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Germ tube mediated invasion of Batrachochytrium dendrobatidis in amphibian skin is host dependent

Pascale Van Rooij UGent, An Martel UGent, Katharina D'Herde UGent, Melanie Brutyn UGent, Siska Croubels UGent, Richard Ducatelle UGent, Freddy Haesebrouck UGent and Frank Pasmans UGent (2012) PLOS ONE. 7(7).
abstract
Batrachochytrium dendrobatidis (Bd) is the causative agent of chytridiomycosis, a fungal skin disease in amphibians and driver of worldwide amphibian declines. We focussed on the early stages of infection by Bd in 3 amphibian species with a differential susceptibility to chytridiomycosis. Skin explants of Alytes muletensis, Litoria caerulea and Xenopus leavis were exposed to Bd in an Ussing chamber for 3 to 5 days. Early interactions of Bd with amphibian skin were observed using light microscopy and transmission electron microscopy. To validate the observations in vitro, comparison was made with skin from experimentally infected frogs. Additional in vitro experiments were performed to elucidate the process of intracellular colonization in L. caerulea. Early interactions of Bd with amphibian skin are: attachment of zoospores to host skin, zoospore germination, germ tube development, penetration into skin cells, invasive growth in the host skin, resulting in the loss of host cell cytoplasm. Inoculation of A. muletensis and L. caerulea skin was followed within 24 h by endobiotic development, with sporangia located intracellularly in the skin. Evidence is provided of how intracellular colonization is established and how colonization by Bd proceeds to deeper skin layers. Older thalli develop rhizoid-like structures that spread to deeper skin layers, form a swelling inside the host cell to finally give rise to a new thallus. In X. laevis, interaction of Bd with skin was limited to an epibiotic state, with sporangia developing upon the skin. Only the superficial epidermis was affected. Epidermal cells seemed to be used as a nutrient source without development of intracellular thalli. The in vitro data agreed with the results obtained after experimental infection of the studied frog species. These data suggest that the colonization strategy of B. dendrobatidis is host dependent, with the extent of colonization most likely determined by inherent characteristics of the host epidermis.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
SP-NOV, CHYTRIDIOMYCOSIS, POPULATIONS, PATHOGENESIS, DECLINES, PEPTIDE DEFENSES, XENOPUS-LAEVIS, CHYTRID FUNGUS, AFRICAN CLAWED FROG, FROGS LITORIA-CAERULEA
journal title
PLOS ONE
PLoS One
volume
7
issue
7
article_number
e41481
pages
8 pages
Web of Science type
Article
Web of Science id
000306644600080
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
3.73 (2012)
JCR rank
7/56 (2012)
JCR quartile
1 (2012)
ISSN
1932-6203
DOI
10.1371/journal.pone.0041481
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
3005774
handle
http://hdl.handle.net/1854/LU-3005774
date created
2012-10-03 17:19:53
date last changed
2012-10-09 09:44:11
@article{3005774,
  abstract     = {Batrachochytrium dendrobatidis (Bd) is the causative agent of chytridiomycosis, a fungal skin disease in amphibians and driver of worldwide amphibian declines. We focussed on the early stages of infection by Bd in 3 amphibian species with a differential susceptibility to chytridiomycosis. Skin explants of Alytes muletensis, Litoria caerulea and Xenopus leavis were exposed to Bd in an Ussing chamber for 3 to 5 days. Early interactions of Bd with amphibian skin were observed using light microscopy and transmission electron microscopy. To validate the observations in vitro, comparison was made with skin from experimentally infected frogs. Additional in vitro experiments were performed to elucidate the process of intracellular colonization in L. caerulea. Early interactions of Bd with amphibian skin are: attachment of zoospores to host skin, zoospore germination, germ tube development, penetration into skin cells, invasive growth in the host skin, resulting in the loss of host cell cytoplasm. Inoculation of A. muletensis and L. caerulea skin was followed within 24 h by endobiotic development, with sporangia located intracellularly in the skin. Evidence is provided of how intracellular colonization is established and how colonization by Bd proceeds to deeper skin layers. Older thalli develop rhizoid-like structures that spread to deeper skin layers, form a swelling inside the host cell to finally give rise to a new thallus. In X. laevis, interaction of Bd with skin was limited to an epibiotic state, with sporangia developing upon the skin. Only the superficial epidermis was affected. Epidermal cells seemed to be used as a nutrient source without development of intracellular thalli. The in vitro data agreed with the results obtained after experimental infection of the studied frog species. These data suggest that the colonization strategy of B. dendrobatidis is host dependent, with the extent of colonization most likely determined by inherent characteristics of the host epidermis.},
  articleno    = {e41481},
  author       = {Van Rooij, Pascale and Martel, An and D'Herde, Katharina and Brutyn, Melanie and Croubels, Siska and Ducatelle, Richard and Haesebrouck, Freddy and Pasmans, Frank},
  issn         = {1932-6203},
  journal      = {PLOS ONE},
  keyword      = {SP-NOV,CHYTRIDIOMYCOSIS,POPULATIONS,PATHOGENESIS,DECLINES,PEPTIDE DEFENSES,XENOPUS-LAEVIS,CHYTRID FUNGUS,AFRICAN CLAWED FROG,FROGS LITORIA-CAERULEA},
  language     = {eng},
  number       = {7},
  pages        = {8},
  title        = {Germ tube mediated invasion of Batrachochytrium dendrobatidis in amphibian skin is host dependent},
  url          = {http://dx.doi.org/10.1371/journal.pone.0041481},
  volume       = {7},
  year         = {2012},
}

Chicago
Van Rooij, Pascale, An Martel, Katharina D’Herde, Melanie Brutyn, Siska Croubels, Richard Ducatelle, Freddy Haesebrouck, and Frank Pasmans. 2012. “Germ Tube Mediated Invasion of Batrachochytrium Dendrobatidis in Amphibian Skin Is Host Dependent.” Plos One 7 (7).
APA
Van Rooij, P., Martel, A., D’Herde, K., Brutyn, M., Croubels, S., Ducatelle, R., Haesebrouck, F., et al. (2012). Germ tube mediated invasion of Batrachochytrium dendrobatidis in amphibian skin is host dependent. PLOS ONE, 7(7).
Vancouver
1.
Van Rooij P, Martel A, D’Herde K, Brutyn M, Croubels S, Ducatelle R, et al. Germ tube mediated invasion of Batrachochytrium dendrobatidis in amphibian skin is host dependent. PLOS ONE. 2012;7(7).
MLA
Van Rooij, Pascale, An Martel, Katharina D’Herde, et al. “Germ Tube Mediated Invasion of Batrachochytrium Dendrobatidis in Amphibian Skin Is Host Dependent.” PLOS ONE 7.7 (2012): n. pag. Print.