On sialic acid transport and utilization by Vibrio cholerae

Thomas, Gavin H.; Boyd, E. Fidelma

doi:10.1099/mic.0.054692-0

Cited by 11 publications

(12 citation statements)

References 15 publications

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“…They argued that in an El Tor strain of V. cholerae, VC1929 was a mannose-sensitive hemagglutinin that was required for sialic acid utilization (41). This was an unexpected finding since VC1929 shared high sequence homology with C4-dicarboxylate permeases that are involved in the transport of malate, fumurate, or succinate (45). Recently, we investigated the role of DctP (VC1929) in V. cholerae using its nonpolar knockout mutant and demonstrated that it plays a role in C4-dicarboxylate but not sialic acid uptake (our unpublished data).…”

Section: Fig 4 Growth Analysis Of V Vulnificus In M9 Minimal Medium mentioning

confidence: 95%

“…The homologous TRAP transporter associated with the SAC cluster in Haemophilus influenzae was shown to be highly efficient in the uptake of sialic acid (14,27,40). It has been more recently demonstrated in V. cholerae that the SBP of the TRAP transporter SiaPQM (VC1777 to VC1779) is a Na ϩ -dependent high-affinity secondary transporter for sialic acid also (28,45).…”

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confidence: 99%

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Sialic Acid Catabolism and Transport Gene Clusters Are Lineage Specific in Vibrio vulnificus

Lubin

Kingston

Chowdhury

et al. 2012

Appl Environ Microbiol

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ABSTRACTSialic or nonulosonic acids are nine-carbon alpha ketosugars that are present in all vertebrate mucous membranes. Among bacteria, the ability to catabolize sialic acid as a carbon source is present mainly in pathogenic and commensal species of animals. Previously, it was shown that severalVibriospecies carry homologues of the genes required for sialic acid transport and catabolism, which are genetically linked. InVibrio choleraeon chromosome I, these genes are carried on theVibriopathogenicity island-2 region, which is confined to pathogenic isolates. We found that among the three sequencedVibrio vulnificusclinical strains, these genes are present on chromosome II and are not associated with a pathogenicity island. To determine whether the sialic acid transport (SAT) and catabolism (SAC) region is universally present withinV. vulnificus, we examined 67 natural isolates whose phylogenetic relationships are known. We found that the region was present predominantly among lineage I ofV. vulnificus, which is comprised mainly of clinical isolates. We demonstrate that the isolates that contain this region can catabolize sialic acid as a sole carbon source. Two putative transporters are genetically linked to the region inV. vulnificus, the tripartite ATP-independent periplasmic (TRAP) transporter SiaPQM and a component of an ATP-binding cassette (ABC) transporter. We constructed an in-frame deletion mutation insiaM, a component of the TRAP transporter, and demonstrate that this transporter is essential for sialic acid uptake in this species. Expression analysis of the SAT and SAC genes indicates that sialic acid is an inducer of expression. Overall, our study demonstrates that the ability to catabolize and transport sialic acid is predominately lineage specific inV. vulnificusand that the TRAP transporter is essential for sialic acid uptake.

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Section: Fig 4 Growth Analysis Of V Vulnificus In M9 Minimal Medium mentioning

confidence: 95%

mentioning

confidence: 99%

Sialic Acid Catabolism and Transport Gene Clusters Are Lineage Specific in Vibrio vulnificus

Lubin

Kingston

Chowdhury

et al. 2012

Appl Environ Microbiol

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“…Besides serving as attachment and recognition point for various pathogens, Neu5Ac is also an important source of carbon and energy available in various host niches such as the oral cavity and the respiratory, intestinal, and urogenital tracts (29)(30)(31)(32). Therefore, Neu5Ac metabolism and its control have been studied in detail for various, often pathogenic, bacteria such as Escherichia coli, Vibrio vulnificus, Staphylococcus aureus, Streptococcus pneumoniae, Haemophilus influenzae, Clostridium perfringens, and the probiotic Bifidobacterium breve (33)(34)(35)(36)(37)(38). In H. influenzae, transcription of the nan and the siaPT operons for Neu5Ac utilization is repressed by SiaR and is activated in the presence of glucosamine 6-phosphate (see Table S1 in the supplemental material), which is an intermediate of Neu5Ac catabolism and acts as a coactivator of the RpiR-type regulator SiaR (37,(39)(40)(41).…”

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Transcription of Sialic Acid Catabolism Genes in Corynebacterium glutamicum Is Subject to Catabolite Repression and Control by the Transcriptional Repressor NanR

et al. 2016

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Corynebacterium glutamicum metabolizes sialic acid (Neu5Ac) to fructose-6-phosphate (fructose-6P) via the consecutive activity of the sialic acid importer SiaEFGI, N-acetylneuraminic acid lyase (NanA), N-acetylmannosamine kinase (NanK), N-acetylmannosamine-6P epimerase (NanE), N-acetylglucosamine-6P deacetylase (NagA), and glucosamine-6P deaminase (NagB). Within the cluster of the three operons nagAB, nanAKE, and siaEFGI for Neu5Ac utilization a fourth operon is present, which comprises cg2936, encoding a GntR-type transcriptional regulator, here named NanR. Microarray studies and reporter gene assays showed that nagAB, nanAKE, siaEFGI, and nanR are repressed in wild-type (WT) C. glutamicum but highly induced in a ⌬nanR C. glutamicum mutant. Purified NanR was found to specifically bind to the nucleotide motifs A [AC]G[CT][AC]TGATGT C[AT][TG]ATGT[AC]TA located within the nagA-nanA and nanR-sialA intergenic regions. Binding of NanR to promoter regions was abolished in the presence of the Neu5Ac metabolism intermediates GlcNAc-6P and N-acetylmannosamine-6-phosphate (ManNAc-6P). We observed consecutive utilization of glucose and Neu5Ac as well as fructose and Neu5Ac by WT C. glutamicum, whereas the deletion mutant C. glutamicum ⌬nanR simultaneously consumed these sugars. Increased reporter gene activities for nagAB, nanAKE, and nanR were observed in cultivations of WT C. glutamicum with Neu5Ac as the sole substrate compared to cultivations when fructose was present. Taken together, our findings show that Neu5Ac metabolism in C. glutamicum is subject to catabolite repression, which involves control by the repressor NanR. IMPORTANCENeu5Ac utilization is currently regarded as a common trait of both pathogenic and commensal bacteria. Interestingly, the nonpathogenic soil bacterium C. glutamicum efficiently utilizes Neu5Ac as a substrate for growth. Expression of genes for Neu5Ac utilization in C. glutamicum is here shown to depend on the transcriptional regulator NanR, which is the first GntR-type regulator of Neu5Ac metabolism not to use Neu5Ac as effector but relies instead on the inducers GlcNAc-6P and ManNAc-6P. The identification of conserved NanR-binding sites in intergenic regions within the operons for Neu5Ac utilization in pathogenic Corynebacterium species indicates that the mechanism for the control of Neu5Ac catabolism in C. glutamicum by NanR as described in this work is probably conserved within this genus. The Gram-positive Corynebacterium glutamicum is mostly known for its application in the industrial production of amino acids, mainly L-glutamate and L-lysine (1, 2), and has become a versatile cell factory for the production of various commodity products (3-5). C. glutamicum utilizes a large variety of sugars and organic acids as sources of carbon and energy (6, 7) and additionally has been genetically engineered for the utilization of alternative feedstocks such as starch, glycerol, xylose, glucuronic acid, and N-acetylglucosamine (8-12). In contrast to many other bacterial species, C. glutamic...

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“…A siaPQM (vc1777, vc1778 and vc1779 encode siaM, siaQ and siaP, respectively) homologue that encodes a substrate binding-dependent (SBP) secondary transporter belonging to the TRAP transporter family is genetically linked with the SAC gene cluster in V. cholerae (Jermyn & Boyd, 2002;Almagro-Moreno & Boyd, 2009a, b;Fischer et al, 2010;Mulligan et al, 2011Mulligan et al, , 2012 and has been characterized in vitro as a sialic acid transporter (Mulligan et al, 2009(Mulligan et al, , 2012Thomas & Boyd, 2011). The TRAP transporter (SiaPQM or SiaPT) associated with the SAC gene cluster in H. influenzae has been shown to be highly efficient in the uptake of sialic acid (Allen et al, 2005;Severi et al, 2005;Müller et al, 2006;Mulligan et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

“…However, VC1929 is a part of a TRAP gene cluster (vc1927, vc1928 and vc1929 encode dctM, dctQ and dctP, respectively), which is more similar to the C 4 -dicarboxylate-binding members of the TRAP family (Thomas & Boyd, 2011). Moreover, the vc1927-vc1929 genes are adjacent to two genes (vc1925/vc1926) encoding homologues of the twocomponent sensor-regulator system DctS/DctR that likely sense C 4 -dicarboxylates such as malate, fumarate and succinate (Thomas & Boyd, 2011).…”

Section: Introductionmentioning

confidence: 99%

The VC1777–VC1779 proteins are members of a sialic acid-specific subfamily of TRAP transporters (SiaPQM) and constitute the sole route of sialic acid uptake in the human pathogen Vibrio cholerae

et al. 2012

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On sialic acid transport and utilization by Vibrio cholerae

Cited by 11 publications

References 15 publications

Sialic Acid Catabolism and Transport Gene Clusters Are Lineage Specific in Vibrio vulnificus

Sialic Acid Catabolism and Transport Gene Clusters Are Lineage Specific in Vibrio vulnificus

Transcription of Sialic Acid Catabolism Genes in Corynebacterium glutamicum Is Subject to Catabolite Repression and Control by the Transcriptional Repressor NanR

The VC1777–VC1779 proteins are members of a sialic acid-specific subfamily of TRAP transporters (SiaPQM) and constitute the sole route of sialic acid uptake in the human pathogen Vibrio cholerae

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