An Uncharacterized Member of the Gls24 Protein Superfamily Is a Putative Sensor of Essential Amino Acid Availability in Streptococcus pneumoniae.


Journal

Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663

Informations de publication

Date de publication:
Feb 2019
Historique:
received: 10 01 2018
accepted: 03 06 2018
pubmed: 7 7 2018
medline: 1 3 2019
entrez: 7 7 2018
Statut: ppublish

Résumé

Proteins belonging to the Gls24 superfamily are involved in survival of pathogenic Gram-positive cocci under oligotrophic conditions and other types of stress, by a still unknown molecular mechanism. In Firmicutes, this superfamily includes three different valine-rich orthologal families (Gls24A, B, C) with different potential interactive partners. Whereas the Streptococcus pneumoniae Δgls24A deletion mutant experienced a general long growth delay, the Δgls24B mutant grew as the parental strain in the semisynthetic AGCH medium but failed to grow in the complex Todd-Hewitt medium. Bovine seroalbumin (BSA) was the component responsible for this phenotype. The effect of BSA on growth was concentration-dependent and was maintained when the protein was proteolyzed but not when heat-denatured, suggesting that BSA dependence was related to oligopeptide supplementation. Global transcriptional analyses of the knockout mutant revealed catabolic derepression and induction of chaperone and oligopeptide transport genes. This mutant also showed increased sensibility to cadmium and high temperature. The Δgls24B mutant behaved as a poor colonizer in the nasopharynx of mice and showed 20-fold competence impairment. Experimental data suggest that Gls24B plays a central role as a sensor of amino acid availability and its connection to sugar catabolism. This metabolic rewiring can be compensated in vitro, at the expenses of external oligopeptide supplementation, but reduce important bacteria skills prior to efficiently address systemic virulence traits. This is an example of how metabolic factors conserved in enterococci, streptococci, and staphylococci can be essential for survival in poor oligopeptide environments prior to infection progression.

Identifiants

pubmed: 29978356
doi: 10.1007/s00248-018-1218-9
pii: 10.1007/s00248-018-1218-9
doi:

Substances chimiques

Amino Acids, Essential 0
Bacterial Proteins 0
Culture Media 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

471-487

Subventions

Organisme : Ministerio de Economía y Competitividad
ID : BIO2014-55462-R
Organisme : Ministerio de Economía y Competitividad
ID : SAF2012-39444-C02

Références

J Mol Biol. 1999 Sep 17;292(2):195-202
pubmed: 10493868
Nucleic Acids Res. 2000 Jan 1;28(1):33-6
pubmed: 10592175
Microbiology. 2000 Jan;146 ( Pt 1):107-17
pubmed: 10658657
Int J Food Microbiol. 2000 Apr 10;55(1-3):99-102
pubmed: 10791725
J Bacteriol. 2001 Mar;183(6):1843-52
pubmed: 11222581
J Bacteriol. 2001 Oct;183(19):5709-17
pubmed: 11544234
FEMS Microbiol Lett. 2002 Jan 10;206(2):235-9
pubmed: 11814669
Mol Microbiol. 2002 Sep;45(5):1389-406
pubmed: 12207705
Antimicrob Agents Chemother. 2003 Apr;47(4):1257-61
pubmed: 12654655
J Exp Med. 1962 Oct 1;116:491-519
pubmed: 13940741
Genetics. 1964 Jul;50:31-44
pubmed: 14191356
Mol Microbiol. 2003 Nov;50(4):1103-10
pubmed: 14622402
Mol Microbiol. 2004 Feb;51(4):1051-70
pubmed: 14763980
Clin Infect Dis. 2004 Mar 1;38(5):632-9
pubmed: 14986245
Lancet Infect Dis. 2004 Mar;4(3):144-54
pubmed: 14998500
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
J Bacteriol. 2004 Apr;186(8):2511-4
pubmed: 15060059
Infect Immun. 2004 Jul;72(7):3902-6
pubmed: 15213133
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W424-8
pubmed: 15215423
Microbiology. 2004 Jul;150(Pt 7):2313-25
pubmed: 15256573
J Infect Dis. 2005 Feb 1;191(3):472-80
pubmed: 15633107
Nucleic Acids Res. 2005 Feb 08;33(3):880-92
pubmed: 15701760
Mol Biol Evol. 2005 Nov;22(11):2147-56
pubmed: 16014871
Infect Immun. 2005 Nov;73(11):7772-4
pubmed: 16239583
J Bacteriol. 2005 Dec;187(24):8340-9
pubmed: 16321938
Mol Microbiol. 2006 Feb;59(4):1297-307
pubmed: 16430701
Curr Opin Microbiol. 2007 Apr;10(2):146-51
pubmed: 17383224
Proc Natl Acad Sci U S A. 2009 Jan 27;106(4):1234-8
pubmed: 19141630
Environ Microbiol. 2009 Oct;11(10):2542-55
pubmed: 19549167
J Mol Med (Berl). 2010 Feb;88(2):97-102
pubmed: 19898768
FEMS Microbiol Lett. 2010 Jan;302(1):69-75
pubmed: 19903200
Science. 1991 May 24;252(5009):1162-4
pubmed: 2031185
Microbiology. 2011 Feb;157(Pt 2):572-82
pubmed: 20947575
Infect Immun. 2011 Jan;79(1):44-58
pubmed: 21078855
Anal Chem. 2011 Apr 1;83(7):2677-84
pubmed: 21395229
J Infect Dis. 2011 Apr 15;203(8):1147-54
pubmed: 21451003
Mol Biol Evol. 2011 Oct;28(10):2731-9
pubmed: 21546353
Infect Immun. 2011 Oct;79(10):4193-200
pubmed: 21825065
J Biol Chem. 2011 Dec 30;286(52):44594-605
pubmed: 22084243
J Biol Chem. 2012 Feb 3;287(6):4260-74
pubmed: 22167202
PLoS One. 2012;7(3):e33320
pubmed: 22428019
PLoS One. 2014 Jul 14;9(7):e101574
pubmed: 25019515
Mol Microbiol. 2014 Sep;93(6):1259-68
pubmed: 25074408
BMC Genomics. 2014 Aug 05;15:652
pubmed: 25096389
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
PLoS One. 2015 Mar 31;10(3):e0121042
pubmed: 25826206
Nucleic Acids Res. 2015 Jul 1;43(W1):W39-49
pubmed: 25953851
J Biol Chem. 2015 Aug 28;290(35):21185-98
pubmed: 26085091
FEMS Microbiol Lett. 1989 Nov;53(1-2):113-8
pubmed: 2612880
Front Microbiol. 2015 Oct 07;6:1041
pubmed: 26500614
Infect Immun. 2015 Nov 02;84(1):286-92
pubmed: 26527213
Nucleic Acids Res. 2016 Jan 4;44(D1):D330-5
pubmed: 26635392
Nucleic Acids Res. 2016 Sep 6;44(15):7292-303
pubmed: 27378778
Nucleic Acids Res. 2017 Jan 4;45(D1):D362-D368
pubmed: 27924014
Front Microbiol. 2017 May 19;8:883
pubmed: 28579978
Bioinformatics. 2017 Nov 1;33(21):3454-3460
pubmed: 29036270
Mol Biol Evol. 1987 Jul;4(4):406-25
pubmed: 3447015
Biochem Biophys Res Commun. 1995 Feb 27;207(3):978-84
pubmed: 7864904
J Mol Biol. 1994 Aug 5;241(1):44-58
pubmed: 8051706
Appl Environ Microbiol. 1997 Feb;63(2):812-4
pubmed: 9023964
Res Microbiol. 1997 Jan;148(1):27-35
pubmed: 9404502
Appl Environ Microbiol. 1998 Nov;64(11):4238-45
pubmed: 9797271

Auteurs

María J Ferrándiz (MJ)

Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain.

María I Cercenado (MI)

Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain.

Miriam Domenech (M)

Centro de Investigaciones Biológicas (CIB-CSIC), Madrid, Spain.
CIBER de Enfermedades Respiratorias (CIBERES), Madrid, Spain.

José M Tirado-Vélez (JM)

Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain.

María S Escolano-Martínez (MS)

Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain.

Jose Yuste (J)

Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain.
CIBER de Enfermedades Respiratorias (CIBERES), Madrid, Spain.

Ernesto García (E)

Centro de Investigaciones Biológicas (CIB-CSIC), Madrid, Spain.
CIBER de Enfermedades Respiratorias (CIBERES), Madrid, Spain.

Adela G de la Campa (AG)

Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain.
Presidencia, Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain.

Antonio J Martín-Galiano (AJ)

Centro Nacional de Microbiología, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain. mgaliano@isciii.es.

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Classifications MeSH