Honey bee larval peritrophic matrix degradation during infection with <i><scp>P</scp>aenibacillus larvae</i>, the aetiological agent of <scp>A</scp>merican foulbrood of honey bees, is a key step in pathogenesis

Garcia‐Gonzalez, Eva; Genersch, Elke

doi:10.1111/1462-2920.12167

Cited by 41 publications

(51 citation statements)

References 46 publications

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“…This phenomenon has been attributed to the growing PM already in the early days of AFB research [17], [18]. Recently, we demonstrated that the honey bee larval gut is lined by a chitin-containing PM which is degraded during P. larvae infection [19], confirming earlier results showing that the PM is the first barrier the bacteria have to overcome when trying to breach the epithelium and to enter the haemocoel [20]. Proteases and chitin-degrading proteins are most likely involved in this process.…”

Section: Introductionmentioning

confidence: 84%

“…Recently, the genomes of representatives of two P. larvae genotypes, ERIC I and ERIC II, were sequenced, annotated and used for comparative genome analysis [26]. Surprisingly, no complete, uninterrupted and, hence, putatively functional gene coding for a classical chitinase could be detected in any of the genomes [26] posing the intriguing question: how is the described chitin-degradation by P. larvae during infection [19] achieved? We are now answering this question by describing the identification and functional characterization of P. larvae Pl CBP49, a novel member of the AA10 (formerly CBM33) family of chitin-binding and –degrading LPMOs.…”

Section: Introductionmentioning

confidence: 99%

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Paenibacillus larvae Chitin-Degrading Protein PlCBP49 Is a Key Virulence Factor in American Foulbrood of Honey Bees

et al. 2014

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Paenibacillus larvae, the etiological agent of the globally occurring epizootic American Foulbrood (AFB) of honey bees, causes intestinal infections in honey bee larvae which develop into systemic infections inevitably leading to larval death. Massive brood mortality might eventually lead to collapse of the entire colony. Molecular mechanisms of host-microbe interactions in this system and of differences in virulence between P. larvae genotypes are poorly understood. Recently, it was demonstrated that the degradation of the peritrophic matrix lining the midgut epithelium is a key step in pathogenesis of P. larvae infections. Here, we present the isolation and identification of PlCBP49, a modular, chitin-degrading protein of P. larvae and demonstrate that this enzyme is crucial for the degradation of the larval peritrophic matrix during infection. PlCBP49 contains a module belonging to the auxiliary activity 10 (AA10, formerly CBM33) family of lytic polysaccharide monooxygenases (LPMOs) which are able to degrade recalcitrant polysaccharides. Using chitin-affinity purified PlCBP49, we provide evidence that PlCBP49 degrades chitin via a metal ion-dependent, oxidative mechanism, as already described for members of the AA10 family. Using P. larvae mutants lacking PlCBP49 expression, we analyzed in vivo biological functions of PlCBP49. In the absence of PlCBP49 expression, peritrophic matrix degradation was markedly reduced and P. larvae virulence was nearly abolished. This indicated that PlCBP49 is a key virulence factor for the species P. larvae. The identification of the functional role of PlCBP49 in AFB pathogenesis broadens our understanding of this important family of chitin-binding and -degrading proteins, especially in those bacteria that can also act as entomopathogens.

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Section: Introductionmentioning

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Paenibacillus larvae Chitin-Degrading Protein PlCBP49 Is a Key Virulence Factor in American Foulbrood of Honey Bees

et al. 2014

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Section: Identification and Role Of Secondary Metabolitesmentioning

confidence: 99%

“…The PM of honey bee larvae consists mainly of chitin and its functional integrity is essential for larval survival [37]. Degradation of the PM during P. larvae infection and the ability of P. larvae to metabolize colloidal chitin could both be demonstrated [37]. PlCBP49, a chitinbinding and -degrading enzyme expressed by both P. larvae genotypes, was shown to be crucial for PM degradation during larval infection and to mediate chitindegradation via a metal-ion dependent, oxidative mechanism [38 ].…”

Section: Identification and Role Of Secondary Metabolitesmentioning

confidence: 99%

Molecular pathogenesis of American Foulbrood: how Paenibacillus larvae kills honey bee larvae

Poppinga

Genersch

2015

Current Opinion in Insect Science

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“…The PM also protects the midgut epithelium from mechanical and biochemical damage by abrasive food particles, digestive enzymes and pathogens [7]. In the development of American foulbrood, degradation of the PM occurs in the gut of P. larvae -infected larvae, which enables P. larvae to access the underlying epithelial cells directly and attack them [5]. At the advanced stage of EFB, the PM also tended to have degenerated or be absent in some parts.…”

Section: Discussionmentioning

confidence: 99%

Infection of <i>Melissococcus plutonius</i> clonal complex 12 strain in European honeybee larvae is essentially confined to the digestive tract

Takamatsu

Sato

Yoshiyama

2016

The Journal of Veterinary Medical Science

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Melissococcus plutonius is an important pathogen that causes European foulbrood (EFB) in honeybee larvae. Recently, we discovered a group of M. plutonius strains that are phenotypically and genetically distinct from other strains. These strains belong to clonal complex (CC) 12, as determined by multilocus sequence typing analysis, and show atypical cultural and biochemical characteristics in vitro compared with strains of other CCs tested. Although EFB is considered to be a purely intestinal infection according to early studies, it is unknown whether the recently found CC12 strains cause EFB by the same pathomechanism. In this study, to obtain a better understanding of EFB, we infected European honeybee (Apis mellifera) larvae per os with a well-characterized CC12 strain, DAT561, and analyzed the larvae histopathologically. Ingested DAT561 was mainly localized in the midgut lumen surrounded by the peritrophic matrix (PM) in the larvae. In badly affected larvae, the PM and midgut epithelial cells degenerated, and some bacterial cells were detected outside of the midgut. However, they did not proliferate in the deep tissues actively. By immunohistochemical analysis, the PM was stained with anti-M. plutonius serum in most of the DAT561-infected larvae. In some larvae, luminal surfaces of the PM were more strongly stained than the inside. These results suggest that infection of CC12 strain in honeybee larvae is essentially confined to the intestine. Moreover, our results imply the presence of M. plutonius-derived substances diffusing into the larval tissues in the course of infection.

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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

Cited by 41 publications

References 46 publications

Paenibacillus larvae Chitin-Degrading Protein PlCBP49 Is a Key Virulence Factor in American Foulbrood of Honey Bees

Paenibacillus larvae Chitin-Degrading Protein PlCBP49 Is a Key Virulence Factor in American Foulbrood of Honey Bees

Molecular pathogenesis of American Foulbrood: how Paenibacillus larvae kills honey bee larvae

Infection of <i>Melissococcus plutonius</i> clonal complex 12 strain in European honeybee larvae is essentially confined to the digestive tract

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