Identification and functional analysis of the S-layer protein SplA of Paenibacillus larvae, the causative agent of American Foulbrood of honey bees

PLoS Pathogens

Volumn 8, Issue 5, 2012, Pages

  Poppinga, Lena ^a   Janesch, Bettina ^b   Fünfhaus, Anne ^a   Sekot, Gerhard ^b   Garcia Gonzalez, Eva ^a   Hertlein, Gillian ^a   Hedtke, Kati ^a   Schäffer, Christina ^b   Genersch, Elke ^a  

^a Institute for Bee Research   (Germany)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN SPIA; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; S LAYER PROTEINS; S-LAYER PROTEINS; VIRULENCE FACTOR;

AMERICAN FOULBROOD; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; GENE DISRUPTION; GENE EXPRESSION; HONEYBEE; NONHUMAN; NUCLEOTIDE SEQUENCE; PAENIBACILLUS; PAENIBACILLUS LARVAE; PROTEIN ASSEMBLY; PROTEIN FUNCTION; SEQUENCE ANALYSIS; SPIA GENE; ANIMAL; BEE; CELL CULTURE; CHEMISTRY; GENE INACTIVATION; GENETICS; GENOTYPE; LARVA; METABOLISM; MICROBIOLOGY; PATHOGENICITY; SEQUENCE ALIGNMENT;

APIS MELLIFERA; BACTERIA (MICROORGANISMS); PAENIBACILLUS LARVAE; POSIBACTERIA;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BEES; CELLS, CULTURED; GENE KNOCKOUT TECHNIQUES; GENOTYPE; LARVA; MEMBRANE GLYCOPROTEINS; PAENIBACILLUS; SEQUENCE ALIGNMENT; VIRULENCE FACTORS;

EID: 84863659604     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002716     Document Type: Article

References (68)

1. Aizen M, Garibaldi L, Cunningham S, Klein A, (2008) Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr Biol 18: 1572-1575.
2. Aizen MA, Harder LD, (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19: 915-918.
3. Genersch E, (2010) Honey bee pathology: Current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87: 87-97.
4. Genersch E, Evans JD, Fries I, (2010) Honey bee disease overview. J Invertebr Pathol 103: S2-S4.
5. Genersch E, Forsgren E, Pentikäinen J, Ashiralieva A, Rauch S, et al. (2006) Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int J Syst Evol Microbiol 56: 501-511.
6. Yue D, Nordhoff M, Wieler LH, Genersch E, (2008) Fluorescence in situ-hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environ Microbiol 10: 1612-1620.
7. Genersch E, (2010) American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invertebr Pathol 103: S10-S19.
8. Genersch E, (2007) Paenibacillus larvae and American foulbrood in honeybees. Berl Münch Tierärztl Wschr 120: 26-33.
9. Genersch E, (2008) Paenibacillus larvae and American foulbrood - long since known and still surprising. J Verbr Lebensm 3: 429-434.
10. Versalovic J, Schneider M, de Bruijn FJ, Lupski JR, (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5: 25-40.
11. Genersch E, Otten C, (2003) The use of repetitive element PCR fingerprinting (rep-PCR) for genetic subtyping of German field isolates of Paenibacillus larvae subsp. larvae. Apidologie 34: 195-206.
12. Neuendorf S, Hedtke K, Tangen G, Genersch E, (2004) Biochemical characterization of different genotypes of Paenibacillus larvae subsp. larvae, a honey bee bacterial pathogen. Microbiology 150: 2381-2390.
13. Genersch E, Ashiralieva A, Fries I, (2005) Strain- and genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, the causative agent of American foulbrood disease in honey bees. Appl Environ Microbiol 71: 7551-7555.
14. Rauch S, Ashiralieva A, Hedtke K, Genersch E, (2009) Negative correlation between individual-insect-level virulence and colony-level virulence of Paenibacillus larvae, the etiological agent of American foulbrood of honeybees. Appl Environ Microbiol 75: 3344-3347.
15. Peters M, Kilwinski J, Beringhoff A, Reckling D, Genersch E, (2006) American foulbrood of the honey bee: Occurrence and distribution of different genotypes of Paenibacillus larvae in the administrative district of Arnsberg (North Rhine-Westphalia). J Vet Med B 53: 100-104.
16. Loncaric I, Derakhshifar I, Oberlerchner JT, Köglberger H, Moosbeckhofer R, (2009) Genetic diversity among isolates of Paenibacillus larvae from Austria. J Invertebr Pathol 100: 44-46.
17. Alippi AM, Lopez AC, Aguilar OM, (2004) A PCR-based method that permits specific detection of Paenibacillus larvae subsp. larvae, the cause of American Foulbrood of honey bees, at the subspecies level. Lett Appl Microbiol 39: 25-33.
18. Holst EC, Sturtevant AP, (1940) Relation of proteolytic enzymes to phase of life cycle of Bacillus larvae and two new culture media for this organism. Bacteriol 40: 723-731.
19. Dancer BN, Chantawannakul P, (1997) The proteases of American foulbrood scales. J Invertebr Pathol 70: 79-87.
20. Antúnez K, Anido M, Schlapp G, Evans JD, Zunino P, (2009) Characterization of secreted proteases of Paenibacillus larvae, potential virulence factors involved in honeybee larval infection. J Invertebr Pathol 102: 129-132.
21. Jarosz J, Glinski Z, (1990) Selective inhibition of cecropin-like activity of insect immune blood by proteases from American foulbrood scales. J Invertebr Pathol 56: 143-149.
22. Antunez K, Anido M, Arredondo D, Evans JD, Zunino P, (2011) Paenibacillus larvae enolase as a virulence factor in honeybee larvae infection. Vet Microbiol 147: 83-89.
23. Qin X, Evans JD, Aronstein KA, Murray KD, Weinstock GM, (2006) Genome sequence of the honey bee pathogens Paenibacillus larvae and Ascosphaera apis. Insect Mol Biol 15: 715-718.
24. Fünfhaus A, Ashiralieva A, Borriss R, Genersch E, (2009) Use of suppression subtractive hybridization to identify genetic differences between differentially virulent genotypes of Paenibacillus larvae, the etiological agent of American Foulbrood of honeybees. Environ Microbiol Rep 1: 240-250.
25. Fünfhaus A, Genersch E, (2012) Proteome analysis of Paenibacillus larvae reveals the existence of a putative S-layer protein. Environ Microbiol Rep 4: 194-202.
26. Sleytr UB, Egelseer EM, Ilk N, Pum D, Schuster B, (2007) S-Layers as a basic building block in a molecular construction kit. FEBS J 274: 323-334.
27. Sleytr UB, Huber C, Ilk N, Pum D, Schuster B, et al. (2007) S-layers as a tool kit for nanobiotechnological applications. FEMS Microbiol Lett 267: 131-144.
28. Mesnage S, Tosi-Couture E, Mock M, Gounon P, Fouet A, (1997) Molecular characterization of the Bacillus anthracis main S-layer component: Evidence that it is the major cell-associated antigen. Mol Microbiol 23: 1147-1155.
29. Chitlaru T, Ariel N, Zvi A, Lion M, Velan B, et al. (2004) Identification of chromosomally encoded membranal polypeptides of Bacillus anthracis by a proteomic analysis: Prevalence of proteins containing S-layer homology domains. Proteomics 4: 677-691.
30. Fouet A, (2009) The surface of Bacillus anthracis. Mol Aspects Med 30: 374-385.
31. Kelly CP, LaMont JT, (1998) Clostridium difficile infection. Annu Rev Med 49: 375-390.
32. Calabi E, Calabi F, Phillips AD, Fairweather NF, (2002) Binding of Clostridium difficile surface layer proteins to gastrointestinal tissues. Infect Immun 10: 5770-5778.
33. Cerquetti M, Serafino A, Sebastianelli A, Mastrantonio P, (2002) Binding of Clostridium difficile to Caco-2 epithelial cell line and to extracellular matrix proteins. FEMS Immunol Med Microbiol 32: 211-218.
34. Ausiello CM, Cerquetti M, Fedele G, Spensieri F, Palazzo R, et al. (2006) Surface layer proteins from Clostridium difficile induce inflammatory and regulatory cytokines in human monocytes and dendritic cells. Microb Infect 8: 2640-2646.
35. Sakakibara J, Nagano K, Murakami Y, Higuchi N, Nakamura H, et al. (2007) Loss of adherence ability to human gingival epithelial cells in S-layer protein-deficient mutants of Tannerella forsythensis. Microbiology 153: 866-876.
36. Sekot G, Posch G, Messner P, Matejka M, Rausch-Fan X, et al. (2011) Potential of the Tannerella forsythia S-layer to delay the immune response. J Dent Res 90: 109-114.
37. Kesavalu L, Holt SC, Crawley RR, Borinski R, Ebersole JL, (1991) Virulence of Wolinella recta in a murine abscess model. Infect Immun 59: 2806-2817.
38. Grogono-Thomas R, Blaser MJ, Ahmadi M, Newell DG, (2003) Role of S-layer protein antigenic diversity in the immune responses of sheep experimentally challenged with Campylobacter fetus subsp fetus. Infect Immun 71: 147-154.
39. Ishiguro EE, Kay WW, Ainsworth T, Chamberlain JB, Austen RA, et al. (1981) Loss of virulence during culture of Aeromonas salmonicida at high temperature. J Bacteriol 148: 333-340.
40. Pena G, Miranda-Rios J, de la Riva G, Pardo-López L, Soberón M, et al. (2006) A Bacillus thuringiensis S-layer protein involved in toxicity against Epilachna varivestis (Coleoptera: Coccinellidae). Appl Environ Microbiol 72: 353-360.
41. Dingman DW, Stahly DP, (1983) Medium promoting sporulation of Bacillus larvae and metabolism of medium components. Appl Environ Microbiol 46: 860-869.
42. Zarschler K, Janesch B, Pabst M, Altmann F, Messner P, et al. (2010) Protein tyrosine O-glycosylation - A rather unexplored prokaryotic glycosylation system. Glycobiology 20: 787-798.
43. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-33402.
44. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular cloning: a laboratory manual Cold Spring Harbor Cold Spring Harbor Laboratory Press.
45. Messner P, Pum D, Sara M, Stetter KO, Sleytr UB, (1986) Ultrastructure of the cell envelope of the archaebacteria Thermoproteus tenax and Thermoproteus neutrophilus. J Bacteriol 166: 1046-1054.
46. Wrigley NG, (1986) The lattice spacing of crystalline catalase as an internal standard of length in electron microscopy. J Ultrastruct Res 24: 454-464.
47. Amos LA, Henderson R, Unwin PNT, (1982) Three-dimensional structure determination by electron micrsocopy of two-dimensional crystals. Progr Biophys Mol Biol 39: 183-231.
48. Saxton WO, (1996) Semper: Distortion compensation, selective averaging, 3-D reconstruction, and transfer function correction in a highly programmable system. J Struct Biol 116: 230-236.
49. Zarschler K, Janesch B, Zayni S, Schäffer C, Messner P, (2009) Construction of a gene knockout system for application in Paenibacillus alvei CCM 2051T, exemplified by the S-layer glycan biosynthesis initiation enzyme WsfP. Appl Environ Microbiol 75: 3077-3085.
50. Novotny R, Schäffer C, Strauss J, Messner P, (2004) S-layer glycan-specific loci on the chromosome of Geobacillus stearothermophilus NRS 2004/3a and dTDP-L-rhamnose biosynthesis potential of G. stearothermophilus strains. Microbiology 150: 953-965.
51. Murray KD, Aronstein KA, (2008) Transformation of the Gram-positive honey bee pathogen, Paenibacillus larvae, by electroporation. J Microbiol Meth 75: 325-328.
52. Poppinga L, Genersch E, (2012) Heterologous expression of green fluorescent protein in Paenibacillus larvae, the causative agent of American Foulbrood of honey bees. J Appl Microbiol 112: 430-435.
53. Grünewald B, Wersing A, (2008) An ionotropic GABA receptor in cultured mushroom body Kenyon cells of the honeybee and its modulation by intracellular calcium. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 194: 329-340.
54. Manetti AGO, Koeller T, Becherelli M, Buccato S, Kreikemeyer B, et al. (2010) Environmental acidification drives S. pyogenes pilus expression and microcolony formation on epithelial cells in a FCT-dependent manner. PLoS ONE 5: e13864.
55. Thomas SR, Elkinton JS, (2004) Pathogenicity and virulence. J Invertebr Pathol 85: 146-151.
56. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, et al. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37: 205-210.
57. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, et al. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: 225-229.
58. Marchler-Bauer A, Bryant SH, (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32: 327-331.
59. Sára M, Sleytr UB, (2000) S-layer proteins. J Bacteriol 182: 859-868.
60. Diatchenko L, Lau Y, Campbell A, Chenchik A, Moqadam F, et al. (1996) Suppression subtractive hybridization: A method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci U S A 93: 6025-6030.
61. Petersen TN, Brunak S, von Heijne G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
62. Boot HJ, Pouwels PH, (1996) Expression, secretion and antigenic variation of bacterial S-layer proteins. Mol Microbiol 21: 1117-1123.
63. Mesnage S, Fontaine T, Mignot T, Delepierre M, Mock M, et al. (2000) Bacterial SLH domain proteins are non-covalently anchored to the cell surface via a conserved mechanism involving wall polysaccharide pyruvylation. EMBO J 19: 4473-4484.
64. Mesnage S, Tosi-Couture E, Fouet A, (1999) Production and cell surface anchoring of functional fusions between the SLH motifs of the Bacillus anthracis S-layer proteins and the Bacillus subtilis levansucrase. Mol Microbiol 31: 927-936.
65. Sleytr UB, Messner P, Pum D, Sara M, (1993) Crystalline bacterial cell surface layers. Mol Microbiol 10: 911-916.
66. Etienne-Toumelin I, Sirard JC, Duflot E, Mock M, Fouet A, (1995) Characterization of the Bacillus anthracis S-layer: cloning and sequencing of the structural gene. J Bacteriol 177: 614-620.
67. Messner P, Schäffer C, Egelseer EM, Sleytr UB, (2010) Occurrence, structure, chemistry, genetics, morphogenesis, and functions of S-Layers. In: König H, editors. Prokaryotic Cell Wall Compounds Berlin Heidelberg Springer-Verlag.
68. Sillanpää J, Martínez B, Antikainen J, Toba T, Kalkkinen N, et al. (2000) Characterization of the collagen-binding S-layer protein CbsA of Lactobacillus crispatus. J Bacteriol 182: 6440-6450.