Aeromonas salmonicida Growth in Response to Atlantic Salmon Mucins Differs between Epithelial Sites, Is Governed by Sialylated and N -Acetylhexosamine-Containing O -Glycans, and Is Affected by Ca 2+

ABSTRACT Aeromonas salmonicida causes furunculosis in salmonids and is a threat to Atlantic salmon aquaculture. The epithelial surfaces that the pathogen colonizes are covered by a mucus layer predominantly comprised of secreted mucins. By using mass spectrometry to identify mucin glycan structures...

Full description

Bibliographic Details
Published in:Infection and Immunity
Main Authors: Padra, János Tamás, Sundh, Henrik, Sundell, Kristina, Venkatakrishnan, Vignesh, Jin, Chunsheng, Samuelsson, Tore, Karlsson, Niclas G., Lindén, Sara K.
Other Authors: McCormick, Beth, Swedish Research Council, Engkvists Foundation, Wilhelm and Martina Lundgrens Foundation, Norwegian Research Council, Knut and Alice Wallenberg Foundation
Format: Article in Journal/Newspaper
Language:English
Published: American Society for Microbiology 2017
Subjects:
Online Access:http://dx.doi.org/10.1128/iai.00189-17
https://journals.asm.org/doi/pdf/10.1128/IAI.00189-17
id crasmicro:10.1128/iai.00189-17
record_format openpolar
spelling crasmicro:10.1128/iai.00189-17 2024-10-13T14:06:02+00:00 Aeromonas salmonicida Growth in Response to Atlantic Salmon Mucins Differs between Epithelial Sites, Is Governed by Sialylated and N -Acetylhexosamine-Containing O -Glycans, and Is Affected by Ca 2+ Padra, János Tamás Sundh, Henrik Sundell, Kristina Venkatakrishnan, Vignesh Jin, Chunsheng Samuelsson, Tore Karlsson, Niclas G. Lindén, Sara K. McCormick, Beth Swedish Research Council Swedish Research Council Engkvists Foundation Wilhelm and Martina Lundgrens Foundation Norwegian Research Council Knut and Alice Wallenberg Foundation 2017 http://dx.doi.org/10.1128/iai.00189-17 https://journals.asm.org/doi/pdf/10.1128/IAI.00189-17 en eng American Society for Microbiology https://journals.asm.org/non-commercial-tdm-license Infection and Immunity volume 85, issue 8 ISSN 0019-9567 1098-5522 journal-article 2017 crasmicro https://doi.org/10.1128/iai.00189-17 2024-09-17T04:08:16Z ABSTRACT Aeromonas salmonicida causes furunculosis in salmonids and is a threat to Atlantic salmon aquaculture. The epithelial surfaces that the pathogen colonizes are covered by a mucus layer predominantly comprised of secreted mucins. By using mass spectrometry to identify mucin glycan structures with and without enzymatic removal of glycan residues, coupled to measurements of bacterial growth, we show here that the complex Atlantic salmon intestinal mucin glycans enhance A. salmonicida growth, whereas the more simple skin mucin glycans do not. Of the glycan residues present terminally on the salmon mucins, only N -acetylglucosamine (GlcNAc) enhances growth. Sialic acids, which have an abundance of 75% among terminal glycans from skin and of <50% among intestinal glycans, cannot be removed or used by A. salmonicida for growth-enhancing purposes, and they shield internal GlcNAc from utilization. A Ca 2+ concentration above 0.1 mM is needed for A. salmonicida to be able to utilize mucins for growth-promoting purposes, and 10 mM further enhances both A. salmonicida growth in response to mucins and binding of the bacterium to mucins. In conclusion, GlcNAc and sialic acids are important determinants of the A. salmonicida interaction with its host at the mucosal surface. Furthermore, since the mucin glycan repertoire affects pathogen growth, the glycan repertoire may be a factor to take into account during breeding and selection of strains for aquaculture. Article in Journal/Newspaper Atlantic salmon ASM Journals (American Society for Microbiology) Infection and Immunity 85 8
institution Open Polar
collection ASM Journals (American Society for Microbiology)
op_collection_id crasmicro
language English
description ABSTRACT Aeromonas salmonicida causes furunculosis in salmonids and is a threat to Atlantic salmon aquaculture. The epithelial surfaces that the pathogen colonizes are covered by a mucus layer predominantly comprised of secreted mucins. By using mass spectrometry to identify mucin glycan structures with and without enzymatic removal of glycan residues, coupled to measurements of bacterial growth, we show here that the complex Atlantic salmon intestinal mucin glycans enhance A. salmonicida growth, whereas the more simple skin mucin glycans do not. Of the glycan residues present terminally on the salmon mucins, only N -acetylglucosamine (GlcNAc) enhances growth. Sialic acids, which have an abundance of 75% among terminal glycans from skin and of <50% among intestinal glycans, cannot be removed or used by A. salmonicida for growth-enhancing purposes, and they shield internal GlcNAc from utilization. A Ca 2+ concentration above 0.1 mM is needed for A. salmonicida to be able to utilize mucins for growth-promoting purposes, and 10 mM further enhances both A. salmonicida growth in response to mucins and binding of the bacterium to mucins. In conclusion, GlcNAc and sialic acids are important determinants of the A. salmonicida interaction with its host at the mucosal surface. Furthermore, since the mucin glycan repertoire affects pathogen growth, the glycan repertoire may be a factor to take into account during breeding and selection of strains for aquaculture.
author2 McCormick, Beth
Swedish Research Council
Swedish Research Council
Engkvists Foundation
Wilhelm and Martina Lundgrens Foundation
Norwegian Research Council
Knut and Alice Wallenberg Foundation
format Article in Journal/Newspaper
author Padra, János Tamás
Sundh, Henrik
Sundell, Kristina
Venkatakrishnan, Vignesh
Jin, Chunsheng
Samuelsson, Tore
Karlsson, Niclas G.
Lindén, Sara K.
spellingShingle Padra, János Tamás
Sundh, Henrik
Sundell, Kristina
Venkatakrishnan, Vignesh
Jin, Chunsheng
Samuelsson, Tore
Karlsson, Niclas G.
Lindén, Sara K.
Aeromonas salmonicida Growth in Response to Atlantic Salmon Mucins Differs between Epithelial Sites, Is Governed by Sialylated and N -Acetylhexosamine-Containing O -Glycans, and Is Affected by Ca 2+
author_facet Padra, János Tamás
Sundh, Henrik
Sundell, Kristina
Venkatakrishnan, Vignesh
Jin, Chunsheng
Samuelsson, Tore
Karlsson, Niclas G.
Lindén, Sara K.
author_sort Padra, János Tamás
title Aeromonas salmonicida Growth in Response to Atlantic Salmon Mucins Differs between Epithelial Sites, Is Governed by Sialylated and N -Acetylhexosamine-Containing O -Glycans, and Is Affected by Ca 2+
title_short Aeromonas salmonicida Growth in Response to Atlantic Salmon Mucins Differs between Epithelial Sites, Is Governed by Sialylated and N -Acetylhexosamine-Containing O -Glycans, and Is Affected by Ca 2+
title_full Aeromonas salmonicida Growth in Response to Atlantic Salmon Mucins Differs between Epithelial Sites, Is Governed by Sialylated and N -Acetylhexosamine-Containing O -Glycans, and Is Affected by Ca 2+
title_fullStr Aeromonas salmonicida Growth in Response to Atlantic Salmon Mucins Differs between Epithelial Sites, Is Governed by Sialylated and N -Acetylhexosamine-Containing O -Glycans, and Is Affected by Ca 2+
title_full_unstemmed Aeromonas salmonicida Growth in Response to Atlantic Salmon Mucins Differs between Epithelial Sites, Is Governed by Sialylated and N -Acetylhexosamine-Containing O -Glycans, and Is Affected by Ca 2+
title_sort aeromonas salmonicida growth in response to atlantic salmon mucins differs between epithelial sites, is governed by sialylated and n -acetylhexosamine-containing o -glycans, and is affected by ca 2+
publisher American Society for Microbiology
publishDate 2017
url http://dx.doi.org/10.1128/iai.00189-17
https://journals.asm.org/doi/pdf/10.1128/IAI.00189-17
genre Atlantic salmon
genre_facet Atlantic salmon
op_source Infection and Immunity
volume 85, issue 8
ISSN 0019-9567 1098-5522
op_rights https://journals.asm.org/non-commercial-tdm-license
op_doi https://doi.org/10.1128/iai.00189-17
container_title Infection and Immunity
container_volume 85
container_issue 8
_version_ 1812812086084894720