Acquisition of the capsule locus by horizontal gene transfer in Neisseria meningitidis is often accompanied by the loss of UDP-GalNAc synthesis

Stephanie N. Bartley, Shakeel Mowlaboccus, Christopher A. Mullally, Keith A. Stubbs, Alice Vrielink, Martin C J Maiden, Odile B. Harrison, Timothy T. Perkins, Charlene M. Kahler

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Abstract

Pathogenic meningococci have acquired a 24 kb capsule synthesis island (cps) by horizontal gene transfer which consists of a synthetic locus and associated capsule transport genes flanked by repetitive Regions D and D'. Regions D and D' contain an intact gene encoding a UDP-galactose epimerase (galE1) and a truncated remnant (galE2), respectively. In this study, GalE protein alleles were shown to be either mono-functional, synthesising UDP-galactose (UDP-Gal), or bi-functional, synthesising UDP-Gal and UDP-galactosamine (UDP-GalNAc). Meningococci possessing a capsule null locus (cnl) typically possessed a single bi-functional galE. Separation of functionality between galE1 and galE2 alleles in meningococcal isolates was retained for all serogroups except serogroup E which has a synthetic requirement for UDP-GalNAc. The truncated galE2 remnant in Region D' was also phylogenetically related to the bi-functional galE of the cnl locus suggesting common ancestry. A model is proposed in which the illegitimate recombination of the cps island into the galE allele of the cnl locus results in the formation of Region D' containing the truncated galE2 locus and the capture of the cps island en bloc. The retention of the duplicated Regions D and D' enables inversion of the synthetic locus within the cps island during bacterial growth.

LanguageEnglish
Article number44442
Number of pages14
JournalScientific Reports
Volume7
DOIs
StatePublished - 14 Mar 2017

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Horizontal Gene Transfer
Uridine Diphosphate
Neisseria meningitidis
Capsules
Islands
Alleles
UDPglucose 4-Epimerase
Uridine Diphosphate Galactose
Nucleic Acid Repetitive Sequences
Genetic Recombination
Genes
Growth

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Bartley, Stephanie N. ; Mowlaboccus, Shakeel ; Mullally, Christopher A. ; Stubbs, Keith A. ; Vrielink, Alice ; Maiden, Martin C J ; Harrison, Odile B. ; Perkins, Timothy T. ; Kahler, Charlene M./ Acquisition of the capsule locus by horizontal gene transfer in Neisseria meningitidis is often accompanied by the loss of UDP-GalNAc synthesis. In: Scientific Reports. 2017 ; Vol. 7.
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abstract = "Pathogenic meningococci have acquired a 24 kb capsule synthesis island (cps) by horizontal gene transfer which consists of a synthetic locus and associated capsule transport genes flanked by repetitive Regions D and D'. Regions D and D' contain an intact gene encoding a UDP-galactose epimerase (galE1) and a truncated remnant (galE2), respectively. In this study, GalE protein alleles were shown to be either mono-functional, synthesising UDP-galactose (UDP-Gal), or bi-functional, synthesising UDP-Gal and UDP-galactosamine (UDP-GalNAc). Meningococci possessing a capsule null locus (cnl) typically possessed a single bi-functional galE. Separation of functionality between galE1 and galE2 alleles in meningococcal isolates was retained for all serogroups except serogroup E which has a synthetic requirement for UDP-GalNAc. The truncated galE2 remnant in Region D' was also phylogenetically related to the bi-functional galE of the cnl locus suggesting common ancestry. A model is proposed in which the illegitimate recombination of the cps island into the galE allele of the cnl locus results in the formation of Region D' containing the truncated galE2 locus and the capture of the cps island en bloc. The retention of the duplicated Regions D and D' enables inversion of the synthetic locus within the cps island during bacterial growth.",
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Acquisition of the capsule locus by horizontal gene transfer in Neisseria meningitidis is often accompanied by the loss of UDP-GalNAc synthesis. / Bartley, Stephanie N.; Mowlaboccus, Shakeel; Mullally, Christopher A.; Stubbs, Keith A.; Vrielink, Alice; Maiden, Martin C J; Harrison, Odile B.; Perkins, Timothy T.; Kahler, Charlene M.

In: Scientific Reports, Vol. 7, 44442, 14.03.2017.

Research output: Contribution to journalArticle

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T1 - Acquisition of the capsule locus by horizontal gene transfer in Neisseria meningitidis is often accompanied by the loss of UDP-GalNAc synthesis

AU - Bartley,Stephanie N.

AU - Mowlaboccus,Shakeel

AU - Mullally,Christopher A.

AU - Stubbs,Keith A.

AU - Vrielink,Alice

AU - Maiden,Martin C J

AU - Harrison,Odile B.

AU - Perkins,Timothy T.

AU - Kahler,Charlene M.

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N2 - Pathogenic meningococci have acquired a 24 kb capsule synthesis island (cps) by horizontal gene transfer which consists of a synthetic locus and associated capsule transport genes flanked by repetitive Regions D and D'. Regions D and D' contain an intact gene encoding a UDP-galactose epimerase (galE1) and a truncated remnant (galE2), respectively. In this study, GalE protein alleles were shown to be either mono-functional, synthesising UDP-galactose (UDP-Gal), or bi-functional, synthesising UDP-Gal and UDP-galactosamine (UDP-GalNAc). Meningococci possessing a capsule null locus (cnl) typically possessed a single bi-functional galE. Separation of functionality between galE1 and galE2 alleles in meningococcal isolates was retained for all serogroups except serogroup E which has a synthetic requirement for UDP-GalNAc. The truncated galE2 remnant in Region D' was also phylogenetically related to the bi-functional galE of the cnl locus suggesting common ancestry. A model is proposed in which the illegitimate recombination of the cps island into the galE allele of the cnl locus results in the formation of Region D' containing the truncated galE2 locus and the capture of the cps island en bloc. The retention of the duplicated Regions D and D' enables inversion of the synthetic locus within the cps island during bacterial growth.

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