A Tale of Three Species: Adaptation of <named-content content-type="genus-species">Sodalis glossinidius</named-content> to Tsetse Biology, <italic toggle="yes">Wigglesworthia</italic> Metabolism, and Host Diet

ABSTRACT The tsetse fly is the insect vector for the Trypanosoma brucei parasite, the causative agent of human African trypanosomiasis. The colonization and spread of the trypanosome correlate positively with the presence of a secondary symbiotic bacterium, Sodalis glossinidius. The metabolic requir...

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Autores principales:	Rebecca J. Hall, Lindsey A. Flanagan, Michael J. Bottery, Vicki Springthorpe, Stephen Thorpe, Alistair C. Darby, A. Jamie Wood, Gavin H. Thomas
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	metabolism microbiome physiology symbiosis vector biology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c0668f1dd80e47818646dc391404b3f5
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spelling	oai:doaj.org-article:c0668f1dd80e47818646dc391404b3f52021-11-15T15:55:14ZA Tale of Three Species: Adaptation of <named-content content-type="genus-species">Sodalis glossinidius</named-content> to Tsetse Biology, <italic toggle="yes">Wigglesworthia</italic> Metabolism, and Host Diet10.1128/mBio.02106-182150-7511https://doaj.org/article/c0668f1dd80e47818646dc391404b3f52019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02106-18https://doaj.org/toc/2150-7511ABSTRACT The tsetse fly is the insect vector for the Trypanosoma brucei parasite, the causative agent of human African trypanosomiasis. The colonization and spread of the trypanosome correlate positively with the presence of a secondary symbiotic bacterium, Sodalis glossinidius. The metabolic requirements and interactions of the bacterium with its host are poorly understood, and herein we describe a metabolic model of S. glossinidius metabolism. The model enabled the design and experimental verification of a defined medium that supports S. glossinidius growth ex vivo. This has been used subsequently to analyze in vitro aspects of S. glossinidius metabolism, revealing multiple unique adaptations of the symbiont to its environment. Continued dependence on a sugar, and the importance of the chitin monomer N-acetyl-d-glucosamine as a carbon and energy source, suggests adaptation to host-derived molecules. Adaptation to the amino acid-rich blood diet is revealed by a strong dependence on l-glutamate as a source of carbon and nitrogen and by the ability to rescue a predicted l-arginine auxotrophy. Finally, the selective loss of thiamine biosynthesis, a vitamin provided to the host by the primary symbiont Wigglesworthia glossinidia, reveals an intersymbiont dependence. The reductive evolution of S. glossinidius to exploit environmentally derived metabolites has resulted in multiple weaknesses in the metabolic network. These weaknesses may become targets for reagents that inhibit S. glossinidius growth and aid the reduction of trypanosomal transmission. IMPORTANCE Human African trypanosomiasis is caused by the Trypanosoma brucei parasite. The tsetse fly vector is of interest for its potential to prevent disease spread, as it is essential for T. brucei life cycle progression and transmission. The tsetse’s mutualistic endosymbiont Sodalis glossinidius has a link to trypanosome establishment, providing a disease control target. Here, we describe a new, experimentally verified model of S. glossinidius metabolism. This model has enabled the development of a defined growth medium that was used successfully to test aspects of S. glossinidius metabolism. We present S. glossinidius as uniquely adapted to life in the tsetse, through its reliance on the blood diet and host-derived sugars. Additionally, S. glossinidius has adapted to the tsetse’s obligate symbiont Wigglesworthia glossinidia by scavenging a vitamin it produces for the insect. This work highlights the use of metabolic modeling to design defined growth media for symbiotic bacteria and may provide novel inhibitory targets to block trypanosome transmission.Rebecca J. HallLindsey A. FlanaganMichael J. BotteryVicki SpringthorpeStephen ThorpeAlistair C. DarbyA. Jamie WoodGavin H. ThomasAmerican Society for Microbiologyarticlemetabolismmicrobiomephysiologysymbiosisvector biologyMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	metabolism microbiome physiology symbiosis vector biology Microbiology QR1-502
spellingShingle	metabolism microbiome physiology symbiosis vector biology Microbiology QR1-502 Rebecca J. Hall Lindsey A. Flanagan Michael J. Bottery Vicki Springthorpe Stephen Thorpe Alistair C. Darby A. Jamie Wood Gavin H. Thomas A Tale of Three Species: Adaptation of <named-content content-type="genus-species">Sodalis glossinidius</named-content> to Tsetse Biology, <italic toggle="yes">Wigglesworthia</italic> Metabolism, and Host Diet
description	ABSTRACT The tsetse fly is the insect vector for the Trypanosoma brucei parasite, the causative agent of human African trypanosomiasis. The colonization and spread of the trypanosome correlate positively with the presence of a secondary symbiotic bacterium, Sodalis glossinidius. The metabolic requirements and interactions of the bacterium with its host are poorly understood, and herein we describe a metabolic model of S. glossinidius metabolism. The model enabled the design and experimental verification of a defined medium that supports S. glossinidius growth ex vivo. This has been used subsequently to analyze in vitro aspects of S. glossinidius metabolism, revealing multiple unique adaptations of the symbiont to its environment. Continued dependence on a sugar, and the importance of the chitin monomer N-acetyl-d-glucosamine as a carbon and energy source, suggests adaptation to host-derived molecules. Adaptation to the amino acid-rich blood diet is revealed by a strong dependence on l-glutamate as a source of carbon and nitrogen and by the ability to rescue a predicted l-arginine auxotrophy. Finally, the selective loss of thiamine biosynthesis, a vitamin provided to the host by the primary symbiont Wigglesworthia glossinidia, reveals an intersymbiont dependence. The reductive evolution of S. glossinidius to exploit environmentally derived metabolites has resulted in multiple weaknesses in the metabolic network. These weaknesses may become targets for reagents that inhibit S. glossinidius growth and aid the reduction of trypanosomal transmission. IMPORTANCE Human African trypanosomiasis is caused by the Trypanosoma brucei parasite. The tsetse fly vector is of interest for its potential to prevent disease spread, as it is essential for T. brucei life cycle progression and transmission. The tsetse’s mutualistic endosymbiont Sodalis glossinidius has a link to trypanosome establishment, providing a disease control target. Here, we describe a new, experimentally verified model of S. glossinidius metabolism. This model has enabled the development of a defined growth medium that was used successfully to test aspects of S. glossinidius metabolism. We present S. glossinidius as uniquely adapted to life in the tsetse, through its reliance on the blood diet and host-derived sugars. Additionally, S. glossinidius has adapted to the tsetse’s obligate symbiont Wigglesworthia glossinidia by scavenging a vitamin it produces for the insect. This work highlights the use of metabolic modeling to design defined growth media for symbiotic bacteria and may provide novel inhibitory targets to block trypanosome transmission.
format	article
author	Rebecca J. Hall Lindsey A. Flanagan Michael J. Bottery Vicki Springthorpe Stephen Thorpe Alistair C. Darby A. Jamie Wood Gavin H. Thomas
author_facet	Rebecca J. Hall Lindsey A. Flanagan Michael J. Bottery Vicki Springthorpe Stephen Thorpe Alistair C. Darby A. Jamie Wood Gavin H. Thomas
author_sort	Rebecca J. Hall
title	A Tale of Three Species: Adaptation of <named-content content-type="genus-species">Sodalis glossinidius</named-content> to Tsetse Biology, <italic toggle="yes">Wigglesworthia</italic> Metabolism, and Host Diet
title_short	A Tale of Three Species: Adaptation of <named-content content-type="genus-species">Sodalis glossinidius</named-content> to Tsetse Biology, <italic toggle="yes">Wigglesworthia</italic> Metabolism, and Host Diet
title_full	A Tale of Three Species: Adaptation of <named-content content-type="genus-species">Sodalis glossinidius</named-content> to Tsetse Biology, <italic toggle="yes">Wigglesworthia</italic> Metabolism, and Host Diet
title_fullStr	A Tale of Three Species: Adaptation of <named-content content-type="genus-species">Sodalis glossinidius</named-content> to Tsetse Biology, <italic toggle="yes">Wigglesworthia</italic> Metabolism, and Host Diet
title_full_unstemmed	A Tale of Three Species: Adaptation of <named-content content-type="genus-species">Sodalis glossinidius</named-content> to Tsetse Biology, <italic toggle="yes">Wigglesworthia</italic> Metabolism, and Host Diet
title_sort	tale of three species: adaptation of <named-content content-type="genus-species">sodalis glossinidius</named-content> to tsetse biology, <italic toggle="yes">wigglesworthia</italic> metabolism, and host diet
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/c0668f1dd80e47818646dc391404b3f5
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A Tale of Three Species: Adaptation of <named-content content-type="genus-species">Sodalis glossinidius</named-content> to Tsetse Biology, <italic toggle="yes">Wigglesworthia</italic> Metabolism, and Host Diet

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