Kingella kingae Expresses Four Structurally Distinct Polysaccharide Capsules That Differ in Their Correlation with Invasive Disease
Abstract
Kingella kingae is an encapsulated gram-negative organism that is a common cause of osteoarticular infections in young children. In earlier work, we identified a glycosyltransferase gene called csaA that is necessary for synthesis of the [3)-β-GalpNAc-(1→5)-β-Kdop-(2→] polysaccharide capsule (type a) in K. kingae strain 269–492. In the current study, we analyzed a large collection of invasive and carrier isolates from Israel and found that csaA was present in only 47% of the isolates. Further examination of this collection using primers based on the sequence that flanks csaA revealed three additional gene clusters (designated the csb, csc, and csd loci), all encoding predicted glycosyltransferases. The csb locus contains the csbA, csbB, and csbC genes and is associated with a capsule that is a polymer of [6)-α-GlcpNAc-(1→5)-β-(8-OAc)Kdop-(2→] (type b). The csc locus contains the cscA, cscB, and cscC genes and is associated with a capsule that is a polymer of [3)-β-Ribf-(1→2)-β-Ribf-(1→2)-β-Ribf-(1→4)-β-Kdop-(2→] (type c). The csd locus contains the csdA, csdB, and csdC genes and is associated with a capsule that is a polymer of [P-(O→3)[β-Galp-(1→4)]-β-GlcpNAc-(1→3)-α-GlcpNAc-1-] (type d). Introduction of the csa, csb, csc, and csd loci into strain KK01Δcsa, a strain 269–492 derivative that lacks the native csaA gene, was sufficient tomore »
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1336892
- Alternate Identifier(s):
- OSTI ID: 1365836
- Grant/Contract Number:
- FG02-93ER20097
- Resource Type:
- Published Article
- Journal Name:
- PLoS Pathogens
- Additional Journal Information:
- Journal Name: PLoS Pathogens Journal Volume: 12 Journal Issue: 10; Journal ID: ISSN 1553-7374
- Publisher:
- Public Library of Science (PLoS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES
Citation Formats
Starr, Kimberly F., Porsch, Eric A., Seed, Patrick C., Heiss, Christian, Naran, Radnaa, Forsberg, L. Scott, Amit, Uri, Yagupsky, Pablo, Azadi, Parastoo, St. Geme, Joseph W., and Mitchell, ed., Timothy J. Kingella kingae Expresses Four Structurally Distinct Polysaccharide Capsules That Differ in Their Correlation with Invasive Disease. United States: N. p., 2016.
Web. doi:10.1371/journal.ppat.1005944.
Starr, Kimberly F., Porsch, Eric A., Seed, Patrick C., Heiss, Christian, Naran, Radnaa, Forsberg, L. Scott, Amit, Uri, Yagupsky, Pablo, Azadi, Parastoo, St. Geme, Joseph W., & Mitchell, ed., Timothy J. Kingella kingae Expresses Four Structurally Distinct Polysaccharide Capsules That Differ in Their Correlation with Invasive Disease. United States. https://doi.org/10.1371/journal.ppat.1005944
Starr, Kimberly F., Porsch, Eric A., Seed, Patrick C., Heiss, Christian, Naran, Radnaa, Forsberg, L. Scott, Amit, Uri, Yagupsky, Pablo, Azadi, Parastoo, St. Geme, Joseph W., and Mitchell, ed., Timothy J. Wed .
"Kingella kingae Expresses Four Structurally Distinct Polysaccharide Capsules That Differ in Their Correlation with Invasive Disease". United States. https://doi.org/10.1371/journal.ppat.1005944.
@article{osti_1336892,
title = {Kingella kingae Expresses Four Structurally Distinct Polysaccharide Capsules That Differ in Their Correlation with Invasive Disease},
author = {Starr, Kimberly F. and Porsch, Eric A. and Seed, Patrick C. and Heiss, Christian and Naran, Radnaa and Forsberg, L. Scott and Amit, Uri and Yagupsky, Pablo and Azadi, Parastoo and St. Geme, Joseph W. and Mitchell, ed., Timothy J.},
abstractNote = {Kingella kingae is an encapsulated gram-negative organism that is a common cause of osteoarticular infections in young children. In earlier work, we identified a glycosyltransferase gene called csaA that is necessary for synthesis of the [3)-β-GalpNAc-(1→5)-β-Kdop-(2→] polysaccharide capsule (type a) in K. kingae strain 269–492. In the current study, we analyzed a large collection of invasive and carrier isolates from Israel and found that csaA was present in only 47% of the isolates. Further examination of this collection using primers based on the sequence that flanks csaA revealed three additional gene clusters (designated the csb, csc, and csd loci), all encoding predicted glycosyltransferases. The csb locus contains the csbA, csbB, and csbC genes and is associated with a capsule that is a polymer of [6)-α-GlcpNAc-(1→5)-β-(8-OAc)Kdop-(2→] (type b). The csc locus contains the cscA, cscB, and cscC genes and is associated with a capsule that is a polymer of [3)-β-Ribf-(1→2)-β-Ribf-(1→2)-β-Ribf-(1→4)-β-Kdop-(2→] (type c). The csd locus contains the csdA, csdB, and csdC genes and is associated with a capsule that is a polymer of [P-(O→3)[β-Galp-(1→4)]-β-GlcpNAc-(1→3)-α-GlcpNAc-1-] (type d). Introduction of the csa, csb, csc, and csd loci into strain KK01Δcsa, a strain 269–492 derivative that lacks the native csaA gene, was sufficient to produce the type a capsule, type b capsule, type c capsule, and type d capsule, respectively, indicating that these loci are solely responsible for determining capsule type in K. kingae. Further analysis demonstrated that 96% of the invasive isolates express either the type a or type b capsule and that a disproportionate percentage of carrier isolates express the type c or type d capsule. Lastly, these results establish that there are at least four structurally distinct K. kingae capsule types and suggest that capsule type plays an important role in promoting K. kingae invasive disease},
doi = {10.1371/journal.ppat.1005944},
journal = {PLoS Pathogens},
number = 10,
volume = 12,
place = {United States},
year = {Wed Oct 19 00:00:00 EDT 2016},
month = {Wed Oct 19 00:00:00 EDT 2016}
}
https://doi.org/10.1371/journal.ppat.1005944
Web of Science
Works referenced in this record:
The structure of Cryptococcus neoformans galactoxylomannan contains β-d-glucuronic acid
journal, May 2009
- Heiss, Christian; Stacey Klutts, J.; Wang, Zhirui
- Carbohydrate Research, Vol. 344, Issue 7
Changing Characteristics of Invasive Pneumococcal Disease in Metropolitan Atlanta, Georgia, after Introduction of a 7-Valent Pneumococcal Conjugate Vaccine
journal, June 2007
- Albrich, W. C.; Baughman, W.; Schmotzer, B.
- Clinical Infectious Diseases, Vol. 44, Issue 12
Emerging invasive liver abscess caused by K1 serotype Klebsiella pneumoniae in Korea
journal, June 2007
- Chung, D. R.; Lee, S. S.; Lee, H. R.
- Journal of Infection, Vol. 54, Issue 6
Characterization of the Kingella kingae Polysaccharide Capsule and Exopolysaccharide
journal, September 2013
- Starr, Kimberly F.; Porsch, Eric A.; Heiss, Christian
- PLoS ONE, Vol. 8, Issue 9
Pneumococcal Capsular Polysaccharide Structure Predicts Serotype Prevalence
journal, June 2009
- Weinberger, Daniel M.; Trzciński, Krzysztof; Lu, Ying-Jie
- PLoS Pathogens, Vol. 5, Issue 6
Profiling bacterial community in upper respiratory tracts
journal, November 2014
- Yi, Hana; Yong, Dongeun; Lee, Kyungwon
- BMC Infectious Diseases, Vol. 14, Issue 1
Mechanisms and impact of genetic recombination in the evolution of Streptococcus pneumoniae
journal, January 2015
- Chaguza, Chrispin; Cornick, Jennifer E.; Everett, Dean B.
- Computational and Structural Biotechnology Journal, Vol. 13
Structural characteristics of the antigenic capsular polysaccharides and lipopolysaccharides involved in the serological classification of Actinobacillus (Haemophilus) pleuropneumoniae strains
journal, August 1990
- Perry, Malcolm B.; Altman, Eleonora; Brisson, Jean-Robert
- Serodiagnosis and Immunotherapy in Infectious Disease, Vol. 4, Issue 4
Genotyping of Invasive Kingella kingae Isolates Reveals Predominant Clones and Association With Specific Clinical Syndromes
journal, July 2012
- Amit, Uri; Porat, Nurith; Basmaci, Romain
- Clinical Infectious Diseases, Vol. 55, Issue 8
Invasive Haemophilus influenzae Disease Caused by Non–Type b Strains in Northwestern Ontario, Canada, 2002–2008
journal, October 2009
- Brown, Veronica M.; Madden, Sharen; Kelly, Len
- Clinical Infectious Diseases, Vol. 49, Issue 8
Pneumococcal Capsular Switching: A Historical Perspective
journal, November 2012
- Wyres, K. L.; Lambertsen, L. M.; Croucher, N. J.
- Journal of Infectious Diseases, Vol. 207, Issue 3
Recombinational exchanges at the capsular polysaccharide biosynthetic locus lead to frequent serotype changes among natural isolates of Streptococcus pneumoniae
journal, January 1998
- Coffey, Tracey J.; Enright, Mark C.; Daniels, Maggie
- Molecular Microbiology, Vol. 27, Issue 1
The Biochemistry and Genetics of Capsular Polysaccharide Production in Bacteria
journal, October 1996
- Roberts, Ian S.
- Annual Review of Microbiology, Vol. 50, Issue 1
Klebsiella capsular type versus site of isolation.
journal, May 1981
- Riser, E.; Noone, P.
- Journal of Clinical Pathology, Vol. 34, Issue 5
Major Intercontinentally Distributed Sequence Types of Kingella kingae and Development of a Rapid Molecular Typing Tool
journal, August 2014
- Basmaci, R.; Bidet, P.; Yagupsky, P.
- Journal of Clinical Microbiology, Vol. 52, Issue 11
Outbreaks of Kingella kingae Infections in Daycare Facilities
journal, May 2014
- Yagupsky, Pablo
- Emerging Infectious Diseases, Vol. 20, Issue 5
Respiratory carriage of Kingella kingae among healthy children
journal, January 1995
- Yagupsky, Pablo; Dagan, Ron; Prajgrod, Felisa
- The Pediatric Infectious Disease Journal, Vol. 14, Issue 8
Dissemination of Kingella kingae in the Community and Long-Term Persistence of Invasive Clones
journal, January 2009
- Yagupsky, Pablo; Weiss-Salz, Inbal; Fluss, Ronen
- The Pediatric Infectious Disease Journal, Vol. 28, Issue 8
Identification of the capsule type of Pasteurella multocida isolates from cases of fowl cholera by multiplex PCR and comparison with phenotypic methods
journal, June 2014
- Furian, Tq; Borges, Ka; Pilatti, Rm
- Revista Brasileira de Ciência Avícola, Vol. 16, Issue 2
Genetic Basis for Nongroupable Neisseria meningitidis
journal, May 2003
- Dolan‐Livengood, Jennifer M.; Miller, Yoon K.; Martin, Larry E.
- The Journal of Infectious Diseases, Vol. 187, Issue 10
Neisseria meningitidis: an overview of the carriage state
journal, September 2004
- Yazdankhah, S. P.
- Journal of Medical Microbiology, Vol. 53, Issue 9
Multilocus Sequence Typing and rtxA Toxin Gene Sequencing Analysis of Kingella kingae Isolates Demonstrates Genetic Diversity and International Clones
journal, May 2012
- Basmaci, Romain; Yagupsky, Pablo; Ilharreborde, Brice
- PLoS ONE, Vol. 7, Issue 5
Epidemiology of Invasive Kingella Kingae Infections in 2 Distinct Pediatric Populations Cohabiting in One Geographic Area
journal, January 2012
- Amit, Uri; Dagan, Ron; Porat, Nurith
- The Pediatric Infectious Disease Journal, Vol. 31, Issue 4
Pneumococcal infections
journal, January 1997
- Feldman, Charles; Klugman, Keith
- Current Opinion in Infectious Diseases, Vol. 10, Issue 2
Bacterial Meningitis in the United States in 1995
journal, October 1997
- Schuchat, Anne; Robinson, Katherine; Wenger, Jay D.
- New England Journal of Medicine, Vol. 337, Issue 14
Meningococcal Disease: Still with Us
journal, January 1983
- Peltola, H.
- Clinical Infectious Diseases, Vol. 5, Issue 1
Polymerase Chain Reaction Diagnosis of Kingella kingae Arthritis in a Young Child
journal, November 1998
- Stahelin, J.; Goldenberger, D.; Gnehm, H. E.
- Clinical Infectious Diseases, Vol. 27, Issue 5
Evidence for Capsule Switching between Carried and Disease-Causing Neisseria meningitidis Strains
journal, May 2009
- Beddek, A. J.; Li, M. -S.; Kroll, J. S.
- Infection and Immunity, Vol. 77, Issue 7
Global epidemiology of meningococcal disease
journal, June 2009
- Harrison, Lee H.; Trotter, Caroline L.; Ramsay, Mary E.
- Vaccine, Vol. 27
Structure of the capsular polysaccharide (K19 antigen) from uropathogenic Escherichia coli O25:K19:H12
journal, June 1988
- Jann, Barbara; Ahrens, Ralph; Dengler, Thomas
- Carbohydrate Research, Vol. 177