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


CONCLUSIONS
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.
Thomas
Gavin H
GH
Department of Biology, University of York, PO Box 373, York, YO10 5YW, UK. ght2@york.ac.uk
Zucker
Jeremy
J
Macdonald
Sandy J
SJ
Sorokin
Anatoly
A
Goryanin
Igor
I
Douglas
Angela E
AE
D000601:Amino Acids, Essential / Q000096:biosynthesis; D020635:Buchnera / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D003198:Computer Simulation; D048168:Escherichia coli K12 / Q000235:genetics / Q000378:metabolism; D005798:Genes, Bacterial; D006639:Histidine / Q000096:biosynthesis; D053858:Metabolic Networks and Pathways / Q000235:genetics; D008954:Models, Biological; D011687:Purines / Q000096:biosynthesis; D013045:Species Specificity; D013559:Symbiosis / Q000235:genetics / Q000502:physiology; D049490:Systems Biology
D000601:Amino Acids, Essential; D011687:Purines; D006639:Histidine