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Infection and Immunity, March 2006, p. 1725-1740, Vol. 74, No. 3
0019-9567/06/$08.00+0     doi:10.1128/IAI.74.3.1725-1740.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Identification of a Meningococcal L-Glutamate ABC Transporter Operon Essential for Growth in Low-Sodium Environments

Caterina Monaco,1 Adelfia Talà,1 Maria Rita Spinosa,1 Cinzia Progida,1 Eleanna De Nitto,1 Antonio Gaballo,3 Carmelo B. Bruni,2* Cecilia Bucci,1 and Pietro Alifano1*

Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università di Lecce, Via Monteroni, 73100 Lecce,1 Dipartimento di Biologia e Patologia Cellulare e Molecolare "L. Califano," Università di Napoli "Federico II," and Istituto di Endocrinologia ed Oncologia Sperimentale "G. Salvatore" of the C.N.R., Via S. Pansini 5, 80131 Napoli,2 Institute of Biomembranes and Bioenergetics of the C.N.R., Piazza G. Cesare—Policlinico, 70124 Bari, Italy3

Received 7 September 2005/ Returned for modification 14 October 2005/ Accepted 16 December 2005

GdhR is a meningococcal transcriptional regulator that was previously shown to positively control the expression of gdhA, encoding the NADP-specific L-glutamate dehydrogenase (NADP-GDH), in response to the growth phase and/or to the carbon source. In this study we used reverse transcriptase-PCR-differential display (to identify additional GdhR-regulated genes. The results indicated that GdhR, in addition to NADP-GDH, controls the expression of a number of genes involved in glucose catabolism by the Entner-Doudoroff pathway and in L-glutamate import by an unknown ABC transport system. The genes encoding the putative periplasmic substrate-binding protein (NMB1963) and the permease (NMB1965) of the ABC transporter were genetically inactivated. Uptake experiments demonstrated an impairment of L-glutamate import in the NMB1965-defective mutant in the absence or in the presence of a low sodium ion concentration. In contrast, at a sodium ion concentration above 60 mM, the uptake defect disappeared, possibly because the activity of a sodium-driven secondary transporter became predominant. Indeed, the NMB1965-defective mutant was unable to grow at a low sodium ion concentration (<20 mM) in a chemically defined medium containing L-glutamate and four other amino acids that supported meningococcal growth, but it grew when the sodium ion concentration was raised to higher values (>60 mM). The same growth phenotype was observed in the NMB1963-defective mutant. Cell invasion and intracellular persistence assays and expression data during cell invasion provided evidence that the L-glutamate ABC transporter, tentatively named GltT, was critical for meningococcal adaptation in the low-sodium intracellular environment.

* Corresponding author. Mailing address for Pietro Alifano: Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università di Lecce, Via Monteroni, 73100 Lecce, Italy. Phone: (39) 0832 320856. Fax: (39) 0832 320626. E-mail: alifano{at}ilenic.unile.it. Mailing address for Carmelo B. Bruni: Dipartimento di Biologia e Patologia Cellulare e Molecolare "L. Califano," Università di Napoli "Federico II," and Istituto di Endocrinologia ed Oncologia Sperimentale "G. Salvatore" of the C.N.R., Via S. Pansini 5, 80131 Napoli, Italy. Phone: (39) 081 7462047. Fax: (39) 081 7703285. E-mail: brucar{at}unina.it.

Editor: J. N. Weiser

Infection and Immunity, March 2006, p. 1725-1740, Vol. 74, No. 3
0019-9567/06/$08.00+0     doi:10.1128/IAI.74.3.1725-1740.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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