TroA of Streptococcus suis Is Required for Manganese Acquisition and Full Virulence

Schreur, Paul J. Wichgers; Rebel, Johanna M.J.; Smits, M.A.; Putten, Jos P. M. van; Smith, Hilde E.

doi:10.1128/jb.05305-11

Cited by 56 publications

(55 citation statements)

References 55 publications

(61 reference statements)

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“…Therefore, we named Atu3178, Atu3179, and Atu3180 troA, troB, and troC, respectively. In other bacteria, tro operons are involved in metal uptake and can transport either zinc or manganese and possibly iron (29,(33)(34)(35)(36). The A. tumefaciens troCBA operon (troCBA At ) was shown here to respond specifically to zinc limitation.…”

Section: Discussionmentioning

confidence: 77%

“…While ZnuA has been shown to respond specifically to zinc, the metal selectivity of TroA proteins and regulation of tro operons are different among bacteria (29,(33)(34)(35)(36). Streptococcus suis TroA is involved in the uptake of manganese, not zinc (36), even though it can bind both Mn 2ϩ and Zn 2ϩ with high affinity (35).…”

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confidence: 99%

“…Streptococcus suis TroA is involved in the uptake of manganese, not zinc (36), even though it can bind both Mn 2ϩ and Zn 2ϩ with high affinity (35). A gene encoding a protein that has high similarity to the manganese-responsive transcriptional regulator ScaR, located directly downstream of the S. suis troA gene, may be involved in the manganese regulation of the troA gene (36). Treponema denticola troABCD is negatively regulated by Mn 2ϩ and Fe 2ϩ via TroR (33).…”

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confidence: 99%

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Agrobacterium tumefaciens Zur Regulates the High-Affinity Zinc Uptake System TroCBA and the Putative Metal Chaperone YciC, along with ZinT and ZnuABC, for Survival under Zinc-Limiting Conditions

Chaoprasid

Dokpikul

Johnrod

et al. 2016

Appl Environ Microbiol

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Agrobacterium tumefaciens has a cluster of genes (Atu3178, Atu3179, and Atu3180) encoding an ABC-type transporter, here named troA, troB, and troC, respectively, which is shown here to be a zinc-specific uptake system. Reverse transcription (RT)-PCR analysis confirmed that troA, troB, and troC are cotranscribed, with troC as the first gene of the operon. The yciC (Atu3181) gene is transcribed in the opposite orientation to that of the troCBA operon and belongs to a metal-binding GTPase family. Expression of troCBA and yciC was inducible under zinc-limiting conditions and was controlled by the zinc uptake regulator, Zur. Compared to the wild type, the mutant strain lacking troC was hypersensitive to a metal chelator, EDTA, and the phenotype could be rescued by the addition of zinc, while the strain with a single yciC mutation showed no phenotype. However, yciC was important for survival under zinc limitation when either troC or zinT was inactivated. The periplasmic zinc-binding protein, ZinT, could not function when TroC was inactivated, suggesting that ZinT may interact with TroCBA in zinc uptake. Unlike many other bacteria, the ABC-type transporter ZnuABC was not the major zinc uptake system in A. tumefaciens. However, the important role of A. tumefaciens ZnuABC was revealed when TroCBA was impaired. The strain containing double mutations in the znuA and troC genes exhibited a growth defect in minimal medium. A. tumefaciens requires cooperation of zinc uptake systems and zinc chaperones, including TroCBA, ZnuABC, ZinT, and YciC, for survival under a wide range of zinc-limiting conditions. IMPORTANCEBoth host and pathogen battle over access to essential metals, including zinc. In low-zinc environments, physiological responses that make it possible to acquire enough zinc are important for bacterial survival and could determine the outcome of hostpathogen interactions. A. tumefaciens was found to operate a novel pathway for zinc uptake in which ZinT functions in concert with the high-affinity zinc importer TroCBA. Zinc is an essential metal for bacteria because it is required for the functions of many enzymes and proteins (1, 2). However, zinc overload is toxic to cells (3-7). Bacteria have mechanisms to maintain zinc homeostasis via the coordinated response of genes involved in zinc uptake, efflux, and storage (8-13). The zinc uptake regulator Zur is a transcriptional regulator belonging to the Fur family and functions as a repressor of zinc uptake genes, including znuABC and zinT (10). To prevent excessive amounts of zinc in cells under high-zinc conditions, Zur uses Zn 2ϩ as its cofactor to bind to a conserved AT-rich sequence, called the Zur box (14), found in the promoter region of the zinc uptake genes, leading to inhibition of gene expression (15)(16)(17). ZnuA is a periplasmic protein that binds zinc and transfers it to the membrane permease ZnuB and the ATPase ZnuC (15). The ZinT protein is a periplasmic zinc-binding protein (18-21) that has been shown to directly interact with and assist ZnuABC i...

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Section: Discussionmentioning

confidence: 77%

mentioning

confidence: 99%

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confidence: 99%

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Agrobacterium tumefaciens Zur Regulates the High-Affinity Zinc Uptake System TroCBA and the Putative Metal Chaperone YciC, along with ZinT and ZnuABC, for Survival under Zinc-Limiting Conditions

Chaoprasid

Dokpikul

Johnrod

et al. 2016

Appl Environ Microbiol

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“…The BALB/c mouse infection model (19,20) was used to compare the virulence of the new serotype isolate with that of two known virulent serotype 2 S. suis strains, P1/7 and 9801 (21,22). A total of 5 ϫ 10 7 CFU/mouse of each strain was injected intraperitoneally (10 mice per strain) to obtain the survival curve.…”

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confidence: 99%

“…In accordance with the bacterial colonization capacity in vivo, we used the human laryngeal carcinoma cell line HEp-2 and mouse brain microvascular endothelial cells (bEnd.3) as in the models of bacterial colonization (19,20,23) and meningitis (24,25) in vitro, respectively. The adherence assays were performed as previously described (26).…”

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confidence: 99%

Novel Variant Serotype of Streptococcus suis Isolated from Piglets with Meningitis

Pan

Wang³

et al. 2015

Appl Environ Microbiol

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cStreptococcus suis is an emerging zoonotic pathogen causing severe infections in pigs and humans. In previous studies, 33 serotypes of S. suis have been identified using serum agglutination. Here, we describe a novel S. suis strain, CZ130302, isolated from an outbreak of acute piglet meningitis in eastern China. Strong pathogenicity of meningitis caused by strain CZ130302 was reproduced in the BALB/c mouse model. The strain showed a high fatality rate (8/10), higher than those for known virulent serotype 2 strains P1/7 (1/10) and 9801 (2/10). Cell adhesion assay results with bEnd.3 and HEp2 cells showed that CZ130302 was significantly close to P1/7 and 9801. Both the agglutination test and its complementary test showed that strain CZ130302 had no strong cross-reaction with the other 33 S. suis serotypes. The multiplex PCR assays revealed no specified bands for all four sets used to detect the other 33 serotypes. In addition, genetic analysis of the whole cps gene clusters of all serotypes was performed in this study. The results of comparative genomics showed that the cps gene cluster of CZ130302, which was not previously reported, showed no homology to the gene sequences of the other strains. Especially, the wzy, wzx, and acetyltransferase genes of strain CZ130302 are phylogenetically distinct from strains of the other 33 serotypes. Therefore, this study suggested that strain CZ130302 represents a novel variant serotype of S. suis (designated serotype Chz) which has a high potential to be virulent and associated with meningitis in animals. Streptococcus suis causes meningitis and septicemia in pigs and is also known as a zoonotic agent (1). Human infections of S. suis were first reported in Denmark in 1968 (2). Since then, this pathogen has spread all over the world. The human Streptococcus suis was epidemic in most Europe countries (3, 4), as well as in Asian countries, such as Vietnam and Thailand (5-7). In China, two outbreaks of human streptococcosis have occurred, affecting more than 100 people and causing 39 deaths (8). More and more S. suis infections from China, Thailand, Hong Kong, Taiwan, and Singapore have been reported, which indicates that S. suis has been an important cause of adult meningitis, endocarditis, septicemia, and arthritis in Asia (9).The serotyping of S. suis isolates rests on the basis of the antigenicity of their capsular polysaccharides (CPs); 35 serotypes have been identified by agglutination tests (10). With the development of sequence analysis of 16S rRNA and cpn60 genes in S. suis, the original S. suis serotypes 32 and 34 were reclassified as Streptococcus orisratti (11). Phylogenetic analyses of the cps gene cluster, conserved Wzy polymerase, Wzx flippase, and glycosyltransferase are all taken as important means of classifying a novel serotype (12). Multiplex PCR assays against the specific genes of the cps clusters have also been developed to identify serotypes in S. suis (13)(14)(15).From March to May 2013, strain CZ130302 caused an outbreak of streptococcosis in piglets at ...

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The Cluster A‐I Solute‐Binding Proteins

Yukl

2017

Encyclopedia of Inorganic and Bioinorganic Chemistry

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Iron, zinc, and manganese are essential nutrients required for the function of a wide variety of proteins and enzymes. Thus, their acquisition from the environment is an absolute necessity. In bacteria, high‐affinity uptake of these metals is undertaken by the cluster A‐I solute‐binding proteins (SBPs) associated with ATP‐binding cassette (ABC) transporters. This process is of particular interest to the biomedical community because bacterial ABC transporters of metals are important virulence factors. Many crystal structures of cluster A‐I SBPs are available in both metal‐bound (holo) and metal‐free (apo) states. These structures provide a wealth of information regarding metal coordination environment, specificity, and conformational changes accompanying metal binding and release. Also presented are early examples of how inhibition of metal transport through ABC transporters is being achieved by disrupting cluster A‐I SBP function.

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TroA of Streptococcus suis Is Required for Manganese Acquisition and Full Virulence

Cited by 56 publications

References 55 publications

Agrobacterium tumefaciens Zur Regulates the High-Affinity Zinc Uptake System TroCBA and the Putative Metal Chaperone YciC, along with ZinT and ZnuABC, for Survival under Zinc-Limiting Conditions

Agrobacterium tumefaciens Zur Regulates the High-Affinity Zinc Uptake System TroCBA and the Putative Metal Chaperone YciC, along with ZinT and ZnuABC, for Survival under Zinc-Limiting Conditions

Novel Variant Serotype of Streptococcus suis Isolated from Piglets with Meningitis

The Cluster A‐I Solute‐Binding Proteins

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