3D visualization of the initial Yersinia ruckeri infection route in rainbow trout (Oncorhynchus mykiss) by optical projection tomography

Maki Otani; Kasper Rømer Villumsen; Helene Kragelund Strøm; Martin Kristian Raida

doi:10.1371/journal.pone.0089672

3D visualization of the initial Yersinia ruckeri infection route in rainbow trout (Oncorhynchus mykiss) by optical projection tomography

Maki Otani, Kasper Rømer Villumsen, Helene Kragelund Strøm, Martin Kristian Raida

32 Citationer (Scopus)

Abstract

Despite the fact that enteric redmouth disease (ERM) in farmed rainbow trout is one of the most devastating disease problems, little is known about the initial route of infection and pathogenicity of the aetiological agent, Yersinia ruckeri. In order to determine the initially infected organs, optical projection tomography (OPT), a novel three-dimensional (3D) bio-imaging technique, was applied. OPT not only enables the visualization of Y. ruckeri on mucosal surfaces but also the 3D spatial distribution in whole organs, without sectioning. Rainbow trout were infected by bath challenge exposure to 1 × 10(8) CFU/ml of Y. ruckeri O1 for 1 hour. Three fish were sampled for OPT and immunohistochemistry (IHC) 1, 10 and 30 minutes, 1, 3, 6, 12 and 24 hours, as well as 2, 3, 7 and 21 days after the start of the infection period. Y. ruckeri was re-isolated from the blood of infected fish as early as 1 minute post infection. Both OPT and IHC analysis confirmed that the secondary gill lamellae were the only tissues infected at this early time point, indicating that Y. ruckeri initially infects gill epithelial cells. The experimentally induced infection caused septicemia, and Y. ruckeri was found in all examined organs 7 days post infection including the brain, which correlated with the peak in mortality. To the best of our knowledge this is the first description of Y. ruckeri infection in the brain, which is likely to cause encephalitis. This in part could explain the lethality of ERM in rainbow trout. Using OPT scanning it was possible to visualize the initial route of entry, as well as secondary infection routes along with the proliferation and spread of Y. ruckeri, ultimately causing significant mortality in the exposed rainbow trout. These results demonstrate that OPT is a state-of-the-art technique capable of visualizing pathogenesis at high resolution.

Originalsprog	Engelsk
Tidsskrift	PloS one
Vol/bind	9
Udgave nummer	2
Sider (fra-til)	e89672
Antal sider	10
ISSN	1932-6203
DOI	https://doi.org/10.1371/journal.pone.0089672
Status	Udgivet - 28 feb. 2014

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10.1371/journal.pone.0089672

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abstract = "Despite the fact that enteric redmouth disease (ERM) in farmed rainbow trout is one of the most devastating disease problems, little is known about the initial route of infection and pathogenicity of the aetiological agent, Yersinia ruckeri. In order to determine the initially infected organs, optical projection tomography (OPT), a novel three-dimensional (3D) bio-imaging technique, was applied. OPT not only enables the visualization of Y. ruckeri on mucosal surfaces but also the 3D spatial distribution in whole organs, without sectioning. Rainbow trout were infected by bath challenge exposure to 1 × 10(8) CFU/ml of Y. ruckeri O1 for 1 hour. Three fish were sampled for OPT and immunohistochemistry (IHC) 1, 10 and 30 minutes, 1, 3, 6, 12 and 24 hours, as well as 2, 3, 7 and 21 days after the start of the infection period. Y. ruckeri was re-isolated from the blood of infected fish as early as 1 minute post infection. Both OPT and IHC analysis confirmed that the secondary gill lamellae were the only tissues infected at this early time point, indicating that Y. ruckeri initially infects gill epithelial cells. The experimentally induced infection caused septicemia, and Y. ruckeri was found in all examined organs 7 days post infection including the brain, which correlated with the peak in mortality. To the best of our knowledge this is the first description of Y. ruckeri infection in the brain, which is likely to cause encephalitis. This in part could explain the lethality of ERM in rainbow trout. Using OPT scanning it was possible to visualize the initial route of entry, as well as secondary infection routes along with the proliferation and spread of Y. ruckeri, ultimately causing significant mortality in the exposed rainbow trout. These results demonstrate that OPT is a state-of-the-art technique capable of visualizing pathogenesis at high resolution.",

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AU - Otani, Maki

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AU - Raida, Martin Kristian

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N2 - Despite the fact that enteric redmouth disease (ERM) in farmed rainbow trout is one of the most devastating disease problems, little is known about the initial route of infection and pathogenicity of the aetiological agent, Yersinia ruckeri. In order to determine the initially infected organs, optical projection tomography (OPT), a novel three-dimensional (3D) bio-imaging technique, was applied. OPT not only enables the visualization of Y. ruckeri on mucosal surfaces but also the 3D spatial distribution in whole organs, without sectioning. Rainbow trout were infected by bath challenge exposure to 1 × 10(8) CFU/ml of Y. ruckeri O1 for 1 hour. Three fish were sampled for OPT and immunohistochemistry (IHC) 1, 10 and 30 minutes, 1, 3, 6, 12 and 24 hours, as well as 2, 3, 7 and 21 days after the start of the infection period. Y. ruckeri was re-isolated from the blood of infected fish as early as 1 minute post infection. Both OPT and IHC analysis confirmed that the secondary gill lamellae were the only tissues infected at this early time point, indicating that Y. ruckeri initially infects gill epithelial cells. The experimentally induced infection caused septicemia, and Y. ruckeri was found in all examined organs 7 days post infection including the brain, which correlated with the peak in mortality. To the best of our knowledge this is the first description of Y. ruckeri infection in the brain, which is likely to cause encephalitis. This in part could explain the lethality of ERM in rainbow trout. Using OPT scanning it was possible to visualize the initial route of entry, as well as secondary infection routes along with the proliferation and spread of Y. ruckeri, ultimately causing significant mortality in the exposed rainbow trout. These results demonstrate that OPT is a state-of-the-art technique capable of visualizing pathogenesis at high resolution.

AB - Despite the fact that enteric redmouth disease (ERM) in farmed rainbow trout is one of the most devastating disease problems, little is known about the initial route of infection and pathogenicity of the aetiological agent, Yersinia ruckeri. In order to determine the initially infected organs, optical projection tomography (OPT), a novel three-dimensional (3D) bio-imaging technique, was applied. OPT not only enables the visualization of Y. ruckeri on mucosal surfaces but also the 3D spatial distribution in whole organs, without sectioning. Rainbow trout were infected by bath challenge exposure to 1 × 10(8) CFU/ml of Y. ruckeri O1 for 1 hour. Three fish were sampled for OPT and immunohistochemistry (IHC) 1, 10 and 30 minutes, 1, 3, 6, 12 and 24 hours, as well as 2, 3, 7 and 21 days after the start of the infection period. Y. ruckeri was re-isolated from the blood of infected fish as early as 1 minute post infection. Both OPT and IHC analysis confirmed that the secondary gill lamellae were the only tissues infected at this early time point, indicating that Y. ruckeri initially infects gill epithelial cells. The experimentally induced infection caused septicemia, and Y. ruckeri was found in all examined organs 7 days post infection including the brain, which correlated with the peak in mortality. To the best of our knowledge this is the first description of Y. ruckeri infection in the brain, which is likely to cause encephalitis. This in part could explain the lethality of ERM in rainbow trout. Using OPT scanning it was possible to visualize the initial route of entry, as well as secondary infection routes along with the proliferation and spread of Y. ruckeri, ultimately causing significant mortality in the exposed rainbow trout. These results demonstrate that OPT is a state-of-the-art technique capable of visualizing pathogenesis at high resolution.

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SP - e89672

JO - PLoS Computational Biology

JF - PLoS Computational Biology

IS - 2

ER -

3D visualization of the initial Yersinia ruckeri infection route in rainbow trout (Oncorhynchus mykiss) by optical projection tomography

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