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Title: Structure of the capsule and lipopolysaccharide O-antigen from the channel catfish pathogen, Aeromonas hydrophila

Abstract

A hypervirulent A. hydrophila (vAh) pathotype has been identified as the etiologic agent responsible for disease outbreaks in farmed carp species and channel catfish (Ictalurus punctatus) in China and the Southeastern United States, respectively. The possible route of infection has previously been unknown; however, virulence is believed to be multifactorial, involving the production/secretion of several virulence factors, including a high molecular weight group 4 capsular polysaccharide. Here we present chemical structural evidence of a novel capsule- and LPS-associated O-antigen found present in vAh isolated during these disease outbreaks. In this study, the chemical structure of the vAh O-antigen was determined by chemical analysis, Smith degradation, mass spectrometry, and 2D proton and carbon nuclear magnetic resonance (NMR) spectroscopy and found to be unique among described bacterial O-antigens. The O-antigen consists of hexasaccharide repeating units featuring a 4)-α-l-Fucp-(1–3)-β-d-GlcpNAc-(1–4)-α-l-Fucp-(1–4)-β-d-Glcp-(1- backbone, substituted with single residue side chains of α-d-Glcp and α-d-Quip3NAc linked to O-3 of the two fucose residues. The polysaccharide is partially O-acetylated on O-6 of the 4-substituted β-Glcp residue.

Authors:
 [1];  [1];  [2];  [2];  [2];  [2];  [3];  [1]
  1. Univ. of Georgia, Athens, GA (United States)
  2. Auburn Univ., AL (United States)
  3. Univ. of Michigan, Ann Arbor, MI (United States)
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States); Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1802744
Alternate Identifier(s):
OSTI ID: 1691833; OSTI ID: 1964088
Grant/Contract Number:  
SC0015662
Resource Type:
Accepted Manuscript
Journal Name:
Carbohydrate Research
Additional Journal Information:
Journal Volume: 486; Journal ID: ISSN 0008-6215
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Aeromonas hydrophila; fish pathogen; O-antigen capsule; lipopolysaccharide; NMR; polysaccharide structure; Aeromonas hydrophila, fish pathogen, O-antigen capsule, lipopolysaccharide, NMR, polysaccharide structure

Citation Formats

Heiss, Christian, Wang, Zhirui, Thurlow, Charles M., Hossain, Mohammad J., Sun, Dawei, Liles, Mark R., Saper, Mark A., and Azadi, Parastoo. Structure of the capsule and lipopolysaccharide O-antigen from the channel catfish pathogen, Aeromonas hydrophila. United States: N. p., 2019. Web. doi:10.1016/j.carres.2019.107858.
Heiss, Christian, Wang, Zhirui, Thurlow, Charles M., Hossain, Mohammad J., Sun, Dawei, Liles, Mark R., Saper, Mark A., & Azadi, Parastoo. Structure of the capsule and lipopolysaccharide O-antigen from the channel catfish pathogen, Aeromonas hydrophila. United States. https://doi.org/10.1016/j.carres.2019.107858
Heiss, Christian, Wang, Zhirui, Thurlow, Charles M., Hossain, Mohammad J., Sun, Dawei, Liles, Mark R., Saper, Mark A., and Azadi, Parastoo. Sat . "Structure of the capsule and lipopolysaccharide O-antigen from the channel catfish pathogen, Aeromonas hydrophila". United States. https://doi.org/10.1016/j.carres.2019.107858. https://www.osti.gov/servlets/purl/1802744.
@article{osti_1802744,
title = {Structure of the capsule and lipopolysaccharide O-antigen from the channel catfish pathogen, Aeromonas hydrophila},
author = {Heiss, Christian and Wang, Zhirui and Thurlow, Charles M. and Hossain, Mohammad J. and Sun, Dawei and Liles, Mark R. and Saper, Mark A. and Azadi, Parastoo},
abstractNote = {A hypervirulent A. hydrophila (vAh) pathotype has been identified as the etiologic agent responsible for disease outbreaks in farmed carp species and channel catfish (Ictalurus punctatus) in China and the Southeastern United States, respectively. The possible route of infection has previously been unknown; however, virulence is believed to be multifactorial, involving the production/secretion of several virulence factors, including a high molecular weight group 4 capsular polysaccharide. Here we present chemical structural evidence of a novel capsule- and LPS-associated O-antigen found present in vAh isolated during these disease outbreaks. In this study, the chemical structure of the vAh O-antigen was determined by chemical analysis, Smith degradation, mass spectrometry, and 2D proton and carbon nuclear magnetic resonance (NMR) spectroscopy and found to be unique among described bacterial O-antigens. The O-antigen consists of hexasaccharide repeating units featuring a 4)-α-l-Fucp-(1–3)-β-d-GlcpNAc-(1–4)-α-l-Fucp-(1–4)-β-d-Glcp-(1- backbone, substituted with single residue side chains of α-d-Glcp and α-d-Quip3NAc linked to O-3 of the two fucose residues. The polysaccharide is partially O-acetylated on O-6 of the 4-substituted β-Glcp residue.},
doi = {10.1016/j.carres.2019.107858},
journal = {Carbohydrate Research},
number = ,
volume = 486,
place = {United States},
year = {Sat Oct 26 00:00:00 EDT 2019},
month = {Sat Oct 26 00:00:00 EDT 2019}
}

Works referenced in this record:

Structural Studies of the Lipopolysaccharide from the Fish Pathogen Aeromonas veronii Strain Bs19, Serotype O16
journal, March 2014

  • Turska-Szewczuk, Anna; Duda, Katarzyna; Schwudke, Dominik
  • Marine Drugs, Vol. 12, Issue 3
  • DOI: 10.3390/md12031298

Detailed structural analysis of the O-polysaccharide expressed by Burkholderia thailandensis E264
journal, December 2012


Structure of the O-specific polysaccharide from the lipopolysaccharide of Aeromonas hydrophila strain K691 containing 4-acetamido-4,6-dideoxy- d -glucose
journal, February 2017


Structure of a capsular polysaccharide isolated from Salmonella enteritidis
journal, October 2006


Masquerading microbial pathogens: capsular polysaccharides mimic host-tissue molecules
journal, July 2014

  • Cress, Brady F.; Englaender, Jacob A.; He, Wenqin
  • FEMS Microbiology Reviews, Vol. 38, Issue 4
  • DOI: 10.1111/1574-6976.12056

Characterization of the antigenic O-polysaccharide produced by Escherichia coli serotype O:70
journal, March 2010


Salmonella Produces an O-Antigen Capsule Regulated by AgfD and Important for Environmental Persistence
journal, November 2006

  • Gibson, D. L.; White, A. P.; Snyder, S. D.
  • Journal of Bacteriology, Vol. 188, Issue 22
  • DOI: 10.1128/JB.00809-06

The O-Antigen Capsule of Salmonella enterica Serovar Typhimurium Facilitates Serum Resistance and Surface Expression of FliC
journal, October 2015

  • Marshall, Joanna M.; Gunn, John S.
  • Infection and Immunity, Vol. 83, Issue 10
  • DOI: 10.1128/IAI.00634-15

Glycomic and glycoproteomic analysis of glycoproteins—a tutorial
journal, June 2017

  • Shajahan, Asif; Heiss, Christian; Ishihara, Mayumi
  • Analytical and Bioanalytical Chemistry, Vol. 409, Issue 19
  • DOI: 10.1007/s00216-017-0406-7

High-molecular-weight components in lipopolysaccharides of Salmonella typhimurium, Salmonella minnesota, and Escherichia coli
journal, May 1985


Biosynthesis and Assembly of Capsular Polysaccharides in Escherichia coli
journal, June 2006


Determination of glucosamine and lactose in milk-based formulae by high-performance liquid chromatography
journal, May 2008

  • Xinmin, Wang; Ruili, Zhang; Zhihua, Lv
  • Journal of Food Composition and Analysis, Vol. 21, Issue 3
  • DOI: 10.1016/j.jfca.2007.10.006

Structural determination of the O-specific polysaccharide from Aeromonas hydrophila strain A19 (serogroup O:14) with S-layer
journal, November 2011


Structural studies of Escherichia coli O127 O-antigen polysaccharide
journal, September 1993


Structure of a new acidic O-antigen of Proteusvulgaris O22 containing O-acetylated 3-acetamido-3,6-dideoxy-d-glucose
journal, May 1999

  • Toukach, Filip V.; Bartodziejska, Beata; Senchenkova, Sof’ya N.
  • Carbohydrate Research, Vol. 318, Issue 1-4
  • DOI: 10.1016/S0008-6215(99)00088-9

Novel insights into the pathogenicity of epidemic Aeromonas hydrophila ST251 clones from comparative genomics
journal, May 2015

  • Pang, Maoda; Jiang, Jingwei; Xie, Xing
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep09833

Structural and serological characterization of the O-chain polysaccharide of Aeromonas salmonicida strains A449, 80204 and 80204-1
journal, March 2005


Identification of an Escherichia coli Operon Required for Formation of the O-Antigen Capsule
journal, August 2005


1H, 13C and 15N chemical shift referencing in biomolecular NMR
journal, September 1995

  • Wishart, David S.; Bigam, Colin G.; Yao, Jian
  • Journal of Biomolecular NMR, Vol. 6, Issue 2
  • DOI: 10.1007/BF00211777

Requirement for Capsule in Colonization by Streptococcus pneumoniae
journal, June 2001


Assignment of anomeric structure to carbohydrates through geminal13C-H coupling constants
journal, January 1973


High-molecular-mass lipopolysaccharides are involved in Actinobacillus pleuropneumoniae adherence to porcine respiratory tract cells
journal, August 1994


Implication of Lateral Genetic Transfer in the Emergence of Aeromonas hydrophila Isolates of Epidemic Outbreaks in Channel Catfish
journal, November 2013


Farm size, seining practices, and salt use: Risk factors for Aeromonas hydrophila outbreaks in farm-raised catfish, Alabama, USA
journal, January 2015


The role of the capsular polysaccharide of Aeromonas hydrophila serogroup O:34 in the adherence to and invasion of fish cell lines
journal, September 1997


NMR nomenclature. Nuclear spin properties and conventions for chemical shifts(IUPAC Recommendations 2001)
journal, January 2001

  • Harris, Robin K.; Becker, Edwin D.; Cabral de Menezes, Sonia M.
  • Pure and Applied Chemistry, Vol. 73, Issue 11
  • DOI: 10.1351/pac200173111795

An O Antigen Capsule Modulates Bacterial Pathogenesis in Shigella sonnei
journal, March 2015


Structure of the O-chain polysaccharide of the phenol-phase soluble lipopolysaccharide of Escherichia coli 0:157:H7
journal, January 1986

  • Perry, Malcolm B.; MacLean, Leann; Griffith, Douglas W.
  • Biochemistry and Cell Biology, Vol. 64, Issue 1
  • DOI: 10.1139/o86-004

Streptococcus iniae Capsule Impairs Phagocytic Clearance and Contributes to Virulence in Fish
journal, February 2007

  • Locke, Jeffrey B.; Colvin, Kelly M.; Datta, Anup K.
  • Journal of Bacteriology, Vol. 189, Issue 4
  • DOI: 10.1128/JB.01175-06

Evidence for a LOS and a capsular polysaccharide in Capnocytophaga canimorsus
journal, December 2016

  • Renzi, Francesco; Ittig, Simon J.; Sadovskaya, Irina
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep38914

Molecular and Chemical Analysis of the Lipopolysaccharide from Aeromonas hydrophila Strain AH-1 (Serotype O11)
journal, April 2015

  • Merino, Susana; Canals, Rocío; Knirel, Yuriy
  • Marine Drugs, Vol. 13, Issue 4
  • DOI: 10.3390/md13042233

O-antigen structure in a virulent strain of Aeromonas hydrophila
journal, October 1984


Structural and immunochemical homogeneity of Aeromonas salmonicida lipopolysaccharide
journal, April 1984


Prevalence and distribution of Aeromonas hydrophila in the United States
journal, November 1978


Stereochemical factors determining the effects of glycosylation on the13C chemical shifts in carbohydrates
journal, September 1988

  • Shashkov, Alexander S.; Lipkind, Grigory M.; Knirel, Yuriy A.
  • Magnetic Resonance in Chemistry, Vol. 26, Issue 9
  • DOI: 10.1002/mrc.1260260904

Structural studies on the R-type lipopolysaccharide of Aeromonas hydrophila
journal, March 2004


Structure of the lipopolysaccharide core isolated from a human strain of Aeromonas hydrophila
journal, November 1984


Isolation and characterization of plant cell walls and cell wall components
book, January 1986


Vibrio cholerae O1 secretes an extracellular matrix in response to antibody-mediated agglutination
journal, January 2018