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Altruism of Shiga toxin-producing Escherichia coli: recent hypothesis versus experimental results.

Loś JM, Loś M, Węgrzyn A, Węgrzyn G - Front Cell Infect Microbiol (2013)

Bottom Line: Shiga toxin-producing Escherichia coli (STEC) may cause bloody diarrhea and hemorrhagic colitis (HC), with subsequent systemic disease.Recently, a hypothesis was proposed (simultaneously but independently by two research groups) that STEC may benefit from Shiga toxin production as a result of toxin-dependent killing of eukaryotic cells such as unicellular predators or human leukocytes.On the other hand, analysis of recently published results, discussed here, indicated that the efficiency of prophage excision under conditions that may likely occur in the natural habitat of STEC is sufficiently low to ensure survival of a large fraction of the bacterial host.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Genetics, Department of Molecular Biology, University of Gdańsk Gdańsk, Poland.

ABSTRACT
Shiga toxin-producing Escherichia coli (STEC) may cause bloody diarrhea and hemorrhagic colitis (HC), with subsequent systemic disease. Since genes coding for Shiga toxins (stx genes) are located on lambdoid prophages, their effective production occurs only after prophage induction. Such induction and subsequent lytic development of Shiga toxin-converting bacteriophages results not only in production of toxic proteins, but also in the lysis (and thus, the death) of the host cell. Therefore, one may ask the question: what is the benefit for bacteria to produce the toxin if they die due to phage production and subsequent cell lysis? Recently, a hypothesis was proposed (simultaneously but independently by two research groups) that STEC may benefit from Shiga toxin production as a result of toxin-dependent killing of eukaryotic cells such as unicellular predators or human leukocytes. This hypothesis could make sense only if we assume that prophage induction (and production of the toxin) occurs only in a small fraction of bacterial cells, thus, a few members of the population are sacrificed for the benefit of the rest, providing an example of "bacterial altruism." However, various reports indicating that the frequency of spontaneous induction of Shiga toxin-converting prophages is higher than that of other lambdoid prophages might seem to contradict the for-mentioned model. On the other hand, analysis of recently published results, discussed here, indicated that the efficiency of prophage excision under conditions that may likely occur in the natural habitat of STEC is sufficiently low to ensure survival of a large fraction of the bacterial host. A molecular mechanism by which partial prophage induction may occur is proposed. We conclude that the published data supports the proposed model of bacterial "altruism" where prophage induction occurs at a low enough frequency to render toxin production a positive selective force on the general STEC population.

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The model of STEC altruism, representing the hypothesis on the benefit which E. coli lysogenic with Shiga toxin-converting phages may gain from production of Shiga toxins coupled with prophage induction and subsequent cell death. (A) A protozoan predator (exemplified by Tetrahymena) releases hydrogen peroxide to damage bacterial cells. (B) In the case of STEC, hydrogen peroxide causes induction of Shiga toxin-converting prophage in a small fraction of bacterial cells, which is, nevertheless, sufficient to produce Shiga toxins (Stx) in amounts enough to kill the predator. (C) Neutrophils employ a strategy similar to that used by protozoan predators if human intestine is infected with bacteria recognized as aliens. (D) The response of STEC to neutrophils' attack is analogous to that employed by this bacterium to faith against unicellular eukaryotic predators. The original hypothesis was presented in two articles (Łoś et al., 2011; Mauro and Koudelka, 2011).
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Figure 1: The model of STEC altruism, representing the hypothesis on the benefit which E. coli lysogenic with Shiga toxin-converting phages may gain from production of Shiga toxins coupled with prophage induction and subsequent cell death. (A) A protozoan predator (exemplified by Tetrahymena) releases hydrogen peroxide to damage bacterial cells. (B) In the case of STEC, hydrogen peroxide causes induction of Shiga toxin-converting prophage in a small fraction of bacterial cells, which is, nevertheless, sufficient to produce Shiga toxins (Stx) in amounts enough to kill the predator. (C) Neutrophils employ a strategy similar to that used by protozoan predators if human intestine is infected with bacteria recognized as aliens. (D) The response of STEC to neutrophils' attack is analogous to that employed by this bacterium to faith against unicellular eukaryotic predators. The original hypothesis was presented in two articles (Łoś et al., 2011; Mauro and Koudelka, 2011).

Mentions: The results summarized in the preceding subsection suggest that production of hydrogen peroxide by eukaryotic unicellular predators, like Tetrahymena, may induce Shiga toxin-converting prophages in STEC, resulting in production and release of Shiga toxin. These data provided a basis for the hypothesis that under such conditions, the predator would be killed, which might be beneficial for the bacteria (Łoś et al., 2011; Mauro and Koudelka, 2011). If we consider that infection of humans by STEC is coincidental, one might ask why these bacteria produce Shiga toxins in the intestine? As suggested by the authors of this bacterial “altruism” hypothesis, the occurrence of hydrogen peroxide in the human intestine during infection is possible since human neutrophils may produce H2O2 in response to STEC (Wagner et al., 2001b), a strategy similar to that used by Tetrahymena to hunt bacteria. Moreover, it was demonstrated that bacteria present in the human intestine can cause the generation of reactive oxygen species (Kumar et al., 2007). Therefore, the hypothesis can be presented schematically as shown in Figure 1. However, since prophage induction leads to lytic development and killing of the host cell, the problem with the hypothesis is that it is difficult to imagine how already dead bacteria may benefit from killing a predator or neutrophils (or other human cells). Therefore, the bacterial “altruism” hypothesis presented here (Figure 1) requires that prophage induction only occur in a small fraction of the STEC population. So, what is the experimental evidence rejecting or supporting this model?


Altruism of Shiga toxin-producing Escherichia coli: recent hypothesis versus experimental results.

Loś JM, Loś M, Węgrzyn A, Węgrzyn G - Front Cell Infect Microbiol (2013)

The model of STEC altruism, representing the hypothesis on the benefit which E. coli lysogenic with Shiga toxin-converting phages may gain from production of Shiga toxins coupled with prophage induction and subsequent cell death. (A) A protozoan predator (exemplified by Tetrahymena) releases hydrogen peroxide to damage bacterial cells. (B) In the case of STEC, hydrogen peroxide causes induction of Shiga toxin-converting prophage in a small fraction of bacterial cells, which is, nevertheless, sufficient to produce Shiga toxins (Stx) in amounts enough to kill the predator. (C) Neutrophils employ a strategy similar to that used by protozoan predators if human intestine is infected with bacteria recognized as aliens. (D) The response of STEC to neutrophils' attack is analogous to that employed by this bacterium to faith against unicellular eukaryotic predators. The original hypothesis was presented in two articles (Łoś et al., 2011; Mauro and Koudelka, 2011).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3539655&req=5

Figure 1: The model of STEC altruism, representing the hypothesis on the benefit which E. coli lysogenic with Shiga toxin-converting phages may gain from production of Shiga toxins coupled with prophage induction and subsequent cell death. (A) A protozoan predator (exemplified by Tetrahymena) releases hydrogen peroxide to damage bacterial cells. (B) In the case of STEC, hydrogen peroxide causes induction of Shiga toxin-converting prophage in a small fraction of bacterial cells, which is, nevertheless, sufficient to produce Shiga toxins (Stx) in amounts enough to kill the predator. (C) Neutrophils employ a strategy similar to that used by protozoan predators if human intestine is infected with bacteria recognized as aliens. (D) The response of STEC to neutrophils' attack is analogous to that employed by this bacterium to faith against unicellular eukaryotic predators. The original hypothesis was presented in two articles (Łoś et al., 2011; Mauro and Koudelka, 2011).
Mentions: The results summarized in the preceding subsection suggest that production of hydrogen peroxide by eukaryotic unicellular predators, like Tetrahymena, may induce Shiga toxin-converting prophages in STEC, resulting in production and release of Shiga toxin. These data provided a basis for the hypothesis that under such conditions, the predator would be killed, which might be beneficial for the bacteria (Łoś et al., 2011; Mauro and Koudelka, 2011). If we consider that infection of humans by STEC is coincidental, one might ask why these bacteria produce Shiga toxins in the intestine? As suggested by the authors of this bacterial “altruism” hypothesis, the occurrence of hydrogen peroxide in the human intestine during infection is possible since human neutrophils may produce H2O2 in response to STEC (Wagner et al., 2001b), a strategy similar to that used by Tetrahymena to hunt bacteria. Moreover, it was demonstrated that bacteria present in the human intestine can cause the generation of reactive oxygen species (Kumar et al., 2007). Therefore, the hypothesis can be presented schematically as shown in Figure 1. However, since prophage induction leads to lytic development and killing of the host cell, the problem with the hypothesis is that it is difficult to imagine how already dead bacteria may benefit from killing a predator or neutrophils (or other human cells). Therefore, the bacterial “altruism” hypothesis presented here (Figure 1) requires that prophage induction only occur in a small fraction of the STEC population. So, what is the experimental evidence rejecting or supporting this model?

Bottom Line: Shiga toxin-producing Escherichia coli (STEC) may cause bloody diarrhea and hemorrhagic colitis (HC), with subsequent systemic disease.Recently, a hypothesis was proposed (simultaneously but independently by two research groups) that STEC may benefit from Shiga toxin production as a result of toxin-dependent killing of eukaryotic cells such as unicellular predators or human leukocytes.On the other hand, analysis of recently published results, discussed here, indicated that the efficiency of prophage excision under conditions that may likely occur in the natural habitat of STEC is sufficiently low to ensure survival of a large fraction of the bacterial host.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Genetics, Department of Molecular Biology, University of Gdańsk Gdańsk, Poland.

ABSTRACT
Shiga toxin-producing Escherichia coli (STEC) may cause bloody diarrhea and hemorrhagic colitis (HC), with subsequent systemic disease. Since genes coding for Shiga toxins (stx genes) are located on lambdoid prophages, their effective production occurs only after prophage induction. Such induction and subsequent lytic development of Shiga toxin-converting bacteriophages results not only in production of toxic proteins, but also in the lysis (and thus, the death) of the host cell. Therefore, one may ask the question: what is the benefit for bacteria to produce the toxin if they die due to phage production and subsequent cell lysis? Recently, a hypothesis was proposed (simultaneously but independently by two research groups) that STEC may benefit from Shiga toxin production as a result of toxin-dependent killing of eukaryotic cells such as unicellular predators or human leukocytes. This hypothesis could make sense only if we assume that prophage induction (and production of the toxin) occurs only in a small fraction of bacterial cells, thus, a few members of the population are sacrificed for the benefit of the rest, providing an example of "bacterial altruism." However, various reports indicating that the frequency of spontaneous induction of Shiga toxin-converting prophages is higher than that of other lambdoid prophages might seem to contradict the for-mentioned model. On the other hand, analysis of recently published results, discussed here, indicated that the efficiency of prophage excision under conditions that may likely occur in the natural habitat of STEC is sufficiently low to ensure survival of a large fraction of the bacterial host. A molecular mechanism by which partial prophage induction may occur is proposed. We conclude that the published data supports the proposed model of bacterial "altruism" where prophage induction occurs at a low enough frequency to render toxin production a positive selective force on the general STEC population.

Show MeSH
Related in: MedlinePlus