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Temperature-dependent expression of virulence genes in fish-pathogenic bacteria.

Guijarro JA, Cascales D, García-Torrico AI, García-Domínguez M, Méndez J - Front Microbiol (2015)

Bottom Line: A key factor in this expression is temperature.This is an interesting issue and progress needs to be made in order to diminish the economic losses caused by these diseases.The intention of this review is, for the first time, to compile the scattered results existing in the field in order to lay the groundwork for future research.

View Article: PubMed Central - PubMed

ABSTRACT
Virulence gene expression in pathogenic bacteria is modulated by environmental parameters. A key factor in this expression is temperature. Its effect on virulence gene expression in bacteria infecting warm-blooded hosts is well documented. Transcription of virulence genes in these bacteria is induced upon a shift from low environmental to a higher host temperature (37°C). Interestingly, host temperatures usually correspond to the optimum for growth of these pathogenic bacteria. On the contrary, in ectothermic hosts such as fish, molluscs, and amphibians, infection processes generally occur at a temperature lower than that for the optimal growth of the bacteria. Therefore, regulation of virulence gene expression in response to temperature shift has to be modulated in a different way to that which is found in bacteria infecting warm-blooded hosts. The current understanding of virulence gene expression and its regulation in response to temperature in fish-pathogenic bacteria is limited, but constant extension of our knowledge base is essential to enable a rational approach to the problem of the bacterial fish diseases affecting the aquaculture industry. This is an interesting issue and progress needs to be made in order to diminish the economic losses caused by these diseases. The intention of this review is, for the first time, to compile the scattered results existing in the field in order to lay the groundwork for future research. This article is an overview of those relevant virulence genes that are expressed at temperatures lower than that for optimal bacterial growth in different fish-pathogenic bacteria as well as the principal mechanisms that could be involved in their regulation.

No MeSH data available.


Related in: MedlinePlus

Model for temperature signal transduction in Edwardsiella tarda by the PhoP–PhoQ two-component regulatory system. PhoQ displays a different structure at 37°C as compared with 30°C. Autophosphorylation of PhoQ only takes place in a defined range of temperature around 30°C and leads to a subsequent phosphorylation of the response regulator PhoP. PhoP-P is now able to bind to upstream regions of phoP–phoQ and esrB, a response regulator of the EsrA–EsrB two component system, leading to an increase in the synthesis of both PhoP–PhoQ and EsrB. EsrB could be now phosphorylated by EsrA-P, a process depending on an unknown signal (s). EsrB-P binds to the promoter region of both virulence-related T3SS and T6SS activating their transcription.
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Figure 4: Model for temperature signal transduction in Edwardsiella tarda by the PhoP–PhoQ two-component regulatory system. PhoQ displays a different structure at 37°C as compared with 30°C. Autophosphorylation of PhoQ only takes place in a defined range of temperature around 30°C and leads to a subsequent phosphorylation of the response regulator PhoP. PhoP-P is now able to bind to upstream regions of phoP–phoQ and esrB, a response regulator of the EsrA–EsrB two component system, leading to an increase in the synthesis of both PhoP–PhoQ and EsrB. EsrB could be now phosphorylated by EsrA-P, a process depending on an unknown signal (s). EsrB-P binds to the promoter region of both virulence-related T3SS and T6SS activating their transcription.

Mentions: Edwardsiella tarda infects many species of farmed fish, causing “Edwardsiellosis,” a haemorrhagic septicaemia that leads to important losses in aquaculture (Thune et al., 1993; Austin and Austin, 2007). This Gram-negative bacterium has a broad host range and also causes infections in higher animals, including humans, in which it causes gastrointestinal disorders (Plumb, 1993) and bacteraemia (Yang and Wang, 1999) amongst other pathologies (Osiri et al., 1997; Slaven et al., 2001). Although pathogenesis of E. tarda is multifactorial, the two-component system PhoP–PhoQ detects changes in environmental temperature (Chakraborty et al., 2010). Indeed, PhoQ is a histidine kinase which senses temperature changes through conformational modification in its secondary structures (Figure 4). As a result, autophosphorylation of PhoQ only takes places over a defined range of temperature around 30°C (Figure 4). This allows the transfer of the phosphate group from PhoQ to PhoP. When phosphorylated, PhoP binds to the promoter region of esrB and activates its transcription (Figure 4). EsrB is a response regulator of another two-component system (EsrA–EsrB). Phosphorylated EsrB binds to the promoter region of at least two clusters of genes codifying type III (EseBCD) and type VI (EvpA-H) secretion systems, activating their transcription (Srinivasa Rao et al., 2004; Chakraborty et al., 2010; Figure 4). Both Type III and Type VI secretion systems are associated with virulence in this bacterium (Srinivasa Rao et al., 2003, 2004; Zheng et al., 2005; Wang et al., 2009). Interestingly, expression of these clusters together with esrB was temperature-dependent and was higher at 25°C than at 37°C (Srinivasa Rao et al., 2004). In the same way, expression of evpA and evpC was reduced by 84% at 37°C when compared with expression at 25°C (Srinivasa Rao et al., 2004). Therefore, these genes, essential for virulence in E. tarda, were suppressed at 37°C. Besides, a total of 13 proteins in E. tarda were found to require the presence of PhoP for full expression, specifically the zinc metalloprotease Sip1 (Lv et al., 2013). This was found to be essential for serum resistance and host infection (Zhou et al., 2015), corroborating once more the relation between TBO induction of PhoP and E. tarda virulence. Protein secretion was also significantly lowered at 37°C in E. tarda compared to 25°C. In addition, in a challenge experiment, 90% of the fish injected with cells grown at 37°C survived, whereas 70% of the fish died when they received bacteria grown at 25°C (Srinivasa Rao et al., 2004). These results clearly established that the expression of these two protein secretion systems involved in the virulence of E. tarda was significantly lower at 37°C than at 25°C and depends on the PhoP–PhoQ system.


Temperature-dependent expression of virulence genes in fish-pathogenic bacteria.

Guijarro JA, Cascales D, García-Torrico AI, García-Domínguez M, Méndez J - Front Microbiol (2015)

Model for temperature signal transduction in Edwardsiella tarda by the PhoP–PhoQ two-component regulatory system. PhoQ displays a different structure at 37°C as compared with 30°C. Autophosphorylation of PhoQ only takes place in a defined range of temperature around 30°C and leads to a subsequent phosphorylation of the response regulator PhoP. PhoP-P is now able to bind to upstream regions of phoP–phoQ and esrB, a response regulator of the EsrA–EsrB two component system, leading to an increase in the synthesis of both PhoP–PhoQ and EsrB. EsrB could be now phosphorylated by EsrA-P, a process depending on an unknown signal (s). EsrB-P binds to the promoter region of both virulence-related T3SS and T6SS activating their transcription.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4496569&req=5

Figure 4: Model for temperature signal transduction in Edwardsiella tarda by the PhoP–PhoQ two-component regulatory system. PhoQ displays a different structure at 37°C as compared with 30°C. Autophosphorylation of PhoQ only takes place in a defined range of temperature around 30°C and leads to a subsequent phosphorylation of the response regulator PhoP. PhoP-P is now able to bind to upstream regions of phoP–phoQ and esrB, a response regulator of the EsrA–EsrB two component system, leading to an increase in the synthesis of both PhoP–PhoQ and EsrB. EsrB could be now phosphorylated by EsrA-P, a process depending on an unknown signal (s). EsrB-P binds to the promoter region of both virulence-related T3SS and T6SS activating their transcription.
Mentions: Edwardsiella tarda infects many species of farmed fish, causing “Edwardsiellosis,” a haemorrhagic septicaemia that leads to important losses in aquaculture (Thune et al., 1993; Austin and Austin, 2007). This Gram-negative bacterium has a broad host range and also causes infections in higher animals, including humans, in which it causes gastrointestinal disorders (Plumb, 1993) and bacteraemia (Yang and Wang, 1999) amongst other pathologies (Osiri et al., 1997; Slaven et al., 2001). Although pathogenesis of E. tarda is multifactorial, the two-component system PhoP–PhoQ detects changes in environmental temperature (Chakraborty et al., 2010). Indeed, PhoQ is a histidine kinase which senses temperature changes through conformational modification in its secondary structures (Figure 4). As a result, autophosphorylation of PhoQ only takes places over a defined range of temperature around 30°C (Figure 4). This allows the transfer of the phosphate group from PhoQ to PhoP. When phosphorylated, PhoP binds to the promoter region of esrB and activates its transcription (Figure 4). EsrB is a response regulator of another two-component system (EsrA–EsrB). Phosphorylated EsrB binds to the promoter region of at least two clusters of genes codifying type III (EseBCD) and type VI (EvpA-H) secretion systems, activating their transcription (Srinivasa Rao et al., 2004; Chakraborty et al., 2010; Figure 4). Both Type III and Type VI secretion systems are associated with virulence in this bacterium (Srinivasa Rao et al., 2003, 2004; Zheng et al., 2005; Wang et al., 2009). Interestingly, expression of these clusters together with esrB was temperature-dependent and was higher at 25°C than at 37°C (Srinivasa Rao et al., 2004). In the same way, expression of evpA and evpC was reduced by 84% at 37°C when compared with expression at 25°C (Srinivasa Rao et al., 2004). Therefore, these genes, essential for virulence in E. tarda, were suppressed at 37°C. Besides, a total of 13 proteins in E. tarda were found to require the presence of PhoP for full expression, specifically the zinc metalloprotease Sip1 (Lv et al., 2013). This was found to be essential for serum resistance and host infection (Zhou et al., 2015), corroborating once more the relation between TBO induction of PhoP and E. tarda virulence. Protein secretion was also significantly lowered at 37°C in E. tarda compared to 25°C. In addition, in a challenge experiment, 90% of the fish injected with cells grown at 37°C survived, whereas 70% of the fish died when they received bacteria grown at 25°C (Srinivasa Rao et al., 2004). These results clearly established that the expression of these two protein secretion systems involved in the virulence of E. tarda was significantly lower at 37°C than at 25°C and depends on the PhoP–PhoQ system.

Bottom Line: A key factor in this expression is temperature.This is an interesting issue and progress needs to be made in order to diminish the economic losses caused by these diseases.The intention of this review is, for the first time, to compile the scattered results existing in the field in order to lay the groundwork for future research.

View Article: PubMed Central - PubMed

ABSTRACT
Virulence gene expression in pathogenic bacteria is modulated by environmental parameters. A key factor in this expression is temperature. Its effect on virulence gene expression in bacteria infecting warm-blooded hosts is well documented. Transcription of virulence genes in these bacteria is induced upon a shift from low environmental to a higher host temperature (37°C). Interestingly, host temperatures usually correspond to the optimum for growth of these pathogenic bacteria. On the contrary, in ectothermic hosts such as fish, molluscs, and amphibians, infection processes generally occur at a temperature lower than that for the optimal growth of the bacteria. Therefore, regulation of virulence gene expression in response to temperature shift has to be modulated in a different way to that which is found in bacteria infecting warm-blooded hosts. The current understanding of virulence gene expression and its regulation in response to temperature in fish-pathogenic bacteria is limited, but constant extension of our knowledge base is essential to enable a rational approach to the problem of the bacterial fish diseases affecting the aquaculture industry. This is an interesting issue and progress needs to be made in order to diminish the economic losses caused by these diseases. The intention of this review is, for the first time, to compile the scattered results existing in the field in order to lay the groundwork for future research. This article is an overview of those relevant virulence genes that are expressed at temperatures lower than that for optimal bacterial growth in different fish-pathogenic bacteria as well as the principal mechanisms that could be involved in their regulation.

No MeSH data available.


Related in: MedlinePlus