Fructose-Asparagine Is a Primary Nutrient during Growth of Salmonella in the Inflamed Intestine

Mohamed M. Ali, David L. Newsom, Juan F. González, Anice Sabag-Daigle, Christopher Stahl, Brandi Steidley, Judith Dubena, Jessica L. Dyszel, Jenee N. Smith, Yakhya Dieye, Razvan Arsenescu, Prosper N. Boyaka, Steven Krakowka, Tony Romeo, Edward J. Behrman, Peter White, Brian M.M. Ahmer

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

Salmonella enterica serovar Typhimurium (Salmonella) is one of the most significant food-borne pathogens affecting both humans and agriculture. We have determined that Salmonella encodes an uptake and utilization pathway specific for a novel nutrient, fructose-asparagine (F-Asn), which is essential for Salmonella fitness in the inflamed intestine (modeled using germ-free, streptomycin-treated, ex-germ-free with human microbiota, and IL10-/- mice). The locus encoding F-Asn utilization, fra, provides an advantage only if Salmonella can initiate inflammation and use tetrathionate as a terminal electron acceptor for anaerobic respiration (the fra phenotype is lost in Salmonella SPI1- SPI2- or ttrA mutants, respectively). The severe fitness defect of a Salmonella fra mutant suggests that F-Asn is the primary nutrient utilized by Salmonella in the inflamed intestine and that this system provides a valuable target for novel therapies.

Original languageEnglish (US)
Article numbere1004209
JournalPLoS Pathogens
Volume10
Issue number6
DOIs
StatePublished - Jan 1 2014

Fingerprint

Asparagine
Fructose
Salmonella
Intestines
Food
Growth
Salmonella enterica
Microbiota
Streptomycin
Salmonella typhimurium
Agriculture
Interleukin-10
Respiration
Electrons
Inflammation
Phenotype

All Science Journal Classification (ASJC) codes

  • Parasitology
  • Microbiology
  • Immunology
  • Molecular Biology
  • Genetics
  • Virology

Cite this

Ali, M. M., Newsom, D. L., González, J. F., Sabag-Daigle, A., Stahl, C., Steidley, B., ... Ahmer, B. M. M. (2014). Fructose-Asparagine Is a Primary Nutrient during Growth of Salmonella in the Inflamed Intestine. PLoS Pathogens, 10(6), [e1004209]. https://doi.org/10.1371/journal.ppat.1004209
Ali, Mohamed M. ; Newsom, David L. ; González, Juan F. ; Sabag-Daigle, Anice ; Stahl, Christopher ; Steidley, Brandi ; Dubena, Judith ; Dyszel, Jessica L. ; Smith, Jenee N. ; Dieye, Yakhya ; Arsenescu, Razvan ; Boyaka, Prosper N. ; Krakowka, Steven ; Romeo, Tony ; Behrman, Edward J. ; White, Peter ; Ahmer, Brian M.M. / Fructose-Asparagine Is a Primary Nutrient during Growth of Salmonella in the Inflamed Intestine. In: PLoS Pathogens. 2014 ; Vol. 10, No. 6.
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abstract = "Salmonella enterica serovar Typhimurium (Salmonella) is one of the most significant food-borne pathogens affecting both humans and agriculture. We have determined that Salmonella encodes an uptake and utilization pathway specific for a novel nutrient, fructose-asparagine (F-Asn), which is essential for Salmonella fitness in the inflamed intestine (modeled using germ-free, streptomycin-treated, ex-germ-free with human microbiota, and IL10-/- mice). The locus encoding F-Asn utilization, fra, provides an advantage only if Salmonella can initiate inflammation and use tetrathionate as a terminal electron acceptor for anaerobic respiration (the fra phenotype is lost in Salmonella SPI1- SPI2- or ttrA mutants, respectively). The severe fitness defect of a Salmonella fra mutant suggests that F-Asn is the primary nutrient utilized by Salmonella in the inflamed intestine and that this system provides a valuable target for novel therapies.",
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Ali, MM, Newsom, DL, González, JF, Sabag-Daigle, A, Stahl, C, Steidley, B, Dubena, J, Dyszel, JL, Smith, JN, Dieye, Y, Arsenescu, R, Boyaka, PN, Krakowka, S, Romeo, T, Behrman, EJ, White, P & Ahmer, BMM 2014, 'Fructose-Asparagine Is a Primary Nutrient during Growth of Salmonella in the Inflamed Intestine', PLoS Pathogens, vol. 10, no. 6, e1004209. https://doi.org/10.1371/journal.ppat.1004209

Fructose-Asparagine Is a Primary Nutrient during Growth of Salmonella in the Inflamed Intestine. / Ali, Mohamed M.; Newsom, David L.; González, Juan F.; Sabag-Daigle, Anice; Stahl, Christopher; Steidley, Brandi; Dubena, Judith; Dyszel, Jessica L.; Smith, Jenee N.; Dieye, Yakhya; Arsenescu, Razvan; Boyaka, Prosper N.; Krakowka, Steven; Romeo, Tony; Behrman, Edward J.; White, Peter; Ahmer, Brian M.M.

In: PLoS Pathogens, Vol. 10, No. 6, e1004209, 01.01.2014.

Research output: Contribution to journalArticle

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T1 - Fructose-Asparagine Is a Primary Nutrient during Growth of Salmonella in the Inflamed Intestine

AU - Ali, Mohamed M.

AU - Newsom, David L.

AU - González, Juan F.

AU - Sabag-Daigle, Anice

AU - Stahl, Christopher

AU - Steidley, Brandi

AU - Dubena, Judith

AU - Dyszel, Jessica L.

AU - Smith, Jenee N.

AU - Dieye, Yakhya

AU - Arsenescu, Razvan

AU - Boyaka, Prosper N.

AU - Krakowka, Steven

AU - Romeo, Tony

AU - Behrman, Edward J.

AU - White, Peter

AU - Ahmer, Brian M.M.

PY - 2014/1/1

Y1 - 2014/1/1

N2 - Salmonella enterica serovar Typhimurium (Salmonella) is one of the most significant food-borne pathogens affecting both humans and agriculture. We have determined that Salmonella encodes an uptake and utilization pathway specific for a novel nutrient, fructose-asparagine (F-Asn), which is essential for Salmonella fitness in the inflamed intestine (modeled using germ-free, streptomycin-treated, ex-germ-free with human microbiota, and IL10-/- mice). The locus encoding F-Asn utilization, fra, provides an advantage only if Salmonella can initiate inflammation and use tetrathionate as a terminal electron acceptor for anaerobic respiration (the fra phenotype is lost in Salmonella SPI1- SPI2- or ttrA mutants, respectively). The severe fitness defect of a Salmonella fra mutant suggests that F-Asn is the primary nutrient utilized by Salmonella in the inflamed intestine and that this system provides a valuable target for novel therapies.

AB - Salmonella enterica serovar Typhimurium (Salmonella) is one of the most significant food-borne pathogens affecting both humans and agriculture. We have determined that Salmonella encodes an uptake and utilization pathway specific for a novel nutrient, fructose-asparagine (F-Asn), which is essential for Salmonella fitness in the inflamed intestine (modeled using germ-free, streptomycin-treated, ex-germ-free with human microbiota, and IL10-/- mice). The locus encoding F-Asn utilization, fra, provides an advantage only if Salmonella can initiate inflammation and use tetrathionate as a terminal electron acceptor for anaerobic respiration (the fra phenotype is lost in Salmonella SPI1- SPI2- or ttrA mutants, respectively). The severe fitness defect of a Salmonella fra mutant suggests that F-Asn is the primary nutrient utilized by Salmonella in the inflamed intestine and that this system provides a valuable target for novel therapies.

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Ali MM, Newsom DL, González JF, Sabag-Daigle A, Stahl C, Steidley B et al. Fructose-Asparagine Is a Primary Nutrient during Growth of Salmonella in the Inflamed Intestine. PLoS Pathogens. 2014 Jan 1;10(6). e1004209. https://doi.org/10.1371/journal.ppat.1004209