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Applied Microbiology and Biotechnology

, Volume 100, Issue 17, pp 7387–7395 | Cite as

Biology of Paenibacillus larvae, a deadly pathogen of honey bee larvae

  • Julia Ebeling
  • Henriette Knispel
  • Gillian Hertlein
  • Anne Fünfhaus
  • Elke Genersch
Mini-Review

Abstract

The gram-positive bacterium Paenibacillus larvae is the etiological agent of American Foulbrood of honey bees, a notifiable disease in many countries. Hence, P. larvae can be considered as an entomopathogen of considerable relevance in veterinary medicine. P. larvae is a highly specialized pathogen with only one established host, the honey bee larva. No other natural environment supporting germination and proliferation of P. larvae is known. Over the last decade, tremendous progress in the understanding of P. larvae and its interactions with honey bee larvae at a molecular level has been made. In this review, we will present the recent highlights and developments in P. larvae research and discuss the impact of some of the findings in a broader context to demonstrate what we can learn from studying “exotic” pathogens.

Keywords

Paenibacillus larvae American foulbrood Pathobiology Bacterial pathogenesis Secondary metabolites Chitin-degrading enzymes Bacterial toxins S-layer proteins 

Notes

Compliance with ethical standards

Own work reported in this review was funded by the Ministries for Agriculture from Brandenburg and Sachsen-Anhalt, Germany, and by the German Research Foundation (Graduate School 1121 and grants GE1365/1–1, GE1365/1–2).

Conflict of interest

All five authors (J. Ebeling, H. Knispel, G. Hertlein, A. Fünfhaus, and E. Genersch) declare that they have no conflict of interest.

Human and animal studies

This article is a review article and does not contain in itself any studies with human participants or vertebrate animals performed by any of the authors.

References

  1. Aachmann FL, Sørlie M, Skjåk-Bræk G, Eijsink VGH, Vaaje-Kolstad G (2012) NMR structure of a lytic polysaccharide monooxygenase provides insight into copper binding, protein dynamics, and substrate interactions. Proc Natl Acad Sci U S A 109:18779–18784CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aktories K, Wilde C, Vogelsgesang M (2004) Rho-modifying C3-like ADP-ribosyltransferases. Rev Physiol Biochem Pharmacol 152:1–22PubMedGoogle Scholar
  3. Antúnez K, Piccini C, Castro-Sowinski S, Rosado AS, Seldin L, Zunino P (2007) Phenotypic and genotypic characterization of Paenibacillus larvae isolates. Vet Microbiol 124(1–2):178–183CrossRefPubMedGoogle Scholar
  4. Ashiralieva A, Genersch E (2006) Reclassification, genotypes, and virulence of Paenibacillus larvae, the etiological agent of American foulbrood in honeybees—a review. Apidologie 37:411–420CrossRefGoogle Scholar
  5. Bailey L, Ball BV (1991) Honey bee pathology. Academic Press, New YorkGoogle Scholar
  6. Benghezal M, Adam E, Lucas A, Burn C, Orchard MG, Deuschel C, Valentino E, Braillard S, Paccaud J-P, Cosson P (2007) Inhibitors of bacterial virulence identified in a surrogate host model. Cell Microbiol 9:1336–1342CrossRefPubMedGoogle Scholar
  7. Bode HB (2009a) Entomopathogenic bacteria as a source of secondary metabolites. Curr Opin Chem Biol 13:224–230CrossRefPubMedGoogle Scholar
  8. Bode HB (2009b) Insects: true pioneers in anti-infective therapy and what we can learn from them. Angew Chem Int Ed 48:6394–6396CrossRefGoogle Scholar
  9. Brodsgaard CJ, Hansen H, Ritter W (2000) Progress of Paenibacillus larvae infection in individually inoculated honey bee larvae reared singly in vitro, in micro colonies, or in full-size colonies. J Apic Res 39:19–27CrossRefGoogle Scholar
  10. Calabi E, Calabi F, Phillips AD, Fairweather NF (2002) Binding of Clostridium difficile surface layer proteins to gastrointestinal tissues. Infect Immun 10:5770–5778CrossRefGoogle Scholar
  11. Carpusca I, Jank T, Aktories K (2006) Bacillus sphaericus mosquitocidal toxin (MTX) and pierisin: the enigmatic offspring from the family of ADP-ribosyltransferases. Mol Microbiol 62:621–630CrossRefPubMedGoogle Scholar
  12. Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ (2008) The biology and future prospects of antivirulence therapies. Nat Rev Microbiol 6:17–27CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chan QWT, Cornman RS, Birol I, Liao NY, Chan SK, Docking TR, Jackman SD, Taylor GA, Jones SJM, de Graaf DC, Evans JD, Foster LJ (2011) Updated genome assembly and annotation of Paenibacillus larvae, the agent of American foulbrood disease of honey bees. BMC Genomics 12:450CrossRefPubMedPubMedCentralGoogle Scholar
  14. De Graaf DC, Alippi AM, Brown M, Evans JD, Feldlaufer M, Gregorc A, Hornitzky M, Pernal SF, Schuch DMT, Titera D, Tomkies V, Ritter W (2006a) Diagnosis of American foulbrood in honey bees: a synthesis and proposed analytical protocols. Lett Appl Microbiol 43:583–590CrossRefPubMedGoogle Scholar
  15. De Graaf DC, De Vos P, Heyndrickx M, Van Trappen S, Peiren N, Jacobs FJ (2006b) Identification of Paenibacillus larvae to the subspecies level: an obstacle for AFB diagnosis. J Invertebr Pathol 91:115–123CrossRefPubMedGoogle Scholar
  16. Dingman DW, Stahly DP (1983) Medium promoting sporulation of Bacillus larvae and metabolism of medium components. Appl Environ Microbiol 46(4):860–869PubMedPubMedCentralGoogle Scholar
  17. Djukic M, Brzuszkiewicz E, Fünfhaus A, Voss J, Gollnow K, Poppinga L, Liesegang H, Garcia-Gonzalez E, Genersch E, Daniel R (2014) How to kill the honey bee larva: genomic potential and virulence mechanisms of Paenibacillus larvae. PLoS One 9:e90914CrossRefPubMedPubMedCentralGoogle Scholar
  18. Duitman EH, Hamoen LW, Rembold M, Venema G, Seitz H, Saenger W, Bernhard F, Reinhardt R, Schmidt M, Ullrich C, Stein T, Leenders F, Vater J (1999) The mycosubtilin synthetase of Bacillus subtilis ATCC6633: a multifunctional hybrid between a peptide synthetase, an amino transferase, and a fatty acid synthase. Proc Natl Acad Sci U S A 96:13294–13299CrossRefPubMedPubMedCentralGoogle Scholar
  19. Eijsink VGH, Vaaje-Kolstad G, Varum KM, Horn SJ (2008) Towards new enzymes for biofuels: lessons from chitinase research. Trends Biotechnol 26:228–235CrossRefPubMedGoogle Scholar
  20. Ekblad T, Lindgren AEG, Andersson CD, Caraballo R, Thorsell A-G, Karlberg T, Spjut S, Linusson A, Schüler H, Elofsson M (2015) Towards small molecule inhibitors of mono-ADP-ribosyltransferases. Eur J Med Chem 95:546–551CrossRefPubMedGoogle Scholar
  21. Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci U S A 109:11002–11007CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fieldhouse RJ, Merrill AR (2008) Needle in the haystack: structure-based toxin discovery. Trends Biochem Sci 33:546–556CrossRefPubMedGoogle Scholar
  23. 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 1:240–250CrossRefPubMedGoogle Scholar
  24. Fünfhaus A, Genersch E (2012) Proteome analysis of Paenibacillus larvae reveals the existence of a putative S-layer protein. Environ Microbiol Rep 4:194–202CrossRefPubMedGoogle Scholar
  25. 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 15:2951–2965PubMedGoogle Scholar
  26. Garcia-Gonzalez E, Genersch E (2013) Honey bee larval peritrophic matrix degradation during infection with Paenibacillus larvae, the aetiological agent of American foulbrood of honey bees, is a key step in pathogenesis. Environ Microbiol 15:2894–2901PubMedGoogle Scholar
  27. Garcia-Gonzalez E, Müller S, Ensle P, Süssmuth RD, Genersch E (2014a) Elucidation of sevadicin, a novel nonribosomal peptide secondary metabolite produced by the honey bee pathogenic bacterium Paenibacillus larvae. Environ Microbiol 16:1297–1309CrossRefGoogle Scholar
  28. Garcia-Gonzalez E, Müller S, Hertlein G, Heid NC, Süssmuth RD, Genersch E (2014b) Biological effects of paenilamicin, a secondary metabolite antibiotic produced by the honey bee pathogenic bacterium Paenibacillus larvae. Microbiol Open 3:642–656CrossRefGoogle Scholar
  29. Garcia-Gonzalez E, Poppinga L, Fünfhaus A, Hertlein G, Hedtke K, Jakubowska A, Genersch E (2014c) Paenibacillus larvae chitin-degrading protein PlCBP49 is a key virulence factor in American foulbrood of honey bees. PLoS Path 10:e1004284CrossRefGoogle Scholar
  30. Genersch E (2007) Paenibacillus larvae and American foulbrood in honeybees. Berl Münch Tierärztl Wschr 120:26–33Google Scholar
  31. Genersch E (2008) Paenibacillus larvae and American foulbrood—long since known and still surprising. J Verbr Lebensm 3:429–434CrossRefGoogle Scholar
  32. Genersch E (2010) American foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invertebr Pathol 103:S10–S19CrossRefPubMedGoogle Scholar
  33. 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 71:7551–7555CrossRefPubMedPubMedCentralGoogle Scholar
  34. Genersch E, Forsgren E, Pentikäinen J, Ashiralieva A, Rauch S, Kilwinski J, Fries I (2006) Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int J Syst Evol Microbiol 56:501–511CrossRefPubMedGoogle Scholar
  35. Hamdi C, Balloi A, Essanaa J, Crotti E, Gonella E, Raddadi N, Ricci I, Boudabous A, Borin S, Manino A, Bandi C, Alma A, Daffonchio D, Cherif A (2011) Gut microbiome dysbiosis and honeybee health. J Appl Entomol 135:524–533CrossRefGoogle Scholar
  36. Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54:285–302CrossRefPubMedGoogle Scholar
  37. Hertlein G, Müller S, Garcia-Gonzalez E, Poppinga L, Süssmuth R, Genersch E (2014) Production of the catechol type siderophore bacillibactin by the honey bee pathogen Paenibacillus larvae. PLoS One 9:e108272CrossRefPubMedPubMedCentralGoogle Scholar
  38. Heyndrickx M, Vandemeulebroecke K, Hoste B, Janssen P, Kersters K, de Vos P, Logan NA, Ali N, Berkeley RCW (1996) Reclassification of Paenibacillus (formerly Bacillus) pulvifaciens (Nakamura 1984) ash et al. 1994, a later synonym of Paenibacillus (formerly Bacillus) larvae (white, 1906) ash et al. 1994, as a subspecies of P. larvae, with emended descriptions of P. larvae as P. larvae subsp. larvae and P. larvae subsp. pulvifaciens. Int J Syst Bacteriol 46(1):270–279CrossRefPubMedGoogle Scholar
  39. Himmel ME, Ding S-Y, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807CrossRefPubMedGoogle Scholar
  40. Hoage TR, Rothenbuhler WC (1966) Larval honey bee response to various doses of Bacillus larvae spores. J Econ Entomol 59:42–45CrossRefGoogle Scholar
  41. Holst EC (1945) An antibiotic from a bee pathogen. Science 102:593–594CrossRefGoogle Scholar
  42. Hornitzky M, Nicholls PJ (1993) J medium is superior to sheep blood agar and brain heart infusion agar for the isolation of Bacillus larvae from honey samples. J Apic Res 32:51–52CrossRefGoogle Scholar
  43. Hroncova Z, Havlik J, Killer J, Doskocil I, Tyl J, Kamler M, Titera D, Hakl J, Mrazek J, Bunesova V, Rada V (2015) Variation in honey bee gut microbial diversity affected by ontogenetic stage, age and geographic location. PLoS One 10:e0118707CrossRefPubMedPubMedCentralGoogle Scholar
  44. Krska D, Ravulapalli R, Fieldhouse RJ, Lugo MR, Merrill AR (2015) C3larvin toxin, an ADP-ribosyltransferase from Paenibacillus larvae. J Biol Chem 290:1639–1653CrossRefPubMedGoogle Scholar
  45. Langer RC, Vinetz JM (2001) Plasmodium ookinete-secreted chitinase and parasite penetration of the mosquito peritrophic matrix. Trends Parasitol 17:269–272CrossRefPubMedGoogle Scholar
  46. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol 20:619–628CrossRefPubMedGoogle Scholar
  47. Matsushima-Hibiya Y, Watanabe M, Kono T, Kanazawa T, Koyama K, Sugimura T, Wakabayashi K (2000) Purification and cloning of pierisin-2, an apoptosis-inducing protein from the cabbage butterfly, Pieris brassicae. Eur J Biochem 267:5742–5750CrossRefPubMedGoogle Scholar
  48. May JJ, Wendrich TM, Marahiel MA (2001) The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholicsiderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276:7209–7217CrossRefPubMedGoogle Scholar
  49. Meadows D, Meadows D, Randers J, Behrens WW III (1972) The limits to growth. Universe Books, New YorkGoogle Scholar
  50. Merino ST, Cherry J (2007) Progress and challenges in enzyme development for biomass utilization. Adv Biochem Eng Biotechnol 108:95–120PubMedGoogle Scholar
  51. Miethke M, Klotz O, Linne U, May JJ, Beckering CL, Marahiel MA (2006) Ferri-bacillibactin uptake and hydrolysis in Bacillus subtilis. Mol Microbiol 61:1413–1427CrossRefPubMedGoogle Scholar
  52. Moran NA, Hansen AK, Powell JE, Sabree ZL (2012) Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One 7:e36393CrossRefPubMedPubMedCentralGoogle Scholar
  53. Morrissey BJ, Helgason T, Poppinga L, Fünfhaus A, Genersch E, Budge GE (2015) Biogeography of Paenibacillus larvae, the causative agent of American foulbrood, using a new multilocus sequence typing scheme. Environ Microbiol 17:1414–1424CrossRefPubMedGoogle Scholar
  54. Müller S, Garcia-Gonzalez E, Genersch E, Süssmuth R (2015) Involvement of secondary metabolites in the pathogenesis of the American foulbrood of honey bees caused by Paenibacillus larvae. Nat Prod Rep 32:765–778CrossRefPubMedGoogle Scholar
  55. Müller S, Garcia-Gonzalez E, Mainz A, Hertlein G, Heid NC, Mösker E, van den Elst H, Overkleeft HS, Genersch E, Süssmuth RD (2014) Paenilamicin—structure and biosynthesis of a hybrid non-ribosomal peptide/polyketide antibiotic from the bee pathogen Paenibacillus larvae. Angew Chem Int Ed Eng 53:10547–10828CrossRefGoogle Scholar
  56. Murray KD, Aronstein KA (2008) Transformation of the gram-positive honey bee pathogen, Paenibacillus larvae, by electroporation. J Microbiol Methods 75:325–328CrossRefPubMedGoogle Scholar
  57. 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 150:2381–2390CrossRefPubMedGoogle Scholar
  58. Pelaseyed T, Bergström JH, Gustafsson JK, Ermund A, Birchenough GMH, Schütte A, van der Post S, Svensson F, Rodríguez-Pineiro AM, Nyström EEL, Wising C, Johansson MEV, Hansson GC (2014) The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol Rev 260:8–20CrossRefPubMedPubMedCentralGoogle Scholar
  59. Pentikäinen J, Kalliainen E, Pelkonen S (2009) Molecular epidemiology of Paenibacillus larvae infection in Finland. Apidologie 40:73–81CrossRefGoogle Scholar
  60. 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 Veterinary Med Ser B 53:100–104CrossRefGoogle Scholar
  61. Plagemann O (1985) Eine einfache Kulturmethode zur bakteriologischen Identifizierung von Bacillus larvae mit Columbia-Blut-Schrägagar. Berl Münch Tierärztl Wschr 98:61–62Google Scholar
  62. Poppinga L, Fünfhaus A, Aupperle H, Genersch E (2016) American foulbrood. In: Aupperle H, Genersch E (eds) Diagnostic colour atlas of bee pathology. Laboklin, Bad KissingenGoogle Scholar
  63. 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 112:430–435CrossRefPubMedGoogle Scholar
  64. Poppinga L, Janesch B, Fünfhaus A, Sekot G, Garcia-Gonzalez E, Hertlein G, Hedtke K, Schäffer C, Genersch E (2012) Identification and functional analysis of the S-layer protein SplA of Paenibacillus larvae, the causative agent of American foulbrood of honey bees. PLoS Path 8:e1002716CrossRefGoogle Scholar
  65. 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 15:715–718CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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 75:3344–3347CrossRefPubMedPubMedCentralGoogle Scholar
  67. Richards AG, Richards PA (1977) The peritrophic membranes of insects. Annu Rev Entomol 22:219–240CrossRefPubMedGoogle Scholar
  68. Schäfer MO, Genersch E, Fünfhaus A, Poppinga L, Formella N, Bettin B, Karger A (2014) Rapid identification of differentially virulent genotypes of Paenibacillus larvae, the causative organism of American foulbrood of honey bees, by whole cell MALDI-TOF mass spectrometry. Vet Microbiol 170:291–297CrossRefPubMedGoogle Scholar
  69. 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 277:11941–11948CrossRefPubMedGoogle Scholar
  70. Segond D, Abi Khalil E, Buisson C, Daou N, Kallassy M, Lereclus D, Arosio P, Bou-Abdallah F, Nielsen Le Roux C (2014) Iron acquisition in Bacillus cereus: the roles of IlsA and bacillibactin in exogenous ferritin iron mobilization. PLoS Path 10:e1003935CrossRefGoogle Scholar
  71. Shniffer A, Visschedyk DD, Ravulapalli R, Suarez G, Turgeon ZJ, Petrie AA, Chopra AK, Merrill AR (2012) Characterization of an actin-targeting ADP-ribosyltransferase from Aeromonas hydrophila. J Biol Chem 287:37030–37041CrossRefPubMedPubMedCentralGoogle Scholar
  72. Sleytr UB, Egelseer EM, Ilk N, Pum D, Schuster B (2007a) S-layers as a basic building block in a molecular construction kit. FEBS J 274:323–334CrossRefPubMedGoogle Scholar
  73. Sleytr UB, Huber C, Ilk N, Pum D, Schuster B, Egelseer EM (2007b) S-layers as a tool kit for nanobiotechnological applications. FEMS Microbiol Lett 267:131–144CrossRefPubMedGoogle Scholar
  74. Sleytr UB, Messner P, Pum D, Sara M (1993) Crystalline bacterial cell surface layers. Mol Microbiol 10:911–916CrossRefPubMedGoogle Scholar
  75. Sleytr UB, Sára M, Pum D, Schuster B, Messner P, Schäffer C (2002) Self-assembly protein systems: microbial S-layers. In: Steinbüchel A, Fahnestock SR (eds) Biopolymers, vol 7 polyamides and complex proteinaceousmatrices I. Wiley-VCH, Weinheim, pp. 285–338Google Scholar
  76. Sleytr UB, Schuster B, Egelseer E-M, Pum D (2014) S-layers: principles and applications. FEMS Microbiol Rev 38:823–864CrossRefPubMedPubMedCentralGoogle Scholar
  77. Sood S, Steinmetz H, Beims B, Mohr KI, Stadler M, Djukic M, von der Ohe W, Steinert M, Daniel R, Müller R (2014) Paenilarvins: iturin family lipopeptides from the honey bee pathogen Paenibacillus larvae. Chem BioChem 15:1947–1955Google Scholar
  78. Tarr HLA (1937) Studies on American foulbrood of bees. I. The relative pathogenicity of vegetative cells and endospores of Bacillus larvae for the brood of the bee. Ann Appl Biol 24:377–384CrossRefGoogle Scholar
  79. Tautzenberger A, Förtsch C, Zwerger C, Dmochewitz L, Kreja L, Ignatius A, Barth H (2013) C3 rho-inhibitor for targeted pharmacological manipulation of osteoclast-like cells. PLoS One 8:e85695CrossRefPubMedPubMedCentralGoogle Scholar
  80. Terra WR (2001) The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch Insect Biochem Physiol 47:47–61CrossRefPubMedGoogle Scholar
  81. Thompson SA (2002) Campylobacter surface-layers (S-layers) and immune evasion. Ann Periodontol 7:43–53CrossRefPubMedPubMedCentralGoogle Scholar
  82. Tsuge K, Akiyama T, Shoda M (2000) Cloning, sequencing, and characterization of the iturin a operon. J Bacteriol 183:6265–6273CrossRefGoogle Scholar
  83. Turgeon Z, Jørgensen R, Visschedyk D, Edwards PR, Legree S, McGregor C, Fieldhouse RJ, Mangroo D, Schapira M, Merrill AR (2011) Newly discovered and characterized antivirulence compounds inhibit bacterial mono-ADP-ribosyltransferase toxins. Antimicrob Agents Chemother 55:983–991CrossRefPubMedGoogle Scholar
  84. Vaaje-Kolstad G, Bøhle LA, Gåseidnes S, Dalhus B, Bjørås M, Mathiesen G, Eijsink VGH (2012) Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. J Mol Biol 416:239–254CrossRefPubMedGoogle Scholar
  85. Vaaje-Kolstad G, Horn SJ, Sørlie M, Eijsink VGH (2013) The chitinolytic machinery of Serratia marcescens – a model system for enzymatic degradation of recalcitrant polysaccharides. FEBS J 280:3028–3049CrossRefPubMedGoogle Scholar
  86. Vaaje-Kolstad G, Horn SJ, van Aalten DMF, Synstad B, Eijsink VGH (2005) The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J Biol Chem 280:28492–28497CrossRefPubMedGoogle Scholar
  87. Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sørlie M, Eijsink VGH (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219–222CrossRefPubMedGoogle Scholar
  88. Watanabe M, Enomoto S, Takamura-Enya T, Nakano T, Koyama K, Sugimura T, Wakabayashi K (2004) Enzymatic properties of pierisin-1 and its N-terminal domain, a guanine-specific ADP-ribosyltransferase from the cabbage butterfly. J Biochem 135:471–477CrossRefPubMedGoogle Scholar
  89. Watanabe M, Kono T, Matsushima-Hibiya Y, Kanazawa T, Nishisaka N, Kishimoto T, Koyama K, Sugimura T, Wakabayashi K (1999) Molecular cloning of an apoptosis-inducing protein, pierisin, from cabbage butterfly: possible involvement of ADP-ribosylation in its activity. Proc Natl Acad Sci U S A 96:10608–10613CrossRefPubMedPubMedCentralGoogle Scholar
  90. White GF (1906) The bacteria of the apiary with special reference to bee disease. USDA, Bureau of Entomology, Technical Series 14:1–50Google Scholar
  91. Wilde C, Aktories K (2001) The rho-ADP-ribosylating C3 exoenzyme from Clostridium botulinum and related C3-like transferases. Toxicon 39:1647–1660CrossRefPubMedGoogle Scholar
  92. Wilde C, Just I, Aktories K (2002) Structure-function analysis of the rho-ADP-ribosylating exoenzyme C3stau2 from Staphylococcus aureus. Biochemistry 41:1529–1544CrossRefGoogle Scholar
  93. Wilde C, Vogelsgesang M, Aktories K (2003) Rho-specific Bacillus cereus ADP-ribosyltransferase C3cer cloning and characterization. Biochemistry 42:9694–9702CrossRefPubMedGoogle Scholar
  94. Wyman CE (2007) What is (and is not) vital to advancing cellulosic ethanol. Trends Biotechnol 25:153–157CrossRefPubMedGoogle Scholar
  95. Yamamoto M, Nakano T, Matsushima-Hibiya Y, Totsuka Y, Takahashi-Nakaguchi A, Matsumoto Y, Sugimura T, Wakabayashi K (2009) Molecular cloning of apoptosis-inducing pierisin-like proteins, from two species of white butterfly, Pieris melete and Aporia crataegi. Comp Biochem Physiol P Biochem Mol Biol 154:326–333CrossRefGoogle Scholar
  96. 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 10:1612–1620CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Molecular Microbiology and Bee DiseasesInstitute for Bee ResearchHohen NeuendorfGermany
  2. 2.Institute of Microbiology and EpizooticsFreie Universität BerlinBerlinGermany

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