Research article

A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola

Gavin H Thomas^{* 1} , Jeremy Zucker^{* 2} , Sandy J Macdonald¹ , Anatoly Sorokin³ , Igor Goryanin³ and Angela E Douglas^1,4

¹Department of Biology, University of York, PO Box 373, York, YO10 5YW, UK

²Research Computing, Dana Faber Cancer Institute, 44 Binney Street, Boston, MA 0211, USA

³Centre for Intelligent Systems and their Applications, School of Informatics, University of Edinburgh, Appleton Tower, 11 Crichton Street, Edinburgh, EH8 9LE, UK

⁴Department of Entomology, 5136 Comstock Hall, Cornell University, Ithaca, NY 14853, USA

author email corresponding author email* Contributed equally

BMC Systems Biology 2009, 3:24doi:10.1186/1752-0509-3-24

Published:	21 February 2009

Abstract

Background

In silico analyses provide valuable insight into the biology of obligately intracellular pathogens and symbionts with small genomes. There is a particular opportunity to apply systems-level tools developed for the model bacterium Escherichia coli to study the evolution and function of symbiotic bacteria which are metabolically specialised to overproduce specific nutrients for their host and, remarkably, have a gene complement that is a subset of the E. coli genome.

Results

We have reconstructed and analysed the metabolic network of the γ-proteobacterium Buchnera aphidicola (symbiont of the pea aphid) as a model for using systems-level approaches to discover key traits of symbionts with small genomes. The metabolic network is extremely fragile with > 90% of the reactions essential for viability in silico; and it is structured so that the bacterium cannot grow without producing the essential amino acid, histidine, which is released to the insect host. Further, the amount of essential amino acid produced by the bacterium in silico can be controlled by host supply of carbon and nitrogen substrates.

Conclusion

This systems-level analysis predicts that the fragility of the bacterial metabolic network renders the symbiotic bacterium intolerant of drastic environmental fluctuations, whilst the coupling of histidine production to growth prevents the bacterium from exploiting host nutrients without reciprocating. These metabolic traits underpin the sustained nutritional contribution of B. aphidicola to the host and, together with the impact of host-derived substrates on the profile of nutrients released from the bacteria, point to a dominant role of the host in controlling the symbiosis.