The Microbiome of the Tsetse: Metabolic adaptation and the evolution of symbiosis

Bacteria are found in symbiosis with insects of economic and medical importance. The symbionts provide a range of benefits for their hosts, including metabolic supplementation and protection from predation. Consequently, complex interactions can be observed between host and microbiome. The tsetse, genus Glossina, is the vector for the protozoan parasite Trypanosoma brucei. The tsetse has a unique microbiome, consisting of the obligate Wigglesworthia glossinidia and the facultative Sodalis glossinidius. The tsetse is thought to rely on W. glossinidia for the production of B group vitamins, but any benefit of S. glossinidius is yet to be determined. Elucidating key metabolic interactions within the tsetse microbiome, and understanding how these relationships evolved, may open up new avenues for disease control.

To this end, we have constructed and tested metabolic models for S. glossinidius and its free-living relative, Sodalis praecaptivus. The former revealed an intriguing network of metabolic dependencies within the microbiome. S. glossinidius was shown to depend on thiamine produced by W. glossinidia, the chitin monomer N-acetyl-D-glucosamine found in abundance within the tsetse, and amino acids from the blood meal. The S. praecaptivus model was evolved using a multi-objective evolutionary algorithm to explore possible evolutionary trajectories of the Sodalis genus. It was discovered that certain pseudogenisations in S. glossinidius, once thought to be pivotal, may have arisen early in the symbiosis with minimal effect. Finally, substrate binding proteins in W. glossinidia were examined. Whilst functional assays were inconclusive, phylogenetics unexpectedly revealed new information about the relationship of W. glossinidia to other Enterobacteriaeae.

The results presented here demonstrate the interconnected metabolic network within the tsetse microbiome, and provide a platform for investigating other problems in metabolism, adaptation, and evolution in insect-bacterial symbioses.