The Intracellular Citrus Huanglongbing Bacterium, 'Candidatus Liberibacter asiaticus' Encodes Two Novel Autotransporters

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Hao, Guixia ^a   Boyle, Michael ^b   Zhou, Lijuan ^a   Duan, Yongping ^a  

^a U S HORTICULTURAL RESEARCH LABORATORY   (United States)

^b SMITHSONIAN MARINE STATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CANDIDATUS LIBERIBACTER ASIATICUS AI PROTEIN; CANDIDATUS LIBERIBACTER ASIATICUS AII PROTEIN; GREEN FLUORESCENT PROTEIN; MONOCLONAL ANTIBODY; PROTEINASE K; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; BACTERIAL PLANT DISEASE; BACTERIUM; BIOINFORMATICS; CANDIDATUS LIBERIBACTER ASIATICUS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA SEQUENCE; ESCHERICHIA COLI; GENE; GENE EXPRESSION; GENE FUSION; GENE SILENCING; GREEN FLUORESCENT PROTEIN GENE; IMMUNOBLOTTING; NONHUMAN; NUCLEOTIDE SEQUENCE; P19 GENE; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN TARGETING;

ALPHAPROTEOBACTERIA; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CITRUS; COMPUTATIONAL BIOLOGY; ESCHERICHIA COLI; GREEN FLUORESCENT PROTEINS; MITOCHONDRIA; PLANT DISEASES; PLANT LEAVES; PROTEIN STRUCTURE, TERTIARY; TOBACCO; VIRULENCE FACTORS;

EID: 84880080875     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068921     Document Type: Article

References (44)

1. Henderson IR, Navarro-Garcia F, Nataro JP, (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6: 370-378. doi:10.1016/S0966-842X(98)01318-3. PubMed: 9778731.
2. Scott-Tucker A, Henderson IR, (2009) In Bacterial secreted proteins: Secretory mechanisms and role in pathogensis, Wooldridge K, eds. Nottingham, UK. pp. pp. 139-157.
3. Oomen CJ, van Ulsen P, van Gelder P, Feijen M, Tommassen J, et al. (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J 23: 1257-1266. doi:10.1038/sj.emboj.7600148. PubMed: 15014442.
4. St Geme JW, Cutter D, (2000) The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J Bacteriol 182: 6005-6013. doi:10.1128/JB.182.21.6005-6013.2000. PubMed: 11029419.
5. Nummelin H, Merckel MC, Leo JC, Lankinen H, Skurnik M, et al. (2004) The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel beta-roll. EMBO J 23: 701-711. doi:10.1038/sj.emboj.7600100. PubMed: 14765110.
6. Laarmann S, Cutter D, Juehne T, Barenkamp SJ, St Geme JW, (2002) The Haemophilus influenzae Hia autotransporter harbours two adhesive pockets that reside in the passenger domain and recognize the same host cell receptor. Mol Microbiol 46: 731-743. doi:10.1046/j.1365-2958.2002.03189.x. PubMed: 12410830.
7. Hendrixson DR, de la Morena ML, Stathopoulos C, St Geme JW, (1997) Structural determinants of processing and secretion of the Haemophilus influenzae hap protein. Mol Microbiol 26(3):: 505-518. doi:10.1046/j.1365-2958.1997.5921965.x. PubMed: 9402021.
8. Surana NK, Cutter D, Barenkamp SJ, St Geme JW, (2004) The Haemophilus influenzae Hia autotransporter contains an unusually short trimeric translocator domain. J Biol Chem 279: 14679-14685. doi:10.1074/jbc.M311496200. PubMed: 14726537.
9. Roggenkamp A, Ham JH, Deng WL, Doyle JJ, Collmer A, (2003) Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol 185: 3735-3744. doi:10.1128/JB.185.13.3735-3744.2003. PubMed: 12813066.
10. Kim DSH, Chao Y, Saier MH, (2007) Protein-translocating trimeric autotransporters of Gram-Negative bacteria. J Bacteriol 188: 5655-5667. PubMed: 16885434.
11. Jain S, van Ulsen P, Benz I, Schmidt MA, Fernandez R, et al. (2006) Polar localization of the autotransporter family of large bacterial virulence proteins. J Bacteriol 188: 4841-4850. doi:10.1128/JB.00326-06. PubMed: 16788193.
12. Müller JEN, Papic D, Ulrich T, Grin I, Schütz M, et al. (2011) Mitochondria can recognize and assemble fragments of a β-barrel structure. Mol Biol Cell 22: 1638-1647. doi:10.1091/mbc.E10-12-0943. PubMed: 21460184.
13. Gottwald TR, (2010) Current epidemiological understanding of citrus huanglongbing. Annu Rev Phytopathol 48: 119-139. doi:10.1146/annurev-phyto-073009-114418. PubMed: 20415578.
14. Jagoueix S, Bove JM, Garnier M, (1994) The phloem-limited bacterium of greening disease of citrus is a member of the subdivision of the proteobacteria. Int J Syst Bacteriol 44: 379-386. doi:10.1099/00207713-44-3-379. PubMed: 7520729.
15. Duan YP, Zhou LJ, Hall DG, Li WB, Doddapaneni H, et al. (2009) Complete genome sequence of citrus huanglongbing bacterium, 'Candidatus Liberibacter asiaticus' obtained through metagenomics. Mol Plant Microbe Interact 22: 1011-1020. doi:10.1094/MPMI-22-8-1011. PubMed: 19589076.
16. Zhang SJ, Flores-Cruz Z, Zhou LJ, Kang BH, Fleites LA, et al. (2011) 2011) Ca. Liberibacter asiaticus carries an excision plasmid prophage and a chromosomally integrated prophage that becomes lytic in plant. Mol Plant Microbe Interact 24: 458-468. doi:10.1094/MPMI-11-10-0256. PubMed: 21190436.
17. Zhou LJ, Powell CA, Hoffman MT, Li WB, Fan G, et al. (2011) Diversity and plasticity of the intracellular plant pathogen and insect symbiont "Candidatus Liberibacter asiaticus" as revealed by hypervariable prophage genes with intragenic tandem repeats. Appl Environ Microbiol 77: 6663-6673. doi:10.1128/AEM.05111-11. PubMed: 21784907.
18. Boyd EF, Brüssow H, (2002) Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol 10: 521-529. doi:10.1016/S0966-842X(02)02459-9. PubMed: 12419617.
19. Vahling CM, Duan Y, Lin H, (2010) Characterization of an ATP translocase identified in the destructive plant pathogen "Candidatus Liberibacter asiaticus". J Bacteriol 192: 834-840. doi:10.1128/JB.01279-09. PubMed: 19948801.
20. Liu L, Botos I, Wang Y, Leonard JN, Shiloach J, et al. (2008) Toll-like receptor 3 (TLR3) recognizes double-stranded RNA (dsRNA), a molecular signature of most viruses, and triggers inflammatory responses that prevent viral spread. Science 320: 379-381. doi:10.1126/science.1155406. PubMed: 18420935.
21. Zhang Y, (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40. doi:10.1186/1471-2105-9-40. PubMed: 18215316.
22. Akula N, Zheng H, Han FQ, Wang N, (2011) Discovery of novel SecA inhibitors of Candidatus Liberibacter asiaticus by structure based design. Bioorg Med Chem Lett 21: 4183-4188. doi:10.1016/j.bmcl.2011.05.086. PubMed: 21684161.
23. Rojas CM, Ham JH, Deng WL, Doyle JJ, Collmer A, (2004) HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. Proc Natl Acad Sci USA 99: 13142-13147.
24. Matsumoto A, Huston SL, Killiny N, Igo MM, (2010) XatA, an AT-1 autotransporter important for the virulence of Xylella fastidiosa Temecula1. Microbiologyopen 1: 33-45. PubMed: 22950010.
25. Nicolay T, Devleeschouwer K, Vanderleyden J, Spaepen S, (2012) Characterization of esterase A, a Pseudomonas stutzeri A15 autotransporter. Appl Environ Microbiol 78: 2533-2542. doi:10.1128/AEM.07690-11. PubMed: 22307303.
26. Szczesny P, Lupas A, (2008) Domain annotation of trimeric autotransporter adhesions-data. Bioinformatics 24: 1251-1256. doi:10.1093/bioinformatics/btn118. PubMed: 18397894.
27. Charles M, Pérez M, Kobil JH, Goldberg MB, (2001) Polar targeting of Shigella virulence factor IcsA in Enterobacteriacae and Vibrio. Proc Natl Acad Sci USA 98: 9871-9876. doi:10.1073/pnas.171310498. PubMed: 11481451.
28. Goldberg MB, Bârzu O, Parsot C, Sansonetti PJ, (1993) Unipolar localization and ATPase activity of IcsA, a Shigella flexneri protein involved in intracellular movement. J Bacteriol 175: 2189-2196. PubMed: 8468279.
29. Hammond SM, Caudy AA, Hannon GJ, (2001) Post-transcriptional gene silencing by double-stranded RNA. Nat Rev Genet 2: 110-119. doi:10.1038/35052556. PubMed: 11253050.
30. Johansen LK, Carrington JC, (2001) Silencing on the spot induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol 126: 930-938. doi:10.1104/pp.126.3.930. PubMed: 11457942.
31. Silhavy D, Molnár A, Lucioli A, Szittya G, Hornyik C, et al. (2002) A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21: 3070-3080. doi:10.1093/emboj/cdf312. PubMed: 12065420.
32. Domańska G, Motz C, Meinecke M, Harsman A, Papatheodorou P, et al. (2010) Helicobacter pylori VacA Toxin/Subunit p34: Targeting of an Anion Channel to the Inner Mitochondrial Membrane. PLOS Pathog 6: e1000878. doi:10.1371/journal.ppat. 1000878.
33. Rudel T, Kepp O, Kozjak-Pavlovic V, (2010) Interactions between bacterial pathogens and mitochondrial cell death pathways. Nat Rev 8: 693-705. doi:10.1038/nrmicro2421. PubMed: 20818415.
34. Ikegami A, Honma K, Sharma A, Kuramitsu HK, (2004) Multiple functions of the leucine-rich repeat protein LrrA of Treponema denticola. Infect Immun 72: 4619-4627. doi:10.1128/IAI.72.8.4619-4627.2004. PubMed: 15271922.
35. Kobe B, Deisenhofer J J, (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19: 415-421. doi:10.1016/0968-0004(94)90090-6. PubMed: 7817399.
36. Schubert WD, Urbanke C, Ziehm T, Beier V, Machner MP, et al. (2002) Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell 111: 825-836. doi:10.1016/S0092-8674(02)01136-4. PubMed: 12526809.
37. Onishi S, Honma K, Liang S, Stathopoulou P, Kinane D, et al. (2008) Toll-like receptor 2-mediated interleukin-8 expression in gingival epithelial cells by the Tannerella forsythiae leucine-rich repeat protein BspA. Infect Immun 76: 198-205. doi:10.1128/IAI.01139-07. PubMed: 17967853.
38. Iyer D, Anaya-Bergman C, Jones K, Yanamandra S, Sengupta D, et al. (2010) AdpC is a Prevotella intermedia 17 Leucine-Rich Repeat Internalin-Like Protein. Infect Immun 78: 2385-2396. doi:10.1128/IAI.00510-09. PubMed: 20308299.
39. Zou H, Gowda S, Zhou LJ, Hajeri S, Chen GY, et al. (2012) The destructive citrus pathogen, 'Candidatus Liberibacter asiaticus' encodes a functional flagellin characteristic of a pathogen-associated molecular pattern. PLOS ONE 7(9):: e46447. doi:10.1371/journal.pone.0046447. PubMed: 23029520.
40. Goodin MM, Dietzgen RG, Schichnes D, Ruzin S, Jackson AO, (2002) pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J 31: 375-383. doi:10.1046/j.1365-313X.2002.01360.x. PubMed: 12164816.
41. Caldwell RB, Lattemann CT, (2004) Simple and reliable method to precipitate protein from bacterial culture supernatant. Appl Environ Microbiol 70: 610-612. doi:10.1128/AEM.70.1.610-612.2004. PubMed: 14711696.
42. Carroll JA, (2010) Methods of identifying membrane proteins in spirochetes. Curr Protoc Microbiol 16: 12C. PubMed: 20131222.
43. Carlone GM, Thomas ML, Rumschlag HS, Sottnek FO, (1986) Rapid microprocedure for isolating detergent-insoluble outer membrane proteins from Haemophilus species. J Clin Microbiol 24: 330-332. PubMed: 3489731.
44. Koh EL, Zhou LJ, Williams DS, Park J, Ding N, et al. (2011) Callose deposition in the phloem plasmodesmata and inhibition of phloem transport in citrus leaves infected with "Candidatus Liberibacter asiaticus". Protoplasma 249: 687-697. PubMed: 21874517.