Biofilm formation by the human pathogen Neisseria meningitidis

Lappann, Martin; Vogel, Ulrich

doi:10.1007/s00430-010-0149-y

Cited by 25 publications

(36 citation statements)

References 126 publications

(170 reference statements)

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“…Since N. meningitidis exclusively colonizes humans, it needs efficient between-host transmission and host colonization strategies to avoid eradication from the human population. As with other human-specific bacteria, the biology of N. meningitidis and its interaction with the host are commonly investigated in vitro, e.g., in tissue culture infection models and biofilm assays (7)(8)(9). Traditionally, almost all aspects of the biology of N. meningitidis have been analyzed at 37°C on the basis of the assumption of thermal homogeneity throughout the body.…”

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confidence: 99%

Impact of Moderate Temperature Changes on Neisseria meningitidis Adhesion Phenotypes and Proteome

et al. 2016

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bNeisseria meningitidis, the meningococcus, bears the potential to cause life-threatening invasive diseases, but it usually colonizes the nasopharynx without causing any symptoms. Within the nasopharynx, Neisseria meningitidis must face temperature changes depending on the ambient air temperature. Indeed, the nasopharyngeal temperature can be substantially lower than 37°C, the temperature commonly used in experimental settings. Here, we compared the levels of meningococcal biofilm formation, autoaggregation, and cellular adherence at 32°C and 37°C and found a clear increase in all these phenotypes at 32°C suggestive of a stronger in vivo colonization capability at this temperature. A comparative proteome analysis approach revealed differential protein expression levels between 32°C and 37°C, predominantly affecting the bacterial envelope. A total of 375 proteins were detected. Use of database annotation or the PSORTb algorithm predicted 49 of those proteins to be localized in the outer membrane, 21 in either the inner or outer membrane, 35 in the periplasm, 56 in the inner membrane, and 208 in the cytosol; for 6 proteins, no annotation or prediction was available. Temperature-dependent regulation of protein expression was seen particularly in the periplasm as well as in the outer and inner membranes. Neisserial heparin binding antigen (NHBA), NMB1030, and adhesin complex protein (ACP) showed the strongest upregulation at 32°C and were partially responsible for the observed temperature-dependent phenotypes. Screening of different global regulators of Neisseria meningitidis suggested that the extracytoplasmic sigma factor E might be involved in temperature-dependent biofilm formation. In conclusion, subtle temperature changes trigger adaptation events promoting mucosal colonization by meningococci. Microorganisms constantly adapt to changing environmental conditions. These changes include oxygen and nutrient availability, osmotic conditions, and temperature. The physiology of bacterial adaptation, including the underlying regulatory mechanisms that operate in response to radical temperature changes such as classical heat shock or cold shock, has been studied intensely (1-3). The heat shock response occurs during a transient upshift of growth temperature from 37°C to approximately 50°C (4). The heat shock response is controlled by the alternative sigma factor 32 , which regulates the expression of heat shock proteins mainly involved in protein folding or processing (4). In Escherichia coli, the cold shock response is triggered by a transient downshift from 37°C to 10°C that leads to generally slower transcriptional and translational responses except for about 26 upregulated proteins (5). The functions of these so-called cold shock proteins are less well understood than those of heat shock proteins, but they are likely involved in securing proper transcription, translation, and protein folding (5). Surprisingly little is known about the influence on bacterial physiology of slight temperature differences within mamma...

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Impact of Moderate Temperature Changes on Neisseria meningitidis Adhesion Phenotypes and Proteome

et al. 2016

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“…Biofilms are defined as surface-attached microbial communities embedded in a self-produced matrix. The ability of the meningococcus to form biofilm has been demonstrated both in vivo and in vitro (9). Invasive strains of meningococcus are systematically encapsulated, which is necessary for their survival in the bloodstream (10).…”

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Identification of Genes Involved in Neisseria meningitidis Colonization

et al. 2013

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Neisseria meningitidis is a worldwide cause of meningitis and septicemia leading at least to 50,000 deaths every year. Nevertheless, N. meningitidis is also a commensal bacterium that asymptomatically colonizes the epithelial cells of the nasopharynx of 10 to 30% of healthy individuals. Occasionally, N. meningitidis crosses the nasopharyngeal barrier and enters the bloodstream. During bacteremia, N. meningitidis may adhere to endothelial cells of brain vessels and invade meninges. To identify the genes required for meningococcal host colonization, we screened a signature-tagged transposon mutagenesis library using an innovative in vitro colonization model in order to identify mutants displaying decreased capacity to colonize human epithelial cells. Approximately 1,600 defined insertion mutants of invasive serogroup C strain NEM8013 were screened. Candidate mutants were tested individually for quantification of bacterial biomass with confocal microscope and COMSTAT software. Five mutants were demonstrated to exhibit significantly decreased colonization ability. The identified genes, including narP and estD, appeared to be involved in adaptation to hypoxic conditions and stress resistance. Interestingly, the genes fadD1, nnrS, and NMV_2034 (encoding a putative thioredoxin), prior to this study, had not been shown to be involved in colonization. Therefore, we provide here insights into the meningococcal functions necessary for the bacterium to adapt to growth on host cells.

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“…Biofilms contain a high population of bacteria, and so a low concentration of available oxygen would be expected due to the aerobic respiratory activity of the bacterial cells, consistent with the expression of the denitrification reductases. N. meningitidis also can exist in biofilms [32,33], but it is notable that, for N. meningitidis, the capsulated form has a much lower propensity for biofilm formation than acapsulate N. meningitidis. Thus N. meningitidis (which alone among Neisseria species possesses a polysaccharide capsule) may often be found in a capsulated planktonic/low-population-density state under which conditions oxygen may be readily available and aniA and norB are unnecessary for survival.…”

Section: N Meningitidis Is Becoming An Aerobementioning

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A snapshot of a pathogenic bacterium mid-evolution: Neisseria meningitidis is becoming a nitric oxide-tolerant aerobe

Moir

2011

Biochemical Society Transactions

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Members of the Neisseria genus typically display the ability to carry out denitrification of nitrite to nitrous oxide as an alternative to oxygen respiration when oxygen is depleted. The key enzymes nitrite and nitric oxide reductase are found across the Neisseria genus. Within Neisseria meningitidis, however, a number of research groups have found that a significant proportion of strains lack a functional nitrite reductase. It appears that N. meningitidis is on an evolutionary trajectory towards loss of the capacity to reduce nitrite. In the present paper, I propose that N. meningitidis is evolving to become a nitric oxide-tolerant aerobe in order to occupy an oxygen-rich niche close to host tissue (and hence oxygen perfusion). Other features of the genomic and functional specialization of N. meningitidis, such as possession of a polysaccharide capsule and various acquired reactive oxygen species-resistance mechanisms, support this proposition. The importance of oxygen availability more generally is discussed with reference to recent findings with other mucosal pathogens.

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Biofilm formation by the human pathogen Neisseria meningitidis

Cited by 25 publications

References 126 publications

Impact of Moderate Temperature Changes on Neisseria meningitidis Adhesion Phenotypes and Proteome

Impact of Moderate Temperature Changes on Neisseria meningitidis Adhesion Phenotypes and Proteome

Identification of Genes Involved in Neisseria meningitidis Colonization

A snapshot of a pathogenic bacterium mid-evolution: Neisseria meningitidis is becoming a nitric oxide-tolerant aerobe

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