Glucose Signaling Is Important for Nutrient Adaptation during Differentiation of Pleomorphic African Trypanosomes

ABSTRACT The African trypanosome has evolved mechanisms to adapt to changes in nutrient availability that occur during its life cycle. During transition from mammalian blood to insect vector gut, parasites experience a rapid reduction in environmental glucose. Here we describe how pleomorphic parasi...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Yijian Qiu, Jillian E. Milanes, Jessica A. Jones, Rooksana E. Noorai, Vijay Shankar, James C. Morris
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Trypanosoma carbon metabolism glucose sensing Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d57ad760a6a54dfe8ae2289b3c146b36
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:d57ad760a6a54dfe8ae2289b3c146b36
record_format	dspace
spelling	oai:doaj.org-article:d57ad760a6a54dfe8ae2289b3c146b362021-11-15T15:22:26ZGlucose Signaling Is Important for Nutrient Adaptation during Differentiation of Pleomorphic African Trypanosomes10.1128/mSphere.00366-182379-5042https://doaj.org/article/d57ad760a6a54dfe8ae2289b3c146b362018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00366-18https://doaj.org/toc/2379-5042ABSTRACT The African trypanosome has evolved mechanisms to adapt to changes in nutrient availability that occur during its life cycle. During transition from mammalian blood to insect vector gut, parasites experience a rapid reduction in environmental glucose. Here we describe how pleomorphic parasites respond to glucose depletion with a focus on parasite changes in energy metabolism and growth. Long slender bloodstream form parasites were rapidly killed as glucose concentrations fell, while short stumpy bloodstream form parasites persisted to differentiate into the insect-stage procyclic form parasite. The rate of differentiation was lower than that triggered by other cues but reached physiological rates when combined with cold shock. Both differentiation and growth of resulting procyclic form parasites were inhibited by glucose and nonmetabolizable glucose analogs, and these parasites were found to have upregulated amino acid metabolic pathway component gene expression. In summary, glucose transitions from the primary metabolite of the blood-stage infection to a negative regulator of cell development and growth in the insect vector, suggesting that the hexose is not only a key metabolic agent but also an important signaling molecule. IMPORTANCE As the African trypanosome Trypanosoma brucei completes its life cycle, it encounters many different environments. Adaptation to these environments includes modulation of metabolic pathways to parallel the availability of nutrients. Here, we describe how the blood-dwelling life cycle stages of the African trypanosome, which consume glucose to meet their nutritional needs, respond differently to culture in the near absence of glucose. The proliferative long slender parasites rapidly die, while the nondividing short stumpy parasite remains viable and undergoes differentiation to the next life cycle stage, the procyclic form parasite. Interestingly, a sugar analog that cannot be used as an energy source inhibited the process. Furthermore, the growth of procyclic form parasite that resulted from the event was inhibited by glucose, a behavior that is similar to that of parasites isolated from tsetse flies. Our findings suggest that glucose sensing serves as an important modulator of nutrient adaptation in the parasite.Yijian QiuJillian E. MilanesJessica A. JonesRooksana E. NooraiVijay ShankarJames C. MorrisAmerican Society for MicrobiologyarticleTrypanosomacarbon metabolismglucose sensingMicrobiologyQR1-502ENmSphere, Vol 3, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Trypanosoma carbon metabolism glucose sensing Microbiology QR1-502
spellingShingle	Trypanosoma carbon metabolism glucose sensing Microbiology QR1-502 Yijian Qiu Jillian E. Milanes Jessica A. Jones Rooksana E. Noorai Vijay Shankar James C. Morris Glucose Signaling Is Important for Nutrient Adaptation during Differentiation of Pleomorphic African Trypanosomes
description	ABSTRACT The African trypanosome has evolved mechanisms to adapt to changes in nutrient availability that occur during its life cycle. During transition from mammalian blood to insect vector gut, parasites experience a rapid reduction in environmental glucose. Here we describe how pleomorphic parasites respond to glucose depletion with a focus on parasite changes in energy metabolism and growth. Long slender bloodstream form parasites were rapidly killed as glucose concentrations fell, while short stumpy bloodstream form parasites persisted to differentiate into the insect-stage procyclic form parasite. The rate of differentiation was lower than that triggered by other cues but reached physiological rates when combined with cold shock. Both differentiation and growth of resulting procyclic form parasites were inhibited by glucose and nonmetabolizable glucose analogs, and these parasites were found to have upregulated amino acid metabolic pathway component gene expression. In summary, glucose transitions from the primary metabolite of the blood-stage infection to a negative regulator of cell development and growth in the insect vector, suggesting that the hexose is not only a key metabolic agent but also an important signaling molecule. IMPORTANCE As the African trypanosome Trypanosoma brucei completes its life cycle, it encounters many different environments. Adaptation to these environments includes modulation of metabolic pathways to parallel the availability of nutrients. Here, we describe how the blood-dwelling life cycle stages of the African trypanosome, which consume glucose to meet their nutritional needs, respond differently to culture in the near absence of glucose. The proliferative long slender parasites rapidly die, while the nondividing short stumpy parasite remains viable and undergoes differentiation to the next life cycle stage, the procyclic form parasite. Interestingly, a sugar analog that cannot be used as an energy source inhibited the process. Furthermore, the growth of procyclic form parasite that resulted from the event was inhibited by glucose, a behavior that is similar to that of parasites isolated from tsetse flies. Our findings suggest that glucose sensing serves as an important modulator of nutrient adaptation in the parasite.
format	article
author	Yijian Qiu Jillian E. Milanes Jessica A. Jones Rooksana E. Noorai Vijay Shankar James C. Morris
author_facet	Yijian Qiu Jillian E. Milanes Jessica A. Jones Rooksana E. Noorai Vijay Shankar James C. Morris
author_sort	Yijian Qiu
title	Glucose Signaling Is Important for Nutrient Adaptation during Differentiation of Pleomorphic African Trypanosomes
title_short	Glucose Signaling Is Important for Nutrient Adaptation during Differentiation of Pleomorphic African Trypanosomes
title_full	Glucose Signaling Is Important for Nutrient Adaptation during Differentiation of Pleomorphic African Trypanosomes
title_fullStr	Glucose Signaling Is Important for Nutrient Adaptation during Differentiation of Pleomorphic African Trypanosomes
title_full_unstemmed	Glucose Signaling Is Important for Nutrient Adaptation during Differentiation of Pleomorphic African Trypanosomes
title_sort	glucose signaling is important for nutrient adaptation during differentiation of pleomorphic african trypanosomes
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/d57ad760a6a54dfe8ae2289b3c146b36
work_keys_str_mv	AT yijianqiu glucosesignalingisimportantfornutrientadaptationduringdifferentiationofpleomorphicafricantrypanosomes AT jillianemilanes glucosesignalingisimportantfornutrientadaptationduringdifferentiationofpleomorphicafricantrypanosomes AT jessicaajones glucosesignalingisimportantfornutrientadaptationduringdifferentiationofpleomorphicafricantrypanosomes AT rooksanaenoorai glucosesignalingisimportantfornutrientadaptationduringdifferentiationofpleomorphicafricantrypanosomes AT vijayshankar glucosesignalingisimportantfornutrientadaptationduringdifferentiationofpleomorphicafricantrypanosomes AT jamescmorris glucosesignalingisimportantfornutrientadaptationduringdifferentiationofpleomorphicafricantrypanosomes
_version_	1718428037143330816

Glucose Signaling Is Important for Nutrient Adaptation during Differentiation of Pleomorphic African Trypanosomes

Ejemplares similares