A Tale of Three Species: Adaptation of Sodalis glossinidius to tsetse biology, Wigglesworthia metabolism and host diet

TY - JOUR

T1 - A Tale of Three Species

T2 - Adaptation of Sodalis glossinidius to tsetse biology, Wigglesworthia metabolism and host diet

AU - Hall, Rebecca Jane

AU - Flanagan, Lindsey Anne

AU - Bottery, Michael John

AU - Springthorpe, Victoria Jayne

AU - Thorpe, Stephen

AU - Darby, Alistair C

AU - Wood, Andrew James

AU - Thomas, Gavin Hugh

N1 - © 2019 Hall et al.

PY - 2019/1/1

Y1 - 2019/1/1

N2 - The tsetse is the insect vector for the Trypanosoma brucei parasite, the causative agent of human African trypanosomiasis. The colonisation and spread of the trypanosome correlates 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 analyse 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 dependency on L-glutamate as a source of carbon and nitrogen. Finally, the selective loss of thiamine biosynthesis, a vitamin provided to the host by the primary symbiont Wigglesworthia glossinidia, reveals an inter-symbiont dependency. The reductive evolution of S. glossinidius to exploit environmentally-derived metabolites has resulted in multiple weaknesses in the metabolic network. These may become targets for reagents that inhibit S. glossinidius growth and aid the reduction of trypanosomal transmission.

AB - The tsetse is the insect vector for the Trypanosoma brucei parasite, the causative agent of human African trypanosomiasis. The colonisation and spread of the trypanosome correlates 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 analyse 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 dependency on L-glutamate as a source of carbon and nitrogen. Finally, the selective loss of thiamine biosynthesis, a vitamin provided to the host by the primary symbiont Wigglesworthia glossinidia, reveals an inter-symbiont dependency. The reductive evolution of S. glossinidius to exploit environmentally-derived metabolites has resulted in multiple weaknesses in the metabolic network. These may become targets for reagents that inhibit S. glossinidius growth and aid the reduction of trypanosomal transmission.

KW - Metabolism

KW - Microbiome

KW - Physiology

KW - Symbiosis

KW - Vector biology

KW - Adaptation, Physiological

KW - Carbon/metabolism

KW - Feeding Behavior

KW - Thiamine/metabolism

KW - Glutamates/metabolism

KW - Tsetse Flies/microbiology

KW - Animals

KW - Enterobacteriaceae/growth & development

KW - Energy Metabolism

KW - Culture Media/chemistry

KW - Glucose/metabolism

KW - Disease Vectors

KW - Nitrogen/metabolism

UR - http://www.scopus.com/inward/record.url?scp=85059500428&partnerID=8YFLogxK

U2 - 10.1128/mBio.02106-18

DO - 10.1128/mBio.02106-18

M3 - Article

C2 - 30602581

SN - 2161-2129

VL - 10

JO - MBio

JF - MBio

IS - 1

M1 - e02106-18

ER -