Matching the supply of bacterial nutrients to the nutritional demand of the animal host

• Published in: Proceedings of the Royal Society. B, Biological sciences Vol. 281; no. 1791; p. 20141163
• Main Authors: Russell, Calum W., Poliakov, Anton, Haribal, Meena, Jander, Georg, van Wijk, Klaas J., Douglas, Angela E.
• Format: Journal Article
• Language: English
• Published: England The Royal Society 22.09.2014
• Subjects: Acyrthosiphon pisum; Amino Acids, Essential - biosynthesis; Amino Acids, Essential - metabolism; Animals; Aphid; Aphididae; Aphids - genetics; Aphids - growth & development; Aphids - microbiology; Aphids - physiology; Bacteria; Buchnera; Buchnera - metabolism; Buchnera aphidicola; Diet; Essential Amino Acid Synthesis; Metabolic Regulation; Methionine - biosynthesis; Methionine - metabolism; Nymph - genetics; Nymph - growth & development; Nymph - microbiology; Nymph - physiology; Proteome; Symbiosis; Buchnera aphidicola; symbiosis; aphid; essential amino acid synthesis; metabolic regulation
• DOI: 10.1098/rspb.2014.1163
• ISSN: 0962-8452; 1471-2954

Various animals derive nutrients from symbiotic microorganisms with much-reduced genomes, but it is unknown whether, and how, the supply of these nutrients is regulated. Here, we demonstrate that the production of essential amino acids (EAAs) by the bacterium Buchnera aphidicola in the pea aphid Acyrthosiphon pisum is elevated when aphids are reared on diets from which that EAA are omitted, demonstrating that Buchnera scale EAA production to host demand. Quantitative proteomics of bacteriocytes (host cells bearing Buchnera) revealed that these metabolic changes are not accompanied by significant change in Buchnera or host proteins, suggesting that EAA production is regulated post-translationally. Bacteriocytes in aphids reared on diet lacking the EAA methionine had elevated concentrations of both methionine and the precursor cystathionine, indicating that methionine production is promoted by precursor supply and is not subject to feedback inhibition by methionine. Furthermore, methionine production by isolated Buchnera increased with increasing cystathionine concentration. We propose that Buchnera metabolism is poised for EAA production at certain maximal rates, and the realized release rate is determined by precursor supply from the host. The incidence of host regulation of symbiont nutritional function via supply of key nutritional inputs in other symbioses remains to be investigated.