Intracellular Symbioses

Metabolic co-evolution in cooperative symbioses between animals and intracellular bacteria

The pea aphid (A) bears Buchnera bacteria in specialized cells (bacteriocytes). B. FISH micrograph of FITC-labeled Buchnera (green) in bacteriocytes. C. Immunocytochemical localization of Buchnera protein GroEL (red) to bacteriocytes. Micrographs of C. Russell, S. Chandler and S. Bouvaine.

Many animals utilize nutritionally-inadequate diets by associating with symbiotic bacteria that: are restricted to specialized insect cells known as bacteriocytes; are invariably transferred from parent to offspring (vertical transmission); and overproduce key nutrients that supplement the inadequate diet of their animal host.

Our research focuses on the bacteriocyte symbioses in plant sap feeding insects. Plant sap-feeding has evolved multiple times among insects of one order, the Hemiptera, but no other animals; and all sap-feeding hemipteran insects have symbiotic microorganisms. For example, aphids bear a single bacterium, Buchnera aphidicola, which derive their total nutritional requirements from the cytoplasm of the aphid bacteriocyte and release essential amino acids back to the insect host.

Reconstructing the metabolic network of Buchnera

We are investigating how the function of the symbiotic bacteria and the host bacteriocyte are structured for nutrient exchange.We apply metabolic models and experimental approaches, informed by genomic, transcriptomic and proteomic data, to establish how essential amino acid overproduction by the symbiotic bacteria is sustained and scaled to host demand.We have found that:

(1) The metabolic capabilities of the bacteriocytes are exquisitely tuned to the nutritional requirements and products of the Buchnera, including functions that compensate for the loss of metabolism-related genes in the Buchnera; and

(2) Essential amino acid synthesis by Buchnera is substrate-limited. Our current model is that Buchnera metabolic network is poised for maximal essential amino acid synthesis, and the realized rate of synthesis is dictated by substrate supply from the bacteriocyte.

We are extending our analysis of nutrient production by intracellular bacteria to other sap-feeding insects, including systems with multiple symbionts.

Selected Recent Publications

Full publication list

Russell CW, Poliakov A, Haribal M, Jander G, van Wijk K and Douglas AE, 2014. Matching the supply of bacterial nutrients to the nutritional demand of the animal host. Proceedings of the Royal Society of London B, 281: 20141163
Jing X, Wong CAN, Chaston JM, McKenzie CL, Colvin J and Douglas AE, 2014. The bacterial communities in plant phloem sap feeding insects. Molecular Ecology 23:1433-1444.
Russell, CW, Bouvaine S, Newell PD and Douglas AE, 2013. Shared metabolic pathways in a coevolved insect-bacterial symbiosis. Applied and Environmental Microbiology 79, 6117-23.
Macdonald SJ, Lin GG, Russell CW, Thomas GH and Douglas AE 2012. The central role of the host cell in symbiotic nitrogen metabolism. Proceedings of the Royal Society of London B 279, 2965-2973.

For financial support of our research on intracellular symbioses in plant sap-feeding insects, we thank:

NSF IOS-1354743 How nutritional interactions in multi-partner symbioses are structured (current)
NSF IOS-0919765 Metabolic coupling in an obligate insect-bacterial symbiosis (with K. van Wijk and G. Jander, 2009-2011)
Bayer Crop Science Immunological attack as a possible target for pest control (current)