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

Ankrah NYD and Douglas AE, 2018. Nutrient factories: metabolic function of beneficial microorganisms associated with insects. Environmental Microbiology. Epub 9 March.

Chung SH, Jing X, Luo Y and Douglas AE. 2018. Targeting symbiosis-related insect genes by RNAi in the pea aphid-Buchnera symbiosis. Insect Biochemistry and Molecular Biology. Epub 8 March.

Luan J, Sun X, Fei Z and Douglas AE, 2018. Maternal inheritance of a single somatic animal cell displayed by the bacteriocyte in the whitefly Bemisia tabaci. Current Biology 28: 459-465.

Ankrah NYD, Luan JB and Douglas AE, 2017. Cooperative metabolism in a three-partner insect-bacterial symbiosis revealed by metabolic modeling. Journal of Bacteriology 199: e00872-16.

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).


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)

 

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)