Loss of Multicellular Behavior in Epidemic African Nontyphoidal <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium ST313 Strain D23580

ABSTRACT Nontyphoidal Salmonella enterica serovar Typhimurium is a frequent cause of bloodstream infections in children and HIV-infected adults in sub-Saharan Africa. Most isolates from African patients with bacteremia belong to a single sequence type, ST313, which is genetically distinct from gastr...

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Autores principales:	Larissa A. Singletary, Joyce E. Karlinsey, Stephen J. Libby, Jason P. Mooney, Kristen L. Lokken, Renée M. Tsolis, Mariana X. Byndloss, Lauren A. Hirao, Christopher A. Gaulke, Robert W. Crawford, Satya Dandekar, Robert A. Kingsley, Chisomo L. Msefula, Robert S. Heyderman, Ferric C. Fang
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/18c0318f4ce24989a9672270a4aff640
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spelling	oai:doaj.org-article:18c0318f4ce24989a9672270a4aff6402021-11-15T15:41:42ZLoss of Multicellular Behavior in Epidemic African Nontyphoidal <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium ST313 Strain D2358010.1128/mBio.02265-152150-7511https://doaj.org/article/18c0318f4ce24989a9672270a4aff6402016-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02265-15https://doaj.org/toc/2150-7511ABSTRACT Nontyphoidal Salmonella enterica serovar Typhimurium is a frequent cause of bloodstream infections in children and HIV-infected adults in sub-Saharan Africa. Most isolates from African patients with bacteremia belong to a single sequence type, ST313, which is genetically distinct from gastroenteritis-associated ST19 strains, such as 14028s and SL1344. Some studies suggest that the rapid spread of ST313 across sub-Saharan Africa has been facilitated by anthroponotic (person-to-person) transmission, eliminating the need for Salmonella survival outside the host. While these studies have not ruled out zoonotic or other means of transmission, the anthroponotic hypothesis is supported by evidence of extensive genomic decay, a hallmark of host adaptation, in the sequenced ST313 strain D23580. We have identified and demonstrated 2 loss-of-function mutations in D23580, not present in the ST19 strain 14028s, that impair multicellular stress resistance associated with survival outside the host. These mutations result in inactivation of the KatE stationary-phase catalase that protects high-density bacterial communities from oxidative stress and the BcsG cellulose biosynthetic enzyme required for the RDAR (red, dry, and rough) colonial phenotype. However, we found that like 14028s, D23580 is able to elicit an acute inflammatory response and cause enteritis in mice and rhesus macaque monkeys. Collectively, these observations suggest that African S. Typhimurium ST313 strain D23580 is becoming adapted to an anthroponotic mode of transmission while retaining the ability to infect and cause enteritis in multiple host species. IMPORTANCE The last 3 decades have witnessed an epidemic of invasive nontyphoidal Salmonella infections in sub-Saharan Africa. Genomic analysis and clinical observations suggest that the Salmonella strains responsible for these infections are evolving to become more typhoid-like with regard to patterns of transmission and virulence. This study shows that a prototypical African nontyphoidal Salmonella strain has lost traits required for environmental stress resistance, consistent with an adaptation to a human-to-human mode of transmission. However, in contrast to predictions, the strain remains capable of causing acute inflammation in the mammalian intestine. This suggests that the systemic clinical presentation of invasive nontyphoidal Salmonella infections in Africa reflects the immune status of infected hosts rather than intrinsic differences in the virulence of African Salmonella strains. Our study provides important new insights into the evolution of host adaptation in bacterial pathogens.Larissa A. SingletaryJoyce E. KarlinseyStephen J. LibbyJason P. MooneyKristen L. LokkenRenée M. TsolisMariana X. ByndlossLauren A. HiraoChristopher A. GaulkeRobert W. CrawfordSatya DandekarRobert A. KingsleyChisomo L. MsefulaRobert S. HeydermanFerric C. FangAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 2 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Larissa A. Singletary Joyce E. Karlinsey Stephen J. Libby Jason P. Mooney Kristen L. Lokken Renée M. Tsolis Mariana X. Byndloss Lauren A. Hirao Christopher A. Gaulke Robert W. Crawford Satya Dandekar Robert A. Kingsley Chisomo L. Msefula Robert S. Heyderman Ferric C. Fang Loss of Multicellular Behavior in Epidemic African Nontyphoidal <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium ST313 Strain D23580
description	ABSTRACT Nontyphoidal Salmonella enterica serovar Typhimurium is a frequent cause of bloodstream infections in children and HIV-infected adults in sub-Saharan Africa. Most isolates from African patients with bacteremia belong to a single sequence type, ST313, which is genetically distinct from gastroenteritis-associated ST19 strains, such as 14028s and SL1344. Some studies suggest that the rapid spread of ST313 across sub-Saharan Africa has been facilitated by anthroponotic (person-to-person) transmission, eliminating the need for Salmonella survival outside the host. While these studies have not ruled out zoonotic or other means of transmission, the anthroponotic hypothesis is supported by evidence of extensive genomic decay, a hallmark of host adaptation, in the sequenced ST313 strain D23580. We have identified and demonstrated 2 loss-of-function mutations in D23580, not present in the ST19 strain 14028s, that impair multicellular stress resistance associated with survival outside the host. These mutations result in inactivation of the KatE stationary-phase catalase that protects high-density bacterial communities from oxidative stress and the BcsG cellulose biosynthetic enzyme required for the RDAR (red, dry, and rough) colonial phenotype. However, we found that like 14028s, D23580 is able to elicit an acute inflammatory response and cause enteritis in mice and rhesus macaque monkeys. Collectively, these observations suggest that African S. Typhimurium ST313 strain D23580 is becoming adapted to an anthroponotic mode of transmission while retaining the ability to infect and cause enteritis in multiple host species. IMPORTANCE The last 3 decades have witnessed an epidemic of invasive nontyphoidal Salmonella infections in sub-Saharan Africa. Genomic analysis and clinical observations suggest that the Salmonella strains responsible for these infections are evolving to become more typhoid-like with regard to patterns of transmission and virulence. This study shows that a prototypical African nontyphoidal Salmonella strain has lost traits required for environmental stress resistance, consistent with an adaptation to a human-to-human mode of transmission. However, in contrast to predictions, the strain remains capable of causing acute inflammation in the mammalian intestine. This suggests that the systemic clinical presentation of invasive nontyphoidal Salmonella infections in Africa reflects the immune status of infected hosts rather than intrinsic differences in the virulence of African Salmonella strains. Our study provides important new insights into the evolution of host adaptation in bacterial pathogens.
format	article
author	Larissa A. Singletary Joyce E. Karlinsey Stephen J. Libby Jason P. Mooney Kristen L. Lokken Renée M. Tsolis Mariana X. Byndloss Lauren A. Hirao Christopher A. Gaulke Robert W. Crawford Satya Dandekar Robert A. Kingsley Chisomo L. Msefula Robert S. Heyderman Ferric C. Fang
author_facet	Larissa A. Singletary Joyce E. Karlinsey Stephen J. Libby Jason P. Mooney Kristen L. Lokken Renée M. Tsolis Mariana X. Byndloss Lauren A. Hirao Christopher A. Gaulke Robert W. Crawford Satya Dandekar Robert A. Kingsley Chisomo L. Msefula Robert S. Heyderman Ferric C. Fang
author_sort	Larissa A. Singletary
title	Loss of Multicellular Behavior in Epidemic African Nontyphoidal <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium ST313 Strain D23580
title_short	Loss of Multicellular Behavior in Epidemic African Nontyphoidal <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium ST313 Strain D23580
title_full	Loss of Multicellular Behavior in Epidemic African Nontyphoidal <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium ST313 Strain D23580
title_fullStr	Loss of Multicellular Behavior in Epidemic African Nontyphoidal <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium ST313 Strain D23580
title_full_unstemmed	Loss of Multicellular Behavior in Epidemic African Nontyphoidal <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium ST313 Strain D23580
title_sort	loss of multicellular behavior in epidemic african nontyphoidal <named-content content-type="genus-species">salmonella enterica</named-content> serovar typhimurium st313 strain d23580
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/18c0318f4ce24989a9672270a4aff640
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Loss of Multicellular Behavior in Epidemic African Nontyphoidal <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium ST313 Strain D23580

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