Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics

Biology Direct

Volumn 7, Issue , 2012, Pages

  Zhang, Dapeng ^a   de Souza, Robson F ^a,b   Anantharaman, Vivek ^a   Iyer, Lakshminarayan M ^a   Aravind, L ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ARTHROPODA; BACTERIA (MICROORGANISMS); ERINACEIDAE; EUKARYOTA; MIRIDAE; PHOTORHABDUS; PROKARYOTA;

BACTERIAL PROTEIN; BACTERIAL TOXIN; ENDONUCLEASE; METALLOPROTEINASE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BACTERIAL GENOME; BACTERIAL SECRETION SYSTEM; BACTERIUM; ECOSYSTEM; ENZYME ACTIVE SITE; GENE LOCUS; GENETIC VARIABILITY; GENETICS; GENOMICS; HUMAN; IMMUNOLOGY; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; PROTEIN ANALYSIS; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SYMBIOSIS;

AMINO ACID SEQUENCE; ANIMALS; BACTERIA; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BACTERIAL TOXINS; CATALYTIC DOMAIN; ECOSYSTEM; ENDONUCLEASES; EVOLUTION, MOLECULAR; GENETIC LOCI; GENETIC VARIATION; GENOME, BACTERIAL; GENOMICS; HUMANS; METALLOPROTEASES; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SYMBIOSIS;

EID: 84862602464     PISSN: None     EISSN: 17456150     Source Type: Journal    
DOI: 10.1186/1745-6150-7-18     Document Type: Article

References (230)

1. Rochat H, Martin-Eauclaire H. Animal toxins: facts and protocols 2000, Basel Boston: Birkhauser Verlag.
2. Keeler RF, Tu AT. Toxicology of plant and fungal compounds 1991, New York: Dekker.
3. Mackessy SP. Handbook of venoms and toxins of reptiles 2010, Boca Raton: CRC Press.
4. Alouf JE, Popoff MR. The comprehensive sourcebook of bacterial protein toxins 2006, Amsterdam; Boston: Elsevier Academic Press, 3.
5. Walsh C. Antibiotics: actions, origins, resistance 2003, Washington, D.C.: ASM Press.
6. Proft T. Microbial toxins: molecular and cellular biology 2005, Norfolk, England: BIOS Scientific.
7. Rappuoli R, Montecucco C. Guidebook to protein toxins and their use in cell biology 1997, Oxford; New York: Oxford University Press.
8. Dhananjaya BL. CJ DS: An overview on nucleases (DNase, RNase, and phosphodiesterase) in snake venoms. Biochemistry (Mosc) 2010, 75(1):1-6.
9. Endo Y, Tsurugi K. Mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. Nucleic Acids Symp Ser 1986, 17:187-190.
10. Chakrabarti A, Jha BK, Silverman RH. New insights into the role of RNase L in innate immunity. J Interferon Cytokine Res 2011, 31(1):49-57. 10.1089/jir.2010.0120, 3021357, 21190483.
11. Wiesner J, Vilcinskas A. Antimicrobial peptides: the ancient arm of the human immune system. Virulence 2010, 1(5):440-464. 10.4161/viru.1.5.12983, 21178486.
12. Li WM, Barnes T, Lee CH. Endoribonucleases-enzymes gaining spotlight in mRNA metabolism. FEBS J 2010, 277(3):627-641. 10.1111/j.1742-4658.2009.07488.x, 19968858.
13. Rosenberg HF. RNase A ribonucleases and host defense: an evolving story. J Leukoc Biol 2008, 83(5):1079-1087. 10.1189/jlb.1107725, 2692241, 18211964.
14. Merritt EA, Hol WG. AB5 toxins. Curr Opin Struct Biol 1995, 5(2):165-171. 10.1016/0959-440X(95)80071-9, 7648317.
15. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 2011, 475(7356):343-347. 10.1038/nature10244, 3146020, 21776080.
16. Aoki SK, Poole SJ, Hayes CS, Low DA. Toxin on a stick: modular CDI toxin delivery systems play roles in bacterial competition. Virulence 2011, 2(4):356-359. 10.4161/viru.2.4.16463, 3173679, 21705856.
17. Zhang D, Iyer LM, Aravind L. A novel immunity system for bacterial nucleic acid degrading toxins and its recruitment in various eukaryotic and DNA viral systems. Nucleic Acids Res 2011, 39(11):4532-4552. 10.1093/nar/gkr036, 3113570, 21306995.
18. Iyer LM, Zhang D, Rogozin IB, Aravind L. Evolution of the deaminase fold and multiple origins of eukaryotic editing and mutagenic nucleic acid deaminases from bacterial toxin systems. Nucleic Acids Res 2011, 39(22):9473-9497. 10.1093/nar/gkr691, 3239186, 21890906.
19. Sisto A, Cipriani MG, Morea M, Lonigro SL, Valerio F, Lavermicocca P. An Rhs-like genetic element is involved in bacteriocin production by Pseudomonas savastanoi pv. savastanoi. Antonie Van Leeuwenhoek 2010, 98(4):505-517. 10.1007/s10482-010-9468-7, 20563849.
20. Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D. Colicin biology. Microbiol Mol Biol Rev 2007, 71(1):158-229. 10.1128/MMBR.00036-06, 1847374, 17347522.
21. Kobayashi I. Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res 2001, 29(18):3742-3756. 10.1093/nar/29.18.3742, 55917, 11557807.
22. Anantharaman V, Aravind L. New connections in the prokaryotic toxin-antitoxin network: relationship with the eukaryotic nonsense-mediated RNA decay system. Genome Biol 2003, 4(12):R81. 10.1186/gb-2003-4-12-r81, 329420, 14659018.
23. Engelberg-Kulka H, Glaser G. Addiction modules and programmed cell death and antideath in bacterial cultures. Annu Rev Microbiol 1999, 53:43-70. 10.1146/annurev.micro.53.1.43, 10547685.
24. Van Melderen L. Toxin-antitoxin systems: why so many, what for?. Curr Opin Microbiol 2010, 13(6):781-785. 10.1016/j.mib.2010.10.006, 21041110.
25. Aepfelbacher M, Aktories K, Just I. Bacterial protein toxins 2000, Berlin; New York: Springer.
26. Nguyen VT, Kamio Y. Cooperative assembly of beta-barrel pore-forming toxins. J Biochem 2004, 136(5):563-567. 10.1093/jb/mvh160, 15632294.
27. Gilbert RJ. Pore-forming toxins. Cell Mol Life Sci 2002, 59(5):832-844. 10.1007/s00018-002-8471-1, 12088283.
28. Leplae R, Geeraerts D, Hallez R, Guglielmini J, Dreze P, Van Melderen L. Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res 2011, 39(13):5513-5525. 10.1093/nar/gkr131, 3141249, 21422074.
29. MacIntyre DL, Miyata ST, Kitaoka M, Pukatzki S. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci USA 2010, 107(45):19520-19524. 10.1073/pnas.1012931107, 2984155, 20974937.
30. Schwarz S, West TE, Boyer F, Chiang WC, Carl MA, Hood RD, Rohmer L, Tolker-Nielsen T, Skerrett SJ, Mougous JD. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 2010, 6(8):e1001068. 10.1371/journal.ppat.1001068, 2928800, 20865170.
31. Linhartova I, Bumba L, Masin J, Basler M, Osicka R, Kamanova J, Prochazkova K, Adkins I, Hejnova-Holubova J, Sadilkova L, et al. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol Rev 2010, 34(6):1076-1112. 3034196, 20528947.
32. Holberger LE, Garza-Sanchez F, Lamoureux J, Low DA, Hayes CS. A novel family of toxin/antitoxin proteins in Bacillus species. FEBS Lett 2012, 586(2):132-136. 10.1016/j.febslet.2011.12.020, 22200572.
33. Iyer LM, Makarova KS, Koonin EV, Aravind L. Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 2004, 32(17):5260-5279. 10.1093/nar/gkh828, 521647, 15466593.
34. Alvarez-Martinez CE, Christie PJ. Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 2009, 73(4):775-808. 10.1128/MMBR.00023-09, 2786583, 19946141.
35. Cornelis GR. The type III secretion injectisome. Nat Rev Microbiol 2006, 4(11):811-825. 10.1038/nrmicro1526, 17041629.
36. Hayes CS, Aoki SK, Low DA. Bacterial contact-dependent delivery systems. Annu Rev Genet 2010, 44:71-90. 10.1146/annurev.genet.42.110807.091449, 21047256.
37. Delattre AS, Clantin B, Saint N, Locht C, Villeret V, Jacob-Dubuisson F. Functional importance of a conserved sequence motif in FhaC, a prototypic member of the TpsB/Omp85 superfamily. FEBS J 2010, 277(22):4755-4765. 10.1111/j.1742-4658.2010.07881.x, 20955520.
38. Bonemann G, Pietrosiuk A, Mogk A. Tubules and donuts: a type VI secretion story. Mol Microbiol 2010, 76(4):815-821. 10.1111/j.1365-2958.2010.07171.x, 20444095.
39. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 2012, 483(7388):182-186. 10.1038/nature10846, 22367545.
40. Yang G, Dowling AJ, Gerike U, ffrench-Constant RH, Waterfield NR. Photorhabdus virulence cassettes confer injectable insecticidal activity against the wax moth. J Bacteriol 2006, 188(6):2254-2261. 10.1128/JB.188.6.2254-2261.2006, 1428146, 16513755.
41. Hurst MR, Glare TR, Jackson TA. Cloning Serratia entomophila antifeeding genes-a putative defective prophage active against the grass grub Costelytra zealandica. J Bacteriol 2004, 186(15):5116-5128. 10.1128/JB.186.15.5116-5128.2004, 451664, 15262948.
42. Bowen D, Rocheleau TA, Blackburn M, Andreev O, Golubeva E, Bhartia R, ffrench-Constant RH. Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 1998, 280(5372):2129-2132. 10.1126/science.280.5372.2129, 9641921.
43. Ellermeier CD, Losick R. Evidence for a novel protease governing regulated intramembrane proteolysis and resistance to antimicrobial peptides in Bacillus subtilis. Genes Dev 2006, 20(14):1911-1922. 10.1101/gad.1440606, 1522089, 16816000.
44. Aoki SK, Diner EJ, de Roodenbeke CT, Burgess BR, Poole SJ, Braaten BA, Jones AM, Webb JS, Hayes CS, Cotter PA, et al. A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 2010, 468(7322):439-442. 10.1038/nature09490, 3058911, 21085179.
45. Jackson AP, Thomas GH, Parkhill J, Thomson NR. Evolutionary diversification of an ancient gene family (rhs) through C-terminal displacement. BMC Genomics 2009, 10:584. 10.1186/1471-2164-10-584, 2935791, 19968874.
46. Kung VL, Khare S, Stehlik C, Bacon EM, Hughes AJ, Hauser AR. An rhs gene of Pseudomonas aeruginosa encodes a virulence protein that activates the inflammasome. Proc Natl Acad Sci USA 2012, 109(4):1275-1280. 10.1073/pnas.1109285109, 3268321, 22232685.
47. Yongqing T, Potempa J, Pike RN, Wijeyewickrema LC. The lysine-specific gingipain of Porphyromonas gingivalis: importance to pathogenicity and potential strategies for inhibition. Adv Exp Med Biol 2011, 712:15-29. 10.1007/978-1-4419-8414-2_2, 21660656.
48. Tonello F, Montecucco C. The anthrax lethal factor and its MAPK kinase-specific metalloprotease activity. Mol Aspects Med 2009, 30(6):431-438. 10.1016/j.mam.2009.07.006, 19665472.
49. Sheahan KL, Cordero CL, Satchell KJ. Autoprocessing of the Vibrio cholerae RTX toxin by the cysteine protease domain. EMBO J 2007, 26(10):2552-2561. 10.1038/sj.emboj.7601700, 1868911, 17464284.
50. Shao F, Merritt PM, Bao Z, Innes RW, Dixon JE. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 2002, 109(5):575-588. 10.1016/S0092-8674(02)00766-3, 12062101.
51. Rossetto O, de Bernard M, Pellizzari R, Vitale G, Caccin P, Schiavo G, Montecucco C. Bacterial toxins with intracellular protease activity. Clin Chim Acta 2000, 291(2):189-199. 10.1016/S0009-8981(99)00228-4, 10675723.
52. Pei J, Grishin NV. Prediction of a caspase-like fold in Tannerella forsythia virulence factor PrtH. Cell Cycle 2009, 8(9):1453-1455. 10.4161/cc.8.9.8243, 19305154.
53. Makarova KS, Aravind L, Koonin EV. A superfamily of archaeal, bacterial, and eukaryotic proteins homologous to animal transglutaminases. Protein Sci 1999, 8(8):1714-1719. 10.1110/ps.8.8.1714, 2144420, 10452618.
54. Gordon VM, Leppla SH. Proteolytic activation of bacterial toxins: role of bacterial and host cell proteases. Infect Immun 1994, 62(2):333-340. 186112, 8300195.
55. McNulty C, Thompson J, Barrett B, Lord L, Andersen C, Roberts IS. The cell surface expression of group 2 capsular polysaccharides in Escherichia coli: the role of KpsD, RhsA and a multi-protein complex at the pole of the cell. Mol Microbiol 2006, 59(3):907-922. 10.1111/j.1365-2958.2005.05010.x, 16420360.
56. Hill CW, Sandt CH, Vlazny DA. Rhs elements of Escherichia coli: a family of genetic composites each encoding a large mosaic protein. Mol Microbiol 1994, 12(6):865-871. 10.1111/j.1365-2958.1994.tb01074.x, 7934896.
57. Lupardus PJ, Shen A, Bogyo M, Garcia KC. Small molecule-induced allosteric activation of the Vibrio cholerae RTX cysteine protease domain. Science 2008, 322(5899):265-268. 10.1126/science.1162403, 3272704, 18845756.
58. Tinel A, Janssens S, Lippens S, Cuenin S, Logette E, Jaccard B, Quadroni M, Tschopp J. Autoproteolysis of PIDD marks the bifurcation between pro-death caspase-2 and pro-survival NF-kappaB pathway. EMBO J 2007, 26(1):197-208. 10.1038/sj.emboj.7601473, 1782377, 17159900.
59. Janssens S, Tinel A. The PIDDosome, DNA-damage-induced apoptosis and beyond. Cell Death Differ 2012, 19(1):13-20. 10.1038/cdd.2011.162, 22095286.
60. Ponting CP, Hofmann K, Bork P. A latrophilin/CL-1-like GPS domain in polycystin-1. Curr Biol 1999, 9(16):R585-R588. 10.1016/S0960-9822(99)80379-0, 10469603.
61. Mans BJ, Anantharaman V, Aravind L, Koonin EV. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 2004, 3(12):1612-1637. 10.4161/cc.3.12.1345, 15611647.
62. Hurst MR, Glare TR, Jackson TA, Ronson CW. Plasmid-located pathogenicity determinants of Serratia entomophila, the causal agent of amber disease of grass grub, show similarity to the insecticidal toxins of Photorhabdus luminescens. J Bacteriol 2000, 182(18):5127-5138. 10.1128/JB.182.18.5127-5138.2000, 94661, 10960097.
63. Pei J, Mitchell DA, Dixon JE, Grishin NV. Expansion of type II CAAX proteases reveals evolutionary origin of gamma-secretase subunit APH-1. J Mol Biol 2011, 410(1):18-26. 10.1016/j.jmb.2011.04.066, 3155266, 21570408.
64. Frias M, Gonzalez C, Brito N. BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytol 2011, 192(2):483-495. 10.1111/j.1469-8137.2011.03802.x, 21707620.
65. Aravind L, Iyer LM, Anantharaman V. Natural history of sensor domains in bacterial signaling systems. Sensory Mechanisms in Bacteria: Molecular Aspects of Signal Recognition 2010, Norfolk, UK: Caister Academic Press, Spiro S, Dixon R.
66. Aravind L, Koonin EV. Classification of the caspase-hemoglobinase fold: detection of new families and implications for the origin of the eukaryotic separins. Proteins 2002, 46(4):355-367. 10.1002/prot.10060, 11835511.
67. Barrett AJ, Rawlings ND. Evolutionary lines of cysteine peptidases. Biol Chem 2001, 382(5):727-733.
68. Kitadokoro K, Kamitani S, Miyazawa M, Hanajima-Ozawa M, Fukui A, Miyake M, Horiguchi Y. Crystal structures reveal a thiol protease-like catalytic triad in the C-terminal region of Pasteurella multocida toxin. Proc Natl Acad Sci USA 2007, 104(12):5139-5144. 10.1073/pnas.0608197104, 1829276, 17360394.
69. Zhu M, Shao F, Innes RW, Dixon JE, Xu Z. The crystal structure of Pseudomonas avirulence protein AvrPphB: a papain-like fold with a distinct substrate-binding site. Proc Natl Acad Sci USA 2004, 101(1):302-307. 10.1073/pnas.2036536100, 314180, 14694194.
70. Kagawa TF, Cooney JC, Baker HM, McSweeney S, Liu M, Gubba S, Musser JM, Baker EN. Crystal structure of the zymogen form of the group A Streptococcus virulence factor SpeB: an integrin-binding cysteine protease. Proc Natl Acad Sci USA 2000, 97(5):2235-2240. 10.1073/pnas.040549997, 15784, 10681429.
71. Anantharaman V, Aravind L. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol 2003, 4(2):R11. 10.1186/gb-2003-4-2-r11, 151301, 12620121.
72. Pei J, Grishin NV. The Rho GTPase inactivation domain in Vibrio cholerae MARTX toxin has a circularly permuted papain-like thiol protease fold. Proteins: Structure, Function, and Bioinformatics 2009, 77(2):413-419.
73. Wood MW, Williams C, Upadhyay A, Gill AC, Philippe DL, Galyov EE, van den Elsen JM, Bagby S. Structural analysis of Salmonella enterica effector protein SopD. Biochim Biophys Acta 2004, 1698(2):219-226. 10.1016/j.bbapap.2003.12.003, 15134655.
74. Richards GP, Watson MA, Crane EJ, Burt IG, Bushek D. Shewanella and Photobacterium spp. in oysters and seawater from the Delaware Bay. Appl Environ Microbiol 2008, 74(11):3323-3327. 10.1128/AEM.00060-08, 2423050, 18378645.
75. Burroughs AM, Iyer LM, Aravind L. Comparative genomics and evolutionary trajectories of viral ATP dependent DNA-packaging systems. Genome Dyn 2007, 3:48-65.
76. Nanao MH, Tcherniuk SO, Chroboczek J, Dideberg O, Dessen A, Balakirev MY. Crystal structure of human otubain 2. EMBO Rep 2004, 5(8):783-788. 10.1038/sj.embor.7400201, 1299112, 15258613.
77. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, Wu P, Wiesmann C, Baker R, Boone DL, et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004, 430(7000):694-699. 10.1038/nature02794, 15258597.
78. Birtles RJ, Rowbotham TJ, Michel R, Pitcher DG, Lascola B, Alexiou-Daniel S, Raoult D. Candidatus Odyssella thessalonicensis' gen. nov., sp. nov., an obligate intracellular parasite of Acanthamoeba species. Int J Syst Evol Microbiol 2000, 50(Pt 1):63-72.
79. Schmitz-Esser S, Tischler P, Arnold R, Montanaro J, Wagner M, Rattei T, Horn M. The genome of the amoeba symbiont "Candidatus Amoebophilus asiaticus" reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J Bacteriol 2010, 192(4):1045-1057. 10.1128/JB.01379-09, 2812958, 20023027.
80. Loureiro J, Ploegh HL. Antigen presentation and the ubiquitin-proteasome system in host-pathogen interactions. Adv Immunol 2006, 92:225-305.
81. Iyer LM, Leipe DD, Koonin EV, Aravind L. Evolutionary history and higher order classification of AAA + ATPases. J Struct Biol 2004, 146(1-2):11-31.
82. Bonemann G, Pietrosiuk A, Diemand A, Zentgraf H, Mogk A. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J 2009, 28(4):315-325. 10.1038/emboj.2008.269, 2646146, 19131969.
83. Dhanaraj V, Ye QZ, Johnson LL, Hupe DJ, Ortwine DF, Dunbar JB, Rubin JR, Pavlovsky A, Humblet C, Blundell TL. X-ray structure of a hydroxamate inhibitor complex of stromelysin catalytic domain and its comparison with members of the zinc metalloproteinase superfamily. Structure 1996, 4(4):375-386. 10.1016/S0969-2126(96)00043-3, 8740360.
84. ffrench-Constant RH, Dowling A, Waterfield NR. Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture. Toxicon 2007, 49(4):436-451. 10.1016/j.toxicon.2006.11.019, 17207509.
85. Pechy-Tarr M, Bruck DJ, Maurhofer M, Fischer E, Vogne C, Henkels MD, Donahue KM, Grunder J, Loper JE, Keel C. Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environ Microbiol 2008, 10(9):2368-2386. 10.1111/j.1462-2920.2008.01662.x, 18484997.
86. Rodou A, Ankrah DO, Stathopoulos C. Toxins and Secretion Systems of Photorhabdus luminescens. Toxins (Basel) 2010, 2(6):1250-1264.
87. Daborn PJ, Waterfield N, Silva CP, Au CP, Sharma S, ffrench-Constant RH. A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc Natl Acad Sci USA 2002, 99(16):10742-10747. 10.1073/pnas.102068099, 125031, 12136122.
88. Wei CF, Kvitko BH, Shimizu R, Crabill E, Alfano JR, Lin NC, Martin GB, Huang HC, Collmer A. A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J 2007, 51(1):32-46. 10.1111/j.1365-313X.2007.03126.x, 17559511.
89. Li X, Lin H, Zhang W, Zou Y, Zhang J, Tang X, Zhou JM. Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci USA 2005, 102(36):12990-12995. 10.1073/pnas.0502425102, 1200263, 16123135.
90. Masuda M, Betancourt L, Matsuzawa T, Kashimoto T, Takao T, Shimonishi Y, Horiguchi Y. Activation of rho through a cross-link with polyamines catalyzed by Bordetella dermonecrotizing toxin. EMBO J 2000, 19(4):521-530. 10.1093/emboj/19.4.521, 305590, 10675321.
91. Dirix G, Monsieurs P, Dombrecht B, Daniels R, Marchal K, Vanderleyden J, Michiels J. Peptide signal molecules and bacteriocins in Gram-negative bacteria: a genome-wide in silico screening for peptides containing a double-glycine leader sequence and their cognate transporters. Peptides 2004, 25(9):1425-1440. 10.1016/j.peptides.2003.10.028, 15374646.
92. Ishii S, Yano T, Ebihara A, Okamoto A, Manzoku M, Hayashi H. Crystal structure of the peptidase domain of Streptococcus ComA, a bifunctional ATP-binding cassette transporter involved in the quorum-sensing pathway. J Biol Chem 2010, 285(14):10777-10785. 10.1074/jbc.M109.093781, 2856284, 20100826.
93. Kelly M, Hart E, Mundy R, Marches O, Wiles S, Badea L, Luck S, Tauschek M, Frankel G, Robins-Browne RM, et al. Essential role of the type III secretion system effector NleB in colonization of mice by Citrobacter rodentium. Infect Immun 2006, 74(4):2328-2337. 10.1128/IAI.74.4.2328-2337.2006, 1418941, 16552063.
94. Wong AR, Pearson JS, Bright MD, Munera D, Robinson KS, Lee SF, Frankel G, Hartland EL. Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol 2011, 80(6):1420-1438. 10.1111/j.1365-2958.2011.07661.x, 21488979.
95. Iyer LM, Koonin EV, Aravind L. Novel predicted peptidases with a potential role in the ubiquitin signaling pathway. Cell Cycle 2004, 3(11):1440-1450. 10.4161/cc.3.11.1206, 15483401.
96. Odagaki Y, Hayashi A, Okada K, Hirotsu K, Kabashima T, Ito K, Yoshimoto T, Tsuru D, Sato M, Clardy J. The crystal structure of pyroglutamyl peptidase I from Bacillus amyloliquefaciens reveals a new structure for a cysteine protease. Structure 1999, 7(4):399-411. 10.1016/S0969-2126(99)80053-7, 10196127.
97. Takamatsu H, Imamura A, Kodama T, Asai K, Ogasawara N, Watabe K. The yabG gene of Bacillus subtilis encodes a sporulation specific protease which is involved in the processing of several spore coat proteins. FEMS Microbiol Lett 2000, 192(1):33-38. 10.1111/j.1574-6968.2000.tb09355.x, 11040425.
98. Biarrotte-Sorin S, Hugonnet JE, Delfosse V, Mainardi JL, Gutmann L, Arthur M, Mayer C. Crystal structure of a novel beta-lactam-insensitive peptidoglycan transpeptidase. J Mol Biol 2006, 359(3):533-538. 10.1016/j.jmb.2006.03.014, 16647082.
99. Bielnicki J, Devedjiev Y, Derewenda U, Dauter Z, Joachimiak A, Derewenda ZS. B. subtilis ykuD protein at 2.0 A resolution: insights into the structure and function of a novel, ubiquitous family of bacterial enzymes. Proteins 2006, 62(1):144-151. 2792008, 16287140.
100. Degnan PH, Moran NA. Diverse phage-encoded toxins in a protective insect endosymbiont. Appl Environ Microbiol 2008, 74(21):6782-6791. 10.1128/AEM.01285-08, 2576707, 18791000.
101. Oliver KM, Degnan PH, Hunter MS, Moran NA. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 2009, 325(5943):992-994. 10.1126/science.1174463, 19696350.
102. Aravind L, Walker DR, Koonin EV. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res 1999, 27(5):1223-1242. 10.1093/nar/27.5.1223, 148307, 9973609.
103. Aravind L, Makarova KS, Koonin EV. Holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Res 2000, 28(18):3417-3432. 10.1093/nar/28.18.3417, 110722, 10982859.
104. Mak AN, Lambert AR, Stoddard BL. Folding, DNA recognition, and function of GIY-YIG endonucleases: crystal structures of R. Eco29kI. Structure 2010, 18(10):1321-1331. 10.1016/j.str.2010.07.006, 2955809, 20800503.
105. Zhao L, Bonocora RP, Shub DA, Stoddard BL. The restriction fold turns to the dark side: a bacterial homing endonuclease with a PD-(D/E)-XK motif. EMBO J 2007, 26(9):2432-2442. 10.1038/sj.emboj.7601672, 1864971, 17410205.
106. Stoddard BL. Homing endonuclease structure and function. Q Rev Biophys 2005, 38(1):49-95.
107. Yang W. Nucleases: diversity of structure, function and mechanism. Q Rev Biophys 2011, 44(1):1-93. 10.1017/S0033583510000181, 20854710.
108. Anantharaman V, Aravind L. The NYN domains: novel predicted RNAses with a PIN domain-like fold. RNA Biol 2006, 3(1):18-27. 10.4161/rna.3.1.2548, 17114934.
109. Carr S, Walker D, James R, Kleanthous C, Hemmings AM. Inhibition of a ribosome-inactivating ribonuclease: the crystal structure of the cytotoxic domain of colicin E3 in complex with its immunity protein. Structure 2000, 8(9):949-960. 10.1016/S0969-2126(00)00186-6, 10986462.
110. Graille M, Mora L, Buckingham RH, van Tilbeurgh H, de Zamaroczy M. Structural inhibition of the colicin D tRNase by the tRNA-mimicking immunity protein. EMBO J 2004, 23(7):1474-1482. 10.1038/sj.emboj.7600162, 391069, 15014439.
111. Ghosh M, Meiss G, Pingoud A, London RE, Pedersen LC. Structural insights into the mechanism of nuclease A, a betabeta alpha metal nuclease from Anabaena. J Biol Chem 2005, 280(30):27990-27997. 10.1074/jbc.M501798200, 15897201.
112. Guthrie EP, Quinton-Jager T, Moran LS, Slatko BE, Kucera RB, Benner JS, Wilson GG, Brooks JE. Cloning, expression and sequence analysis of the SphI restriction-modification system. Gene 1996, 180(1-2):107-112.
113. Woo EJ, Kim YG, Kim MS, Han WD, Shin S, Robinson H, Park SY, Oh BH. Structural mechanism for inactivation and activation of CAD/DFF40 in the apoptotic pathway. Mol Cell 2004, 14(4):531-539. 10.1016/S1097-2765(04)00258-8, 15149602.
114. Lugovskoy AA, Zhou P, Chou JJ, McCarty JS, Li P, Wagner G. Solution structure of the CIDE-N domain of CIDE-B and a model for CIDE-N/CIDE-N interactions in the DNA fragmentation pathway of apoptosis. Cell 1999, 99(7):747-755. 10.1016/S0092-8674(00)81672-4, 10619428.
115. Minet AD, Rubin BP, Tucker RP, Baumgartner S, Chiquet-Ehrismann R. Teneurin-1, a vertebrate homologue of the Drosophila pair-rule gene ten-m, is a neuronal protein with a novel type of heparin-binding domain. J Cell Sci 1999, 112(Pt 12):2019-2032.
116. Silva JP, Lelianova VG, Ermolyuk YS, Vysokov N, Hitchen PG, Berninghausen O, Rahman MA, Zangrandi A, Fidalgo S, Tonevitsky AG, et al. Latrophilin 1 and its endogenous ligand Lasso/teneurin-2 form a high-affinity transsynaptic receptor pair with signaling capabilities. Proc Natl Acad Sci USA 2011, 108(29):12113-12118. 10.1073/pnas.1019434108, 3141932, 21724987.
117. Topf U, Chiquet-Ehrismann R. Genetic interaction between Caenorhabditis elegans teneurin ten-1 and prolyl 4-hydroxylase phy-1 and their function in collagen IV-mediated basement membrane integrity during late elongation of the embryo. Mol Biol Cell 2011, 22(18):3331-3343. 10.1091/mbc.E10-10-0853, 3172259, 21795395.
118. Qian X, Barsyte-Lovejoy D, Wang L, Chewpoy B, Gautam N, Al Chawaf A, Lovejoy DA. Cloning and characterization of teneurin C-terminus associated peptide (TCAP)-3 from the hypothalamus of an adult rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 2004, 137(2):205-216. 10.1016/j.ygcen.2004.02.007, 15158132.
119. Aravind L, Koonin EV. Prokaryotic homologs of the eukaryotic DNA-end-binding protein Ku, novel domains in the Ku protein and prediction of a prokaryotic double-strand break repair system. Genome Res 2001, 11(8):1365-1374. 10.1101/gr.181001, 311082, 11483577.
120. Aravind L, Iyer LM. The HARE-HTH and associated domains: novel modules in the coordination of epigenetic DNA and protein modifications. Cell Cycle 2012, 11(1):119-131. 10.4161/cc.11.1.18475, 3272235, 22186017.
121. Vosman B, Kuiken G, Kooistra J, Venema G. Transformation in Bacillus subtilis: involvement of the 17-kilodalton DNA-entry nuclease and the competence-specific 18-kilodalton protein. J Bacteriol 1988, 170(8):3703-3710. 211348, 2841296.
122. Johnson EP, Mincer T, Schwab H, Burgin AB, Helinski DR. Plasmid RK2 ParB protein: purification and nuclease properties. J Bacteriol 1999, 181(19):6010-6018. 103628, 10498713.
123. Jonsson TJ, Murray MS, Johnson LC, Poole LB, Lowther WT. Structural basis for the retroreduction of inactivated peroxiredoxins by human sulfiredoxin. Biochemistry 2005, 44(24):8634-8642. 10.1021/bi050131i, 15952770.
124. Chen S, Wang L, Deng Z. Twenty years hunting for sulfur in DNA. Protein Cell 2010, 1(1):14-21. 10.1007/s13238-010-0009-y, 21203994.
125. Iyer LM, Tahiliani M, Rao A, Aravind L. Prediction of novel families of enzymes involved in oxidative and other complex modifications of bases in nucleic acids. Cell Cycle 2009, 8(11):1698-1710. 10.4161/cc.8.11.8580, 2995806, 19411852.
126. Burroughs AM, Iyer LM, Aravind L. Functional diversification of the RING finger and other binuclear treble clef domains in prokaryotes and the early evolution of the ubiquitin system. Mol Biosyst 2011, 7(7):2261-2277. 10.1039/c1mb05061c, 21547297.
127. Iyer LM, Burroughs AM, Aravind L. The prokaryotic antecedents of the ubiquitin-signaling system and the early evolution of ubiquitin-like beta-grasp domains. Genome Biol 2006, 7(7):R60. 10.1186/gb-2006-7-7-r60, 1779556, 16859499.
128. Burns KE, Baumgart S, Dorrestein PC, Zhai H, McLafferty FW, Begley TP. Reconstitution of a new cysteine biosynthetic pathway in Mycobacterium tuberculosis. J Am Chem Soc 2005, 127(33):11602-11603. 10.1021/ja053476x, 2536522, 16104727.
129. Sarkar S, Iyer G, Wu J, Glass NL. Nonself recognition is mediated by HET-C heterocomplex formation during vegetative incompatibility. EMBO J 2002, 21(18):4841-4850. 10.1093/emboj/cdf479, 126278, 12234924.
130. Wichmann G, Sun J, Dementhon K, Glass NL, Lindow SE. A novel gene, phcA from Pseudomonas syringae induces programmed cell death in the filamentous fungus Neurospora crassa. Mol Microbiol 2008, 68(3):672-689. 10.1111/j.1365-2958.2008.06175.x, 18363647.
131. Hough E, Hansen LK, Birknes B, Jynge K, Hansen S, Hordvik A, Little C, Dodson E, Derewenda Z. High-resolution (1.5 A) crystal structure of phospholipase C from Bacillus cereus. Nature 1989, 338(6213):357-360. 10.1038/338357a0, 2493587.
132. Romier C, Dominguez R, Lahm A, Dahl O, Suck D. Recognition of single-stranded DNA by nuclease P1: high resolution crystal structures of complexes with substrate analogs. Proteins 1998, 32(4):414-424. 10.1002/(SICI)1097-0134(19980901)32:4<414::AID-PROT2>3.0.CO;2-G, 9726413.
133. Kawano M, Aravind L, Storz G. An antisense RNA controls synthesis of an SOS-induced toxin evolved from an antitoxin. Mol Microbiol 2007, 64(3):738-754. 10.1111/j.1365-2958.2007.05688.x, 1891008, 17462020.
134. Structural Classification of Proteins http://scop.mrc-lmb.cam.ac.uk/scop/index.html.
135. Gioia U, Laneve P, Dlakic M, Arceci M, Bozzoni I, Caffarelli E. Functional characterization of XendoU, the endoribonuclease involved in small nucleolar RNA biosynthesis. J Biol Chem 2005, 280(19):18996-19002. 10.1074/jbc.M501160200, 15755742.
136. Raines RT. Ribonuclease A. Chem Rev 1998, 98(3):1045-1066. 10.1021/cr960427h, 11848924.
137. Ng CL, Lang K, Meenan NA, Sharma A, Kelley AC, Kleanthous C, Ramakrishnan V. Structural basis for 16 S ribosomal RNA cleavage by the cytotoxic domain of colicin E3. Nat Struct Mol Biol 2010, 17(10):1241-1246. 10.1038/nsmb.1896, 20852642.
138. Duron O. Insights beyond Wolbachia-Drosophila interactions: never completely trust a model: insights from cytoplasmic incompatibility beyond Wolbachia-Drosophila interactions. Heredity (Edinb) 2008, 101(6):473-474.
139. Yarbrough ML, Li Y, Kinch LN, Grishin NV, Ball HL, Orth K. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 2009, 323(5911):269-272. 10.1126/science.1166382, 19039103.
140. Feng F, Yang F, Rong W, Wu X, Zhang J, Chen S, He C, Zhou JM. A Xanthomonas uridine 5'-monophosphate transferase inhibits plant immune kinases. Nature 2012, 485(7396):114-118. 10.1038/nature10962, 22504181.
141. Goto Y, Li B, Claesen J, Shi Y, Bibb MJ, van der Donk WA. Discovery of unique lanthionine synthetases reveals new mechanistic and evolutionary insights. PLoS Biol 2010, 8(3):e1000339. 10.1371/journal.pbio.1000339, 2843593, 20351769.
142. You YO, Levengood MR, Ihnken LA, Knowlton AK, van der Donk WA. Lacticin 481 synthetase as a general serine/threonine kinase. ACS Chem Biol 2009, 4(5):379-385. 10.1021/cb800309v, 2709986, 19292452.
143. Reinert DJ, Jank T, Aktories K, Schulz GE. Structural basis for the function of Clostridium difficile toxin B. J Mol Biol 2005, 351(5):973-981. 10.1016/j.jmb.2005.06.071, 16054646.
144. Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci USA 2009, 106(22):9063-9068. 10.1073/pnas.0900194106, 2690004, 19451630.
145. Fieldhouse RJ, Turgeon Z, White D, Merrill AR. Cholera- and anthrax-like toxins are among several new ADP-ribosyltransferases. PLoS Comput Biol 2010, 6(12):e1001029. 10.1371/journal.pcbi.1001029, 3000352, 21170356.
146. Otto H, Reche PA, Bazan F, Dittmar K, Haag F, Koch-Nolte F. In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 2005, 6:139. 10.1186/1471-2164-6-139, 1266365, 16202152.
147. Bazan JF, Koch-Nolte F. Sequence and structural links between distant ADP-ribosyltransferase families. Adv Exp Med Biol 1997, 419:99-107. 10.1007/978-1-4419-8632-0_12, 9193642.
148. de Souza RF, Aravind L. Identification of novel components of NAD-utilizing metabolic pathways and prediction of their biochemical functions. Mol Biosyst 2012, 8(6):1661-1677. 10.1039/c2mb05487f, 22399070.
149. Jorgensen R, Purdy AE, Fieldhouse RJ, Kimber MS, Bartlett DH, Merrill AR. Cholix toxin, a novel ADP-ribosylating factor from Vibrio cholerae. J Biol Chem 2008, 283(16):10671-10678. 10.1074/jbc.M710008200, 18276581.
150. Yates SP, Jorgensen R, Andersen GR, Merrill AR. Stealth and mimicry by deadly bacterial toxins. Trends Biochem Sci 2006, 31(2):123-133. 10.1016/j.tibs.2005.12.007, 16406634.
151. Reinert DJ, Carpusca I, Aktories K, Schulz GE. Structure of the mosquitocidal toxin from Bacillus sphaericus. J Mol Biol 2006, 357(4):1226-1236. 10.1016/j.jmb.2006.01.025, 16483607.
152. Hayashi S, Ishii T, Matsunaga T, Tominaga R, Kuromori T, Wada T, Shinozaki K, Hirayama T. The glycerophosphoryl diester phosphodiesterase-like proteins SHV3 and its homologs play important roles in cell wall organization. Plant Cell Physiol 2008, 49(10):1522-1535. 10.1093/pcp/pcn120, 18718934.
153. Kang TS, Georgieva D, Genov N, Murakami MT, Sinha M, Kumar RP, Kaur P, Kumar S, Dey S, Sharma S, et al. Enzymatic toxins from snake venom: structural characterization and mechanism of catalysis. FEBS J 2011, 278(23):4544-4576. 10.1111/j.1742-4658.2011.08115.x, 21470368.
154. Sandoval-Calderon M, Geiger O, Guan Z, Barona-Gomez F, Sohlenkamp C. A eukaryote-like cardiolipin synthase is present in Streptomyces coelicolor and in most actinobacteria. J Biol Chem 2009, 284(26):17383-17390. 10.1074/jbc.M109.006072, 2719378, 19439403.
155. Dowhan W. Molecular basis for membrane phospholipid diversity: why are there so many lipids?. Annu Rev Biochem 1997, 66:199-232. 10.1146/annurev.biochem.66.1.199, 9242906.
156. Nambu T, Minamino T, Macnab RM, Kutsukake K. Peptidoglycan-hydrolyzing activity of the FlgJ protein, essential for flagellar rod formation in Salmonella typhimurium. J Bacteriol 1999, 181(5):1555-1561. 93546, 10049388.
157. Henrissat B, Callebaut I, Fabrega S, Lehn P, Mornon JP, Davies G. Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. Proc Natl Acad Sci USA 1995, 92(15):7090-7094. 10.1073/pnas.92.15.7090, 41477, 7624375.
158. Copley RR, Bork P. Homology among (betaalpha)(8) barrels: implications for the evolution of metabolic pathways. J Mol Biol 2000, 303(4):627-641. 10.1006/jmbi.2000.4152, 11054297.
159. Aravind L, Koonin EV. DNA polymerase beta-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res 1999, 27(7):1609-1618. 10.1093/nar/27.7.1609, 148363, 10075991.
160. Potrykus K, Cashel M. (p)ppGpp still magical?. Annu Rev Microbiol 2008, 62:35-51. 10.1146/annurev.micro.62.081307.162903, 18454629.
161. Liu Q, Kriksunov IA, Graeff R, Munshi C, Lee HC, Hao Q. Crystal structure of human CD38 extracellular domain. Structure 2005, 13(9):1331-1339. 10.1016/j.str.2005.05.012, 16154090.
162. Guse AH, Lee HC. NAADP: a universal Ca2+ trigger. Sci Signal 2008, 1(44):re10. 10.1126/scisignal.144re10, 18984909.
163. Chini EN. CD38 as a regulator of cellular NAD: a novel potential pharmacological target for metabolic conditions. Curr Pharm Des 2009, 15(1):57-63. 10.2174/138161209787185788, 2883294, 19149603.
164. Iacovache I, van der Goot FG, Pernot L. Pore formation: an ancient yet complex form of attack. Biochim Biophys Acta 2008, 1778(7-8):1611-1623.
165. Gonzalez MR, Bischofberger M, Pernot L, van der Goot FG, Freche B. Bacterial pore-forming toxins: the (w)hole story?. Cell Mol Life Sci 2008, 65(3):493-507. 10.1007/s00018-007-7434-y, 17989920.
166. Rescher U, Gerke V. Annexins-unique membrane binding proteins with diverse functions. J Cell Sci 2004, 117(Pt 13):2631-2639.
167. Rohou A, Nield J, Ushkaryov YA. Insecticidal toxins from black widow spider venom. Toxicon 2007, 49(4):531-549. 10.1016/j.toxicon.2006.11.021, 2517654,2517654, 17210168.
168. Dulubova IE, Krasnoperov VG, Khvotchev MV, Pluzhnikov KA, Volkova TM, Grishin EV, Vais H, Bell DR, Usherwood PN. Cloning and structure of delta-latroinsectotoxin, a novel insect-specific member of the latrotoxin family: functional expression requires C-terminal truncation. J Biol Chem 1996, 271(13):7535-7543. 10.1074/jbc.271.13.7535, 8631785.
169. King JG, Vernick KD, Hillyer JF. Members of the salivary gland surface protein (SGS) family are major immunogenic components of mosquito saliva. J Biol Chem 2011, 286(47):40824-40834. 10.1074/jbc.M111.280552, 21965675.
170. Klasson L, Kambris Z, Cook PE, Walker T, Sinkins SP. Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics 2009, 10:33. 10.1186/1471-2164-10-33, 2647948, 19154594.
171. Aschtgen MS, Gavioli M, Dessen A, Lloubes R, Cascales E. The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall. Mol Microbiol 2010, 75(4):886-899. 10.1111/j.1365-2958.2009.07028.x, 20487285.
172. Parsons LM, Lin F, Orban J. Peptidoglycan recognition by Pal, an outer membrane lipoprotein. Biochemistry 2006, 45(7):2122-2128. 10.1021/bi052227i, 16475801.
173. Neumann U, Schiltz E, Stahl B, Hillenkamp F, Weckesser J. A peptidoglycan binding domain in the porin-associated protein (PAP) of Rhodospirillum rubrum FR1. FEMS Microbiol Lett 1996, 138(1):55-58. 10.1111/j.1574-6968.1996.tb08134.x, 8674970.
174. Park JS, Lee WC, Yeo KJ, Ryu KS, Kumarasiri M, Hesek D, Lee M, Mobashery S, Song JH, Kim SI, et al. Mechanism of anchoring of OmpA protein to the cell wall peptidoglycan of the gram-negative bacterial outer membrane. FASEB J 2012, 26(1):219-228. 10.1096/fj.11-188425, 21965596.
175. Babu MM, Priya ML, Selvan AT, Madera M, Gough J, Aravind L, Sankaran K. A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J Bacteriol 2006, 188(8):2761-2773. 10.1128/JB.188.8.2761-2773.2006, 1446993, 16585737.
176. Leipe DD, Koonin EV, Aravind L. STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol 2004, 343(1):1-28. 10.1016/j.jmb.2004.08.023, 15381417.
177. Schwefel D, Frohlich C, Eichhorst J, Wiesner B, Behlke J, Aravind L, Daumke O. Structural basis of oligomerization in septin-like GTPase of immunity-associated protein 2 (GIMAP2). Proc Natl Acad Sci USA 2010, 107(47):20299-20304. 10.1073/pnas.1010322107, 2996681, 21059949.
178. Velikovsky CA, Deng L, Tasumi S, Iyer LM, Kerzic MC, Aravind L, Pancer Z, Mariuzza RA. Structure of a lamprey variable lymphocyte receptor in complex with a protein antigen. Nat Struct Mol Biol 2009, 16(7):725-730. 10.1038/nsmb.1619, 2722044, 19543291.
179. Wolf YI, Rogozin IB, Kondrashov AS, Koonin EV. Genome alignment, evolution of prokaryotic genome organization, and prediction of gene function using genomic context. Genome Res 2001, 11(3):356-372. 10.1101/gr.GR-1619R, 11230160.
180. Koonin EV, Wolf YI, Aravind L. Prediction of the archaeal exosome and its connections with the proteasome and the translation and transcription machineries by a comparative-genomic approach. Genome Res 2001, 11(2):240-252. 10.1101/gr.162001, 311015, 11157787.
181. Poole SJ, Diner EJ, Aoki SK, Braaten BA, t'Kint de Roodenbeke C, Low DA, Hayes CS. Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 2011, 7(8):e1002217. 10.1371/journal.pgen.1002217, 3150448, 21829394.
182. Kampstra P. Beanplot: A Boxplot Alternative for Visual Comparison of Distributions. J Stat Softw 2008, 28(1):1-9.
183. Diner EJ, Beck CM, Webb JS, Low DA, Hayes CS. Identification of a target cell permissive factor required for contact-dependent growth inhibition (CDI). Genes Dev 2012, 26(5):515-525. 10.1101/gad.182345.111, 3305988, 22333533.
184. Iyer LM, Koonin EV, Aravind L. Evolution of bacterial RNA polymerase: implications for large-scale bacterial phylogeny, domain accretion, and horizontal gene transfer. Gene 2004, 335:73-88.
185. Vollmer W. Bacterial outer membrane evolution via sporulation?. Nat Chem Biol 2012, 8(1):14-18.
186. Simeone R, Bottai D, Brosch R. ESX/type VII secretion systems and their role in host-pathogen interaction. Curr Opin Microbiol 2009, 12(1):4-10. 10.1016/j.mib.2008.11.003, 19155186.
187. Pallen MJ, Chaudhuri RR, Henderson IR. Genomic analysis of secretion systems. Curr Opin Microbiol 2003, 6(5):519-527. 10.1016/j.mib.2003.09.005, 14572546.
188. Bateman A, Bycroft M. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol 2000, 299(4):1113-1119. 10.1006/jmbi.2000.3778, 10843862.
189. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, et al. The Pfam protein families database. Nucleic Acids Res 2010, 38(Database issue):D211-222. 2808889, 19920124.
190. Ponting CP, Aravind L, Schultz J, Bork P, Koonin EV. Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. J Mol Biol 1999, 289(4):729-745.
191. Wren BW. A family of clostridial and streptococcal ligand-binding proteins with conserved C-terminal repeat sequences. Mol Microbiol 1991, 5(4):797-803. 10.1111/j.1365-2958.1991.tb00752.x, 1830357.
192. Dean P. Functional domains and motifs of bacterial type III effector proteins and their roles in infection. FEMS Microbiol Rev 2011, 35(6):1100-1125. 10.1111/j.1574-6976.2011.00271.x, 21517912.
193. Hayes F, Van Melderen L. Toxins-antitoxins: diversity, evolution and function. Crit Rev Biochem Mol Biol 2011, 46(5):386-408. 10.3109/10409238.2011.600437, 21819231.
194. Ishikawa K, Fukuda E, Kobayashi I. Conflicts targeting epigenetic systems and their resolution by cell death: novel concepts for methyl-specific and other restriction systems. DNA Res 2010, 17(6):325-342. 10.1093/dnares/dsq027, 2993543, 21059708.
195. Iyer LM, Babu MM, Aravind L. The HIRAN domain and recruitment of chromatin remodeling and repair activities to damaged DNA. Cell Cycle 2006, 5(7):775-782. 10.4161/cc.5.7.2629, 16627993.
196. Iyer LM, Abhiman S, Aravind L. MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases. Biol Direct 2008, 3:8. 10.1186/1745-6150-3-8, 2292703, 18346280.
197. Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW. Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 2009, 33(2):376-393. 10.1111/j.1574-6976.2008.00136.x, 2704930, 19178566.
198. Nazina TN, Tourova TP, Poltaraus AB, Novikova EV, Grigoryan AA, Ivanova AE, Lysenko AM, Petrunyaka VV, Osipov GA, Belyaev SS, et al. Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. th. Int J Syst Evol Microbiol 2001, 51(Pt 2):433-446.
199. Viswanathan VK. Eating in, eating out. Gut Microbes 2010, 1(4):207-208. 10.4161/gmic.1.4.12321, 3023601, 21327026.
200. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA, Sahasrabudhe A, Dewhirst FE. Bacterial diversity in human subgingival plaque. J Bacteriol 2001, 183(12):3770-3783. 10.1128/JB.183.12.3770-3783.2001, 95255, 11371542.
201. Jain R, Poulos MG, Gros J, Chakravarty AK, Shuman S. Substrate specificity and mutational analysis of Kluyveromyces lactis gamma-toxin, a eukaryal tRNA anticodon nuclease. RNA 2011, 17(7):1336-1343. 10.1261/rna.2722711, 3138569, 21610213.
202. Klassen R, Paluszynski JP, Wemhoff S, Pfeiffer A, Fricke J, Meinhardt F. The primary target of the killer toxin from Pichia acaciae is tRNA(Gln). Mol Microbiol 2008, 69(3):681-697. 10.1111/j.1365-2958.2008.06319.x, 18532979.
203. Lu J, Huang B, Esberg A, Johansson MJ, Bystrom AS. The Kluyveromyces lactis gamma-toxin targets tRNA anticodons. RNA 2005, 11(11):1648-1654. 10.1261/rna.2172105, 1370851, 16244131.
204. Conticello SG. The AID/APOBEC family of nucleic acid mutators. Genome Biol 2008, 9(6):229. 10.1186/gb-2008-9-6-229, 2530864, 18671835.
205. Kanazawa T, Watanabe M, Matsushima-Hibiya Y, Kono T, Tanaka N, Koyama K, Sugimura T, Wakabayashi K. Distinct roles for the N- and C-terminal regions in the cytotoxicity of pierisin-1, a putative ADP-ribosylating toxin from cabbage butterfly, against mammalian cells. Proc Natl Acad Sci USA 2001, 98(5):2226-2231. 10.1073/pnas.051628898, 30120, 11226221.
206. Orth JH, Schorch B, Boundy S, ffrench-Constant R, Kubick S, Aktories K. Cell-free synthesis and characterization of a novel cytotoxic pierisin-like protein from the cabbage butterfly Pieris rapae. Toxicon 2011, 57(2):199-207. 10.1016/j.toxicon.2010.11.011, 21112350.
207. van Kooij M, de Groot K, van Vugt H, Aten J, Snoek M. Genotype versus phenotype: conflicting results in mapping a lung tumor susceptibility locus to the G7c recombination interval in the mouse MHC class III region. Immunogenetics 2001, 53(8):656-661. 10.1007/s00251-001-0381-0, 11797099.
208. Kumanovics A, Lindahl KF. G7c in the lung tumor susceptibility (Lts) region of the Mhc class III region encodes a von Willebrand factor type A domain protein. Immunogenetics 2001, 53(1):64-68. 10.1007/s002510100297, 11261934.
209. Taylor M, Mediannikov O, Raoult D, Greub G. Endosymbiotic bacteria associated with nematodes, ticks and amoebae. FEMS Immunol Med Microbiol 2012, 64(1):21-31. 10.1111/j.1574-695X.2011.00916.x, 22126456.
210. Yu C, Feng W, Wei Z, Miyanoiri Y, Wen W, Zhao Y, Zhang M. Myosin VI undergoes cargo-mediated dimerization. Cell 2009, 138(3):537-548. 10.1016/j.cell.2009.05.030, 19665975.
211. Zhang J, Xu LG, Han KJ, Shu HB. Identification of a ZU5 and death domain-containing inhibitor of NF-kappaB. J Biol Chem 2004, 279(17):17819-17825. 10.1074/jbc.M310737200, 14769797.
212. Georgiades K, Madoui MA, Le P, Robert C, Raoult D. Phylogenomic analysis of Odyssella thessalonicensis fortifies the common origin of Rickettsiales, Pelagibacter ubique and Reclimonas americana mitochondrion. PLoS One 2011, 6(9):e24857. 10.1371/journal.pone.0024857, 3177885, 21957463.
213. Fournier GP, Huang J, Gogarten JP. Horizontal gene transfer from extinct and extant lineages: biological innovation and the coral of life. Philos Trans R Soc Lond B Biol Sci 2009, 364(1527):2229-2239. 10.1098/rstb.2009.0033, 2873001, 19571243.
214. Wolf YI, Aravind L, Koonin EV. Rickettsiae and Chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends Genet 1999, 15(5):173-175. 10.1016/S0168-9525(99)01704-7, 10322483.
215. Iyer LM, Abhiman S, de Souza RF, Aravind L. Origin and evolution of peptide-modifying dioxygenases and identification of the wybutosine hydroxylase/hydroperoxidase. Nucleic Acids Res 2010, 38(16):5261-5279. 10.1093/nar/gkq265, 2938197, 20423905.
216. Aravind L, Abhiman S, Iyer LM. Natural history of the eukaryotic chromatin protein methylation system. Prog Mol Biol Transl Sci 2011, 101:105-176.
217. Smith EE, Sims EH, Spencer DH, Kaul R, Olson MV. Evidence for diversifying selection at the pyoverdine locus of Pseudomonas aeruginosa. J Bacteriol 2005, 187(6):2138-2147. 10.1128/JB.187.6.2138-2147.2005, 1064051, 15743962.
218. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
219. Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Inform 2009, 23(1):205-211.
220. Lassmann T, Frings O, Sonnhammer EL. Kalign2: high-performance multiple alignment of protein and nucleotide sequences allowing external features. Nucleic Acids Res 2009, 37(3):858-865. 10.1093/nar/gkn1006, 2647288, 19103665.
221. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 2004, 5:113.
222. Pei J, Sadreyev R, Grishin NV. PCMA: fast and accurate multiple sequence alignment based on profile consistency. Bioinformatics 2003, 19(3):427-428. 10.1093/bioinformatics/btg008, 12584134.
223. Cole C, Barber JD, Barton GJ. The Jpred 3 secondary structure prediction server. Nucleic Acids Res 2008, 36(Web Server issue):W197-201. 2447793, 18463136.
224. Buchan DW, Ward SM, Lobley AE, Nugent TC, Bryson K, Jones DT. Protein annotation and modelling servers at University College London. Nucleic Acids Res 2010, 38(Web Server issue):W563-568. 2896093, 20507913.
225. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305(3):567-580. 10.1006/jmbi.2000.4315, 11152613.
226. Kall L, Krogh A, Sonnhammer EL. Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server. Nucleic Acids Res 2007, 35(Web Server issue):W429-432. 1933244, 17483518.
227. Soding J, Biegert A, Lupas AN. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005, 33(Web Server issue):W244-248. 1160169, 15980461.
228. Holm L, Kaariainen S, Rosenstrom P, Schenkel A. Searching protein structure databases with DaliLite v. 3. Bioinformatics 2008, 24(23):2780-2781. 10.1093/bioinformatics/btn507, 2639270, 18818215.
229. Price MN, Dehal PS, Arkin AP. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 2010, 5(3):e9490. 10.1371/journal.pone.0009490, 2835736, 20224823.
230. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996, 14(1):33-38. 10.1016/0263-7855(96)00018-5, 8744570.