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Enteric Pathogens Exploit the Microbiota-generated Nutritional Environment of the Gut

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  • Authors: Alline R. Pacheco1, Vanessa Sperandio2
  • Editors: Tyrrell Conway3, Paul Cohen4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: University of Texas Southwestern Medical Center, Dept. of Microbiology; 2: University of Texas Southwestern Medical Center, Dept. of Microbiology; 3: Oklahoma State University, Stillwater, OK; 4: University of Rhode Island, Kingston, RI
    • Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.MBP-0001-2014
  • Received 27 May 2014 Accepted 12 June 2014 Published 11 June 2015
  • Vanessa Sperandio, [email protected]
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  • Abstract:

    Host bacterial associations have a profound impact on health and disease. The human gastrointestinal (GI) tract is inhabited by trillions of commensal bacteria that aid in the digestion of food and vitamin production and play crucial roles in human physiology. Disruption of these relationships and the structure of the bacterial communities that inhabit the gut can contribute to dysbiosis, leading to disease. This fundamental relationship between the host and microbiota relies on chemical signaling and nutrient availability and exchange. GI pathogens compete with the endogenous microbiota for a colonization niche ( 1 , 2 ). The ability to monitor nutrients and combine this information with the host physiological state is important for the pathogen to precisely program the expression of its virulence repertoire. A major nutrient source is carbon, and although the impact of carbon nutrition on the colonization of the gut by the microbiota has been extensively studied, the extent to which carbon sources affect the regulation of virulence factors by invading pathogens has not been fully defined. The GI pathogen enterohemorrhagic (EHEC) gages sugar sources as an important cue to regulate expression of its virulence genes. EHEC senses whether it is in a gluconeogenic versus a glycolytic environment, as well as fluctuations of fucose levels to fine tune regulation of its virulence repertoire.

  • Citation: Pacheco A, Sperandio V. 2015. Enteric Pathogens Exploit the Microbiota-generated Nutritional Environment of the Gut. Microbiol Spectrum 3(3):MBP-0001-2014. doi:10.1128/microbiolspec.MBP-0001-2014.

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/content/journal/microbiolspec/10.1128/microbiolspec.MBP-0001-2014
2015-06-11
2021-03-01

Abstract:

Host bacterial associations have a profound impact on health and disease. The human gastrointestinal (GI) tract is inhabited by trillions of commensal bacteria that aid in the digestion of food and vitamin production and play crucial roles in human physiology. Disruption of these relationships and the structure of the bacterial communities that inhabit the gut can contribute to dysbiosis, leading to disease. This fundamental relationship between the host and microbiota relies on chemical signaling and nutrient availability and exchange. GI pathogens compete with the endogenous microbiota for a colonization niche ( 1 , 2 ). The ability to monitor nutrients and combine this information with the host physiological state is important for the pathogen to precisely program the expression of its virulence repertoire. A major nutrient source is carbon, and although the impact of carbon nutrition on the colonization of the gut by the microbiota has been extensively studied, the extent to which carbon sources affect the regulation of virulence factors by invading pathogens has not been fully defined. The GI pathogen enterohemorrhagic (EHEC) gages sugar sources as an important cue to regulate expression of its virulence genes. EHEC senses whether it is in a gluconeogenic versus a glycolytic environment, as well as fluctuations of fucose levels to fine tune regulation of its virulence repertoire.

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Enteric Pathogens Exploit the Microbiota-generated Nutritional Environment of the Gut
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Citation: Pacheco A, Sperandio V. 2015. Enteric pathogens exploit the microbiota-generated nutritional environment of the gut. microbiolspec 3(3): doi:10.1128/microbiolspec.MBP-0001-2014
/content/microbiolspec/10.1128/microbiolspec.MBP-0001-2014.fig1
FIGURE 1
Nutritional cues regulate the locus of enterocyte effacement (LEE) gene expression in enterohemorrhagic (EHEC). Glycophagic members of the microbiota such as make fucose from mucin accessible to EHEC, and EHEC interprets this information to recognize that it is in the lumen, where expression of its LEE-encoded type III secretion system (TTSS) is onerous and not advantageous. Using yet another nutrient-based environmental cue, EHEC also times LEE expression through recognition of glycolytic and gluconeogenic environments. The lumen is more glycolytic due to predominant glycophagic members of the microbiota degrading complex polysaccharides into monosaccharides that can be readily utilized by nonglycophagic bacterial species such as and . In contrast, the tight mucus layer between the lumen and the epithelial interface in the gastrointestinal (GI) tract is devoid of microbiota; it is known as a “zone of clearance.” At the epithelial interface, the environment is regarded as gluconeogenic. Hence, the coupling of LEE regulation to optimal expression under gluconeogenic and low-fucose conditions mirrors the interface with the epithelial layer environment in the GI tract, ensuring that EHEC will express only LEE at optimal levels to promote attaching and effacing lesion formation at the epithelial interface.
microbiolspec/3/3/MBP-0001-2014-fig1_thmb.gif
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FIGURE 1

Nutritional cues regulate the locus of enterocyte effacement (LEE) gene expression in enterohemorrhagic (EHEC). Glycophagic members of the microbiota such as make fucose from mucin accessible to EHEC, and EHEC interprets this information to recognize that it is in the lumen, where expression of its LEE-encoded type III secretion system (TTSS) is onerous and not advantageous. Using yet another nutrient-based environmental cue, EHEC also times LEE expression through recognition of glycolytic and gluconeogenic environments. The lumen is more glycolytic due to predominant glycophagic members of the microbiota degrading complex polysaccharides into monosaccharides that can be readily utilized by nonglycophagic bacterial species such as and . In contrast, the tight mucus layer between the lumen and the epithelial interface in the gastrointestinal (GI) tract is devoid of microbiota; it is known as a “zone of clearance.” At the epithelial interface, the environment is regarded as gluconeogenic. Hence, the coupling of LEE regulation to optimal expression under gluconeogenic and low-fucose conditions mirrors the interface with the epithelial layer environment in the GI tract, ensuring that EHEC will express only LEE at optimal levels to promote attaching and effacing lesion formation at the epithelial interface.

Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.MBP-0001-2014
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