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.

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 are finding that the metabolic capabilities of the bacteriocytes are exquisitely tuned to the nutritional requirements and products of the symbiotic bacteria, including functions that compensate for the loss of metabolism-related genes in the bacteria.  In some symbioses, such as the whitefly Bemisia tabaci, the synthesis of certain essential amino acids (e.g. lysine) involves reactions coded by genes horizontally transferred from other bacteria to the insect genome.


Selected Recent Publications

Full publication list

Douglas AE 2016. How multi-partner endosymbiosis function. Nature Reviews Microbiology 14, 731-43.

Luan JB, Shan H-W, Isermann P, Huang J-H, Lammerding J, Liu S-S and Douglas AE 2016. Cellular and molecular remodeling of a host cell for vertical transmission of bacterial symbionts. Proceedings of the Royal Society of London B 283 (1833).

Luan J, Chen W, DK, Simmons AM, Wintermantel WM, Ling K-S, Fei Z, Liu S-S and Douglas AE 2015. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome Biology and Evolution 15, 2635-47.

Douglas AE 2014. Molecular dissection of nutrient exchange at the insect-microbial interface. Current Opinion in Insect Science 4, 23-28.

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.


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

NSF
NSF IOS-1354743   How nutritional interactions in multi-partner symbioses are structured (current)
   USDA2
AFRI-NIFA-2015-67013-23421: Identification of molecular targets to disrupt the bacterial symbiosis in aphid pests (current)

 

Bayer
Bayer Crop Science  Immunological attack as a possible target for pest control (current)

 

 

cassava whitefly project2
OPP1058938: Bill and Melinda Gates Foundation African cassava whitefly: outbreak causes and sustainable solutions (current) This consortium grant is led by PI John Colvin, Natural Resources Institute, London; full details of the consortium are available here)