A large genomic island allows Neisseria meningitidis to utilize propionic acid, with implications for colonisation of the human nasopharynx

TY - JOUR

T1 - A large genomic island allows Neisseria meningitidis to utilize propionic acid, with implications for colonisation of the human nasopharynx

AU - Catenazzi, Maria Chiara E.

AU - Jones, Helen

AU - Wallace, Iain

AU - Clifton, Jacqueline

AU - Chong, James P.J.

AU - Jackson, Matthew A.

AU - Macdonald, Sandy

AU - Edwards, James

AU - Moir, James W. B.

N1 - This article is protected by copyright. All rights reserved.

PY - 2014/7

Y1 - 2014/7

N2 - Neisseria meningitidis is an important human pathogen that is capable of killing within hours of infection. Its normal habitat is the nasopharynx of adult humans. Here we identify a genomic island (the prp gene cluster) in N. meningitidis that enables this species to utilize propionic acid as a supplementary carbon source during growth, particularly under nutrient poor growth conditions. The prp gene cluster encodes enzymes for a methylcitrate cycle. Novel aspects of the methylcitrate cycle in N. meningitidis include a propionate kinase which was purified and characterised, and a putative propionate transporter. This genomic island is absent from the close relative of N. meningitidis, the commensal N. lactamica, which chiefly colonises infants not adults. We reason that the possession of the prp genes provides a metabolic advantage to N. meningitidis in the adult oral cavity, which is rich in propionic acid-generating bacteria. Data from classical microbiological and sequence-based microbiome studies provide several lines of supporting evidence that Neisseria meningitidis colonisation is correlated with propionic acid generating bacteria, with a strong correlation between prp-containing Neisseria and propionic acid generating bacteria from the genus Porphyromonas, and that this may explain adolescent / adult colonisation by N. meningitidis.

AB - Neisseria meningitidis is an important human pathogen that is capable of killing within hours of infection. Its normal habitat is the nasopharynx of adult humans. Here we identify a genomic island (the prp gene cluster) in N. meningitidis that enables this species to utilize propionic acid as a supplementary carbon source during growth, particularly under nutrient poor growth conditions. The prp gene cluster encodes enzymes for a methylcitrate cycle. Novel aspects of the methylcitrate cycle in N. meningitidis include a propionate kinase which was purified and characterised, and a putative propionate transporter. This genomic island is absent from the close relative of N. meningitidis, the commensal N. lactamica, which chiefly colonises infants not adults. We reason that the possession of the prp genes provides a metabolic advantage to N. meningitidis in the adult oral cavity, which is rich in propionic acid-generating bacteria. Data from classical microbiological and sequence-based microbiome studies provide several lines of supporting evidence that Neisseria meningitidis colonisation is correlated with propionic acid generating bacteria, with a strong correlation between prp-containing Neisseria and propionic acid generating bacteria from the genus Porphyromonas, and that this may explain adolescent / adult colonisation by N. meningitidis.

U2 - 10.1111/mmi.12664

DO - 10.1111/mmi.12664

M3 - Article

C2 - 24910087

SN - 0950-382X

VL - 93

SP - 346

EP - 355

JO - Molecular Microbiology

JF - Molecular Microbiology

IS - 2

ER -