How to kill the honey bee larva: Genomic potential and virulence mechanisms of Paenibacillus larvae

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Djukic, Marvin ^a   Brzuszkiewicz, Elzbieta ^a   Fünfhaus, Anne ^b   Voss, Jörn ^a   Gollnow, Kathleen ^a   Poppinga, Lena ^b   Liesegang, Heiko ^a   Garcia Gonzalez, Eva ^b   Genersch, Elke ^b   Daniel, Rolf ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b Institute for Bee Research   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; CHITINASE; FRUCTOSE; GLUCOSE; INTEGRASE; RECOMBINASE; SERINE PROTEINASE; TRANSPOSASE;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CARBOHYDRATE METABOLISM; DNA FRAGMENTATION; ENERGY METABOLISM; ENZYME DEGRADATION; GENE DISRUPTION; GENE IDENTIFICATION; GENE NUMBER; GENE SEQUENCE; GENE TRANSFER; GENETIC VARIABILITY; GENOME SIZE; HONEYBEE; NONHUMAN; NUCLEOTIDE SEQUENCE; PAENIBACILLUS; PAENIBACILLUS LARVAE; PLASTICITY; POINT MUTATION; SERINE PROTEASE GENE;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BASE COMPOSITION; BEES; BIOSYNTHETIC PATHWAYS; CHROMOSOMES, BACTERIAL; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; GENETIC LOCI; GENOME, BACTERIAL; GENOMIC ISLANDS; GENOMICS; LARVA; MODELS, BIOLOGICAL; MULTIGENE FAMILY; PAENIBACILLUS; VIRULENCE;

EID: 84897126141     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090914     Document Type: Article

References (88)

1. Morse RA, Calderon NW (2000) The value of honey bees as pollinators of U.S. Crops in 2000. Bee Culture 128: 1-15.
2. 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.
3. 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.
4. Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotech 87: 87-97.
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. Brodsgaard CJ, Ritter W, Hansen H (1998) Response of in vitro reared honey bee larvae to various doses of Paenibacillus larvae larvae spores. Apidologie 29: 569-578. (Pubitemid 29014277)
7. 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. (Pubitemid 43194253)
8. Yue D, Nordhoff M, Wieler LH, Genersch E (2008) Fluorescence in situhybridization (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. (Pubitemid 351670260)
9. Garcia-Gonzalez E, Genersch E (2013) Honey bee larval peritrophic matrix degradation during infection with Paenibacillus larvae, the etiological agent of American Foulbrood of honey bees, is a key step in pathogenesis. Environ Microbiol 15, 2894-2901.
10. 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. (Pubitemid 36647095)
11. Forsgren E, Stevanovic J, Fries I (2008) Variability in germination and in temperature and storage resistance among Paenibacillus larvae genotypes. Vet Microbiol 129: 342-349.
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. (Pubitemid 39117649)
13. 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.
14. Alippi AM, Reynaldi FJ, Lopez AC, De Giusti MR, Aguilar OM (2004) Molecular epidemiology of Paenibacillus larvae larvae and incidence of American foulbrood in Argentinean honeys from Buenos Aires province. J Apic Res 43: 135-143. (Pubitemid 39584079)
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. (Pubitemid 44400589)
16. 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.
17. 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.
18. Genersch E (2007) Paenibacillus larvae and American foulbrood in honeybees. Berl Münch Tierärztl Wschr 120: 26-33.
19. Genersch E (2010) American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invertebr Pathol 103: S10-S19.
20. Qin X, Evans JD, Aronstein KA, Murray KD, Weinstock GM (2006) Genome sequences of the honey bee pathogens Paenibacillus larvae and Ascosphaera apis. Insect Mol Biol 15: 715-718. (Pubitemid 44652096)
21. Chan QW, Cornman RS, Birol I, Liao NY, Chan SK, et al. (2011) Updated genome assembly and annotation of Paenibacillus larvae, the agent of American foulbrood disease of honey bees. BMC Genomics 12: 450.
22. Zhou Y, Liang Y, Lynch K, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39 (suppl 2): W347-W352.
23. Mahillon J, Leonard C, Chandler M (1999) IS elements as constituents of bacterial genomes. Res Microbiol 150: 675-687. (Pubitemid 30035888)
24. Siguier P, Filée J, Chandler M (2006) Insertion sequences in prokaryotic genomes. Curr Opin Microbiol 9: 526-531. (Pubitemid 44419502)
25. Brodschneider R, Crailsheim K (2010) Nutrition and health in honey bees. Apidologie 41: 278-294.
26. Graham JM, editor (1992) The hive and the honey bee. Hamilton, IL: Dadant & Sons.
27. Woodring J, Boulden M, Das S, Gäde G (1993) Studies on blood sugar homeostasis in the honeybee (Apis mellifera, L.). J Insect Physiol 39: 89-97.
28. 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.
29. Barth H, Aktories K, Popoff MR, Stiles BG (2004) Binary bacterial toxins: biochemistry, biology, and applications of common Clostridium and Bacillus proteins. Microbiol Mol Biol Rev 68: 373-402. (Pubitemid 39238275)
30. Poppinga L, Janesch B, Fünfhaus A, Sekot G, Garcia-Gonzalez E, et al. (2012) Identification and functional analysis of the S-layer protein SplA of Paenibacillus larvae, the causative agent of American foulbrood of honey bees. PLoS Pathog. 8: e1002716.
31. Fünfhaus A, Poppinga L, Genersch E (2013) Identification and characterization of two novel toxins expressed by the lethal honey bee pathogen Paenibacillus larvae, the causative agent of American foulbrood. Environ Microbiol doi:10.1111/1462-2920.12229.
32. Schirmer J, Just I, Aktories K (2002) The ADP-ribosylating mosquitocidal toxin from Bacillus sphaericus - proteolytic activiation, enzyme activity, and cytotoxic effects. J Biol Chem 277: 11941-11948. (Pubitemid 34952753)
33. Watanabe M, Enomoto S, Takamura-Enya T, Nakano T, Koyama K, et al. (2004) Enzymatic properties of Pierisin-1 and its N-terminal domain, a guaninespecific ADP-ribosyltransferase from the cabbage butterfly. J Biochem 135: 471-477. (Pubitemid 38660933)
34. Lúquez C, Raphael BH, Maslanka SE (2009) Neurotoxin gene clusters in Clostridium botulinum type Ab strains. Appl Environ Microbiol 75: 6094-6101.
35. Nakano H, Okabe T, Hashimoto H, Sakaguchi G (1990) Incidence of Clostridium botulinum in honey of various origins. Jpn J Med Sci Biol 43: 183-195.
36. Snowdon JA, Cliver DO (1996) Microorganisms in honey. Int J Food Microbiol 31: 1-26. (Pubitemid 26297205)
37. de Maagd RA, Bravo A, Crickmore N (2001) How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17: 193-9. (Pubitemid 32239538)
38. Petit L, Maier E, Gibert M, Popoff MR, Benz R (2001) Clostridium perfringens epsilon toxin induces a rapid change of cell membrane permeability to ions and forms channels in artificial lipid bilayers. J Biol Chem 276: 15736-15740.
39. Baida GE, Kuzmin NP (1995) Cloning and primary structure of a new hemolysin gene from Bacillus cereus. Biochim Biophys Acta 1264: 151-154.
40. Jarosz J, Glinski Z (1990) Selective inhibition of cecropin-like activity of insect immune blood by protease from American foulbrood scales. J Invertebr Pathol 56: 143-149. (Pubitemid 20291295)
41. Dancer BN, Chantawannakul P (1997) The proteases of American foulbrood scales. J Invertebr Pathol 70: 79-87. (Pubitemid 127439463)
42. Rawlings ND, Morton FR (2008) The MEROPS batch Blast: a tool to detect peptidases and their non-peptidase homologues in a genome. Biochimie 90: 243-259. (Pubitemid 351181248)
43. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, et al. (2002) The extracellular matrix of animals. Molecular Biology of the Cell. 4th edition. New York: Garland Science.
44. Jung C, Matsushita O, Katayama S, Minami J, Sakurai J, et al. (1999) Identification of metal ligands in the Clostridium histolyticum ColH collagenase. J Bacteriol 181, 2816-2822. (Pubitemid 29211098)
45. Keil B (1992) Vibrio alginolyticus ("Achromobacter") collagenase: biosynthesis, function, and application. Matrix Suppl 1: 127-133.
46. Matsushita O, Koide T, Kobayashi R, Nagata K, Okabe A (2001) Substrate recognition by the collagen-binding domain of Clostridium histolyticum class I collagenase. J Biol Chem 276: 8761-8770.
47. Féthière J, Eggimann B, Cygler M (1999) Crystal structure of chondroitin AC lyase, a representative of a family of glycosaminoglycan degrading enzymes. J Mol Biol 288: 635-647. (Pubitemid 29240522)
48. Stern R, Jedrzejas MJ (2006) Hyaluronidases: Their genomics, structures, and mechanisms of action. Chem Rev 106: 818-839.
49. Li SL, Kelly SJ, Lamani E, Ferraroni M, Jedrzejas MJ (2000) Structural basis of hyaluronan degradation by Streptococcus pneumonia hyaluronate lyase. EMBO J 19: 1228-1240. (Pubitemid 30151019)
50. Lindsay AM, Zhang M, Mitchell Z, Holden MT, Waller AS, et al. (2009) The Streptococcus equi prophage-encoded protein SEQ2045 is a hyaluronan-specific hyaluronate lyase that is produced during equine infection. Microbiology 155: 443-449.
51. Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54, 285-302.
52. Sebaihia M, Peck MW, Minton NP, Thomson NR, Holden MT, et al. (2007) Genome sequence of a proteolytic (Group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes. Genome Res 17: 1082-1092. (Pubitemid 47026355)
53. Yamamoto T, Tanada Y (1978) Phospholipid, an enhancing component in the synergistic factor of a granulosis virus of the armyworm, Pseudaletia unipuncta. J Invertebr Pathol 31: 48-56.
54. Zhu Y, Hukuhara T, Tamura K (1989) Location of a synergistic factor in the capsule of a granulosis virus of the armyworm, Pseudaletia unipuncta. J Invertebr Pathol 54: 49-56.
55. Chan QWT, Melathopoulos AP, Pernal SF, Foster LJ (2009) The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae. BMC Genomics 10: 387.
56. Hedstrom L (2002) Serine protease mechanism and specificity. Chem Rev 102: 4501-4524.
57. Barrett AJ (2004) Bioinformatics of proteases in the MEROPS database. Curr Opin Drug Discov Devel 7: 334-341.
58. Evans JD (2004) Transcriptional immune response by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae. J Invertebr Pathol 85: 105-111.
59. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, et al. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15: 645-656. (Pubitemid 44652092)
60. Lövgren A, Zhang M, Engström A, Dalhammar G, Landén R (1990) Molecular characterization of immune inhibitor A, a secreted virulence protease from Bacillus thuringiensis. Mol Microbiol 4: 2137-2146.
61. Khosla C, Gokhale RS, Jacobsen JR, Cane DE (1999) Tolerance and specificity of polyketide synthases. Annu Rev Biochem 68: 219-253. (Pubitemid 29449192)
62. Du L, Lou L (2010) PKS and NRPS release mechanisms. Nat Prod Rep 27: 255-278.
63. Thimon L, Peypoux F, Wallach J, Michel G (1995) Effect of the lipopeptide antibiotic, iturin A, on morphology and membrane ultrastructure of yeast cells. FEMS Microbiol Lett 128: 101-106.
64. Arrebola E, Jacobs R, Korsten L (2010) Iturin A is the principal inhibitor in the biocontrol activity of Bacillus amyloliquefaciens PPCB004 against postharvest fungal pathogens. J Appl Microbiol 108: 386-395.
65. Maget-Dana R, Peypoux F (1994) Iturins, a special-classclass of pore-forming lipopeptides - biological and physicochemical properties. Toxicology 87: 151-174.
66. Quentin MJ, Besson F, Peypoux F, Michel G (1982) Action of peptidolipidic antibiotics of the iturin group on erythrocytes - effect of some lipids on hemolysis. Biochim Biophys Acta 684: 207-211. (Pubitemid 12144153)
67. Duitman EH, Hamoen LW, Rembold M, Venema G, Seitz H, et al. (1999) The mycosubtilin synthetase of Bacillus subtilis ATCC 6633: A multifunctional hybrid between a peptide synthetase, an amino transferase, and a fatty acid synthase. Proc Natl Acad Sci U S A: 13294-13299.
68. Ansari MZ, Yadav G, Gokhale RS, Mohanty D (2004) NRPS-PKS: a knowledge-based resource for analysis of NRPS/PKS megasynthases. Nucleic Acids Res 32: W405-W413. (Pubitemid 39004076)
69. Gilliam M, Shimanuki H (1970) Total hemocyte counts of honey bee larvae (Apis mellifera L) from various elevations. Experientia 26: 1006-1007.
70. Tamaki M, Ishii R, Kikuchi S, Watanabe E (2005) A novel active analogue of gramicidin S with smaller ring size. J Antibiot (Tokyo) 58: 293-295. (Pubitemid 40740608)
71. Winkelmann G (2002) Microbial siderophore-mediated transport. Biochem Soc Trans 30: 691-696.
72. Raymond KN, Carrano CJ (1979) Coordination chemistry and microbial iron transport. Acc Chem Res 12: 183-190.
73. May JJ, Wendrich TM, Marahiel MA (2001) The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276: 7209-7217.
74. Wen Y, Wu X, Teng Y, Qian C, Zhan Z, et al. (2011) Identification and analysis of the gene cluster involved in biosynthesis of paenibactin, a catecholate siderophore produced by Paenibacillus elgii B69. Environ Microbiol 13: 2726-2737.
75. Willey JM, van der Donk WA (2007) Lantibiotics: peptides of diverse structure and function. Annu Rev Microbiol 61: 477-501. (Pubitemid 350058218)
76. Bhaya D, Davison M, Barrangou R (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 45: 273-97.
77. Haft DH, Selengut J, Mongodin EF, Nelson KE (2005) A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 1: e60.
78. Grissa I, Vergnaud G, Pourcel C (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35 (Web Server issue): W52-7.
79. Shah SA, Garrett RA (2011) CRISPR/Cas and Cmr modules, mobility and evolution of adaptive immune systems. Res Microbiol 162: 27-38.
80. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, et al. (2004) Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 22: 1554-1558. (Pubitemid 40039458)
81. Pourcel C, Salvignol G, Vergnaud G (2005) CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151: 653-663. (Pubitemid 40425001)
82. Julian GS, Bulla LAJ (1971) Physiology of sporeforming bacteria associated with insects. J Bacteriol 108: 828-834.
83. 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. J Bacteriol 40: 723-731.
84. Hrabak J, Martinek K (2007) Screening of secreted proteases of Paenibacillus larvae by using substrate-SDS-polyacrylamide gel electrophoresis. J Apic Res 46: 160-164. (Pubitemid 47606570)
85. Bailey L, Ball BV (1991) Honey bee pathology. London: Academic Press.
86. Staden R, Beal KF, Bonfield JK (2000) The Staden package, 1998. Methods Mol Biol 132: 115-130.
87. Markowitz VM, Mavromatis K, Ivanova NN, Chen IM, Chu K, et al. (2009) IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 25 :2271-2278.
88. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, et al. (2005) ACT: the Artemis Comparison tool. Bioinformatics 21: 3422-3423. (Pubitemid 41222448)