nutrient-provisioning genes of the obligate symbiont, Buchnera aphidicola. J Bacteriol 187: 4229-4237.
15. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H, (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407: 81-86.
16. Perez-Brocal V, Gil R, Ramos S, Lamelas A, Postigo M, et al. (2006) A small microbial genome: The end of a long symbiotic relationship? Science 314: 312-313.
17. Moran NA, McLaughlin HJ, Sorek R, (2009) The dynamics and timescale of ongoing genomic erosion in symbiotic bacteria. Science 323: 379-382.
18. Komaki K, Ishikawa H, (1999) Intracellular bacterial symbionts of aphids possess many genomes per bacterium. J Mol Evol 48: 717-722.
19. Cilia M, Tamborindeguy C, Fish T, Howe K, Thannhauser TW, et al. (2011) Genetics coupled to quantitative intact proteomics links heritable aphid and endosymbiont protein expression to circulative polerovirus transmission. J Virology 85: 2148-2166.
20. von Dohlen CD, Moran NA, (2000) Molecular data support a rapid radiation of aphid radiation of aphids in the Cretaceous and multiple origins of host alternation. Biol J Linnean Soc 71: 689-717.
21. Martinez-Torres D, Buades C, Latorre A, Moya A, (2001) Molecular systematics of aphids and their primary endosymbionts. Mol Phyl Evol 20: 437-449.
22. Hansen AK, Moran NA, (2011) Aphid genome expression reveals host symtbion cooperation in the production of amino acids. Proc Natl Acad Sci U S A 108: 2849-2854.
23. Cliften P, Sudarsanam P, Desikan A, Fulton L, Fulton B, et al. (2003) Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301: 71-76.
24. Zhang A, Gerstein M, (2003) Of mice and men: phylogenetic footprinting aids the discovery of regulatory elements. J Biol 2: 11.1-11.4.
25. Moran NA, (1996) Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A 93: 2873-2878.
26. Mira A, Moran N, (2002) Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microbial Ecol 44: 137-143.
27. Wilkinson TL, Fukatsu T, Ishikawa H, (2003) Transmission of symbiotic bacteria Buchnera to parthenogenetic embryos in the aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Arthropod Struct Dev 32: 241-245.
28. Bernays EA, Klein B, (2002) Quantifying the symbiont contribution to essential amino acids in aphids: the importance of tryptophan for Uroleucon ambrosiae. Physiol Ent 27: 275-284.
29. Degnan PH, Moran NA, (2008) Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol Ecol 17: 916-929.
30. Williams LE, Wernegreen JJ, (2010) Unprecedented loss of ammonia assimilation capability in a urease-encoding bacterial mutualist. BMC Genomics 11: 687.
31. Tamas I, Wernegreen JJ, Nystedt B, Kauppinen SN, Darby AC, et al. (2008) Endosymbiont gene functions impaired and rescued by polymerase infidelity at poly(A) tracts. Proc Natl Acad Sci U S A 105: 14934-14939.
32. Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, et al. (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314: 267.
33. McCutcheon JP, McDonald BR, Moran NA, (2009) Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet 5: e1000565 doi:10.1371/journal.pgen.1000565.
34. Charles H, Ishikawa H, (1999) Physical and genetic map of the genome of Buchnera, the primary endosymbiont of the pea aphid Acyrthosiphon pisum. J Mol Evol 48: 142-150.
35. Wernegreen JJ, Lazarus AB, Degnan PH, (2002) Small genome of Candidatus Blochmannia, the bacterial endosymbiont of Camponotus, implies irreversible specialization to an intracellular lifestyle. Microbiology 148: 2551-2556.
36. Gordon D, Abajian C, Green P, (1998) Consed: a graphical tool for sequence finishing. Genome Res 8: 195-202.
37. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, et al. (2009) BLAST+: architecture and applications. BMC Bioinformatics 10: 421.
38. Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA, (2009) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci U S A 106: 9063-9068.
39. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, et al. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
40. Lowe TM, Eddy SR, (1997) tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
41. Keseler IM, Bonavides-Martínez C, Collado-Vides J, Gama-Castro S, Gunsalus RP, et al. (2009) EcoCyc: a comprehensive view of Escherichia coli biology. Nucleic Acids Res 37: D464-D470.
42. Darling AE, Mau B, Perna NT, (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5: e11147 doi:10.1371/journal.pone.0011147.
43. Katoh K, Toh H, (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286-298.
44. Yang Z, (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
45. Stamatakis A, (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
46. Sanderson MJ, (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19: 301-302.
47. Clark MA, Moran NA, Baumann P, (1999) Sequence evolution in bacterial endosymbionts having extreme base composition. Mol Biol Evol 16: 1586-1598.
48. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
49. Anandam P, Torarinsson E, Ruzzo WL, (2009) Multiperm: shuffling multiple sequence alignments while approximately preserving dinucleotide frequencies. Bioinformatics 25: 668-669.
50. Suzek BE, Ermolaeva MD, Schreiber M, Salzberg SL, (2001) A probabilistic method for identifying start codons in bacterial genomes. Bioinformatics 17: 1123-1130.
51. Kingsford CL, Ayanbule K, Salzberg SL, (2007) Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol 8: R22.
52. Washietl S, Hofacker IL, Stadler PF, (2005) Fast and reliable prediction of noncoding RNAs. Proc Natl Acad Sci U S A 102: 2454-2459.
53. Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, et al. (1994) Fast folding and comparison of RNA secondary structures. Monatsh Chem 125: 167-188.