Chitinolytic enzymes contribute to the pathogenicity of Aliivibrio salmonicida LFI1238 in the invasive phase of cold-water vibriosis

Abstract Background Aliivibrio salmonicida is the causative agent of cold-water vibriosis in salmonids (Oncorhynchus mykiss and Salmo salar L.) and gadidae (Gadus morhua L.). Virulence-associated factors that are essential for the full spectrum of A. salmonicida pathogenicity are largely unknown. Ch...

Full description

Bibliographic Details
Published in:BMC Microbiology
Main Authors: Anna Skåne, Per Kristian Edvardsen, Gabriele Cordara, Jennifer Sarah Maria Loose, Kira Daryl Leitl, Ute Krengel, Henning Sørum, Fatemeh Askarian, Gustav Vaaje-Kolstad
Format: Article in Journal/Newspaper
Language:English
Published: BMC 2022
Subjects:
Online Access:https://doi.org/10.1186/s12866-022-02590-2
https://doaj.org/article/edc6e20bb8f54066ad708dbb7c51df96
id ftdoajarticles:oai:doaj.org/article:edc6e20bb8f54066ad708dbb7c51df96
record_format openpolar
spelling ftdoajarticles:oai:doaj.org/article:edc6e20bb8f54066ad708dbb7c51df96 2023-05-15T15:31:40+02:00 Chitinolytic enzymes contribute to the pathogenicity of Aliivibrio salmonicida LFI1238 in the invasive phase of cold-water vibriosis Anna Skåne Per Kristian Edvardsen Gabriele Cordara Jennifer Sarah Maria Loose Kira Daryl Leitl Ute Krengel Henning Sørum Fatemeh Askarian Gustav Vaaje-Kolstad 2022-08-01T00:00:00Z https://doi.org/10.1186/s12866-022-02590-2 https://doaj.org/article/edc6e20bb8f54066ad708dbb7c51df96 EN eng BMC https://doi.org/10.1186/s12866-022-02590-2 https://doaj.org/toc/1471-2180 doi:10.1186/s12866-022-02590-2 1471-2180 https://doaj.org/article/edc6e20bb8f54066ad708dbb7c51df96 BMC Microbiology, Vol 22, Iss 1, Pp 1-16 (2022) lytic polysaccharide monooxygenase LPMO virulence aliivibrio salmonicida chitin cold water vibriosis Microbiology QR1-502 article 2022 ftdoajarticles https://doi.org/10.1186/s12866-022-02590-2 2022-12-30T21:12:55Z Abstract Background Aliivibrio salmonicida is the causative agent of cold-water vibriosis in salmonids (Oncorhynchus mykiss and Salmo salar L.) and gadidae (Gadus morhua L.). Virulence-associated factors that are essential for the full spectrum of A. salmonicida pathogenicity are largely unknown. Chitin-active lytic polysaccharide monooxygenases (LPMOs) have been indicated to play roles in both chitin degradation and virulence in a variety of pathogenic bacteria but are largely unexplored in this context. Results In the present study we investigated the role of LPMOs in the pathogenicity of A. salmonicida LFI238 in Atlantic salmon (Salmo salar L.). In vivo challenge experiments using isogenic deletion mutants of the two LPMOs encoding genes AsLPMO10A and AsLPMO10B, showed that both LPMOs, and in particular AsLPMO10B, were important in the invasive phase of cold-water vibriosis. Crystallographic analysis of the AsLPMO10B AA10 LPMO domain (to 1.4 Å resolution) revealed high structural similarity to viral fusolin, an LPMO known to enhance the virulence of insecticidal agents. Finally, exposure to Atlantic salmon serum resulted in substantial proteome re-organization of the A. salmonicida LPMO deletion variants compared to the wild type strain, indicating the struggle of the bacterium to adapt to the host immune components in the absence of the LPMOs. Conclusion The present study consolidates the role of LPMOs in virulence and demonstrates that such enzymes may have more than one function. Article in Journal/Newspaper Atlantic salmon Gadus morhua Salmo salar Directory of Open Access Journals: DOAJ Articles BMC Microbiology 22 1
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic lytic polysaccharide monooxygenase
LPMO
virulence
aliivibrio salmonicida
chitin
cold water vibriosis
Microbiology
QR1-502
spellingShingle lytic polysaccharide monooxygenase
LPMO
virulence
aliivibrio salmonicida
chitin
cold water vibriosis
Microbiology
QR1-502
Anna Skåne
Per Kristian Edvardsen
Gabriele Cordara
Jennifer Sarah Maria Loose
Kira Daryl Leitl
Ute Krengel
Henning Sørum
Fatemeh Askarian
Gustav Vaaje-Kolstad
Chitinolytic enzymes contribute to the pathogenicity of Aliivibrio salmonicida LFI1238 in the invasive phase of cold-water vibriosis
topic_facet lytic polysaccharide monooxygenase
LPMO
virulence
aliivibrio salmonicida
chitin
cold water vibriosis
Microbiology
QR1-502
description Abstract Background Aliivibrio salmonicida is the causative agent of cold-water vibriosis in salmonids (Oncorhynchus mykiss and Salmo salar L.) and gadidae (Gadus morhua L.). Virulence-associated factors that are essential for the full spectrum of A. salmonicida pathogenicity are largely unknown. Chitin-active lytic polysaccharide monooxygenases (LPMOs) have been indicated to play roles in both chitin degradation and virulence in a variety of pathogenic bacteria but are largely unexplored in this context. Results In the present study we investigated the role of LPMOs in the pathogenicity of A. salmonicida LFI238 in Atlantic salmon (Salmo salar L.). In vivo challenge experiments using isogenic deletion mutants of the two LPMOs encoding genes AsLPMO10A and AsLPMO10B, showed that both LPMOs, and in particular AsLPMO10B, were important in the invasive phase of cold-water vibriosis. Crystallographic analysis of the AsLPMO10B AA10 LPMO domain (to 1.4 Å resolution) revealed high structural similarity to viral fusolin, an LPMO known to enhance the virulence of insecticidal agents. Finally, exposure to Atlantic salmon serum resulted in substantial proteome re-organization of the A. salmonicida LPMO deletion variants compared to the wild type strain, indicating the struggle of the bacterium to adapt to the host immune components in the absence of the LPMOs. Conclusion The present study consolidates the role of LPMOs in virulence and demonstrates that such enzymes may have more than one function.
format Article in Journal/Newspaper
author Anna Skåne
Per Kristian Edvardsen
Gabriele Cordara
Jennifer Sarah Maria Loose
Kira Daryl Leitl
Ute Krengel
Henning Sørum
Fatemeh Askarian
Gustav Vaaje-Kolstad
author_facet Anna Skåne
Per Kristian Edvardsen
Gabriele Cordara
Jennifer Sarah Maria Loose
Kira Daryl Leitl
Ute Krengel
Henning Sørum
Fatemeh Askarian
Gustav Vaaje-Kolstad
author_sort Anna Skåne
title Chitinolytic enzymes contribute to the pathogenicity of Aliivibrio salmonicida LFI1238 in the invasive phase of cold-water vibriosis
title_short Chitinolytic enzymes contribute to the pathogenicity of Aliivibrio salmonicida LFI1238 in the invasive phase of cold-water vibriosis
title_full Chitinolytic enzymes contribute to the pathogenicity of Aliivibrio salmonicida LFI1238 in the invasive phase of cold-water vibriosis
title_fullStr Chitinolytic enzymes contribute to the pathogenicity of Aliivibrio salmonicida LFI1238 in the invasive phase of cold-water vibriosis
title_full_unstemmed Chitinolytic enzymes contribute to the pathogenicity of Aliivibrio salmonicida LFI1238 in the invasive phase of cold-water vibriosis
title_sort chitinolytic enzymes contribute to the pathogenicity of aliivibrio salmonicida lfi1238 in the invasive phase of cold-water vibriosis
publisher BMC
publishDate 2022
url https://doi.org/10.1186/s12866-022-02590-2
https://doaj.org/article/edc6e20bb8f54066ad708dbb7c51df96
genre Atlantic salmon
Gadus morhua
Salmo salar
genre_facet Atlantic salmon
Gadus morhua
Salmo salar
op_source BMC Microbiology, Vol 22, Iss 1, Pp 1-16 (2022)
op_relation https://doi.org/10.1186/s12866-022-02590-2
https://doaj.org/toc/1471-2180
doi:10.1186/s12866-022-02590-2
1471-2180
https://doaj.org/article/edc6e20bb8f54066ad708dbb7c51df96
op_doi https://doi.org/10.1186/s12866-022-02590-2
container_title BMC Microbiology
container_volume 22
container_issue 1
_version_ 1766362191204712448