Symbiotic bacteria enable insect to use a nutritionally inadequate diet

Abstract

Animals generally require a dietary supply of various nutrients (vitamins, essential amino acids, etc.) because their biosynthetic capabilities are limited. The capacity of aphids to use plant phloem sap, with low essential amino acid content, has been attributed to their symbiotic bacteria, Buchnera aphidicola, which can synthesize these nutrients; but this has not been demonstrated empirically. We demonstrate here that phloem sap obtained from the severed stylets of pea aphids Acyrthosiphon pisum feeding on Vicia faba plants generally provided inadequate amounts of at least one essential amino acid to support aphid growth. Complementary analyses using aphids reared on chemically defined diets with each amino acid individually omitted revealed that the capacity of the symbiotic bacterium B. aphidicola to synthesize essential amino acids exceeded the dietary deficit of all phloem amino acids except methionine. It is proposed that this shortfall of methionine was met by aphid usage of the non-protein amino acid 5-methylmethionine in the phloem sap. This study provides the first quantitative demonstration that bacterial symbiosis can meet the nutritional demand of plant-reared aphids. It shows how symbiosis with micro-organisms has enabled this group of animals to escape from the constraint of requiring a balanced dietary supply of amino acids.

Figure 1

Amino acid budget of pea aphids reared on V. faba. (a) Contribution of individual amino acids to protein growth of two- to seven-day-old aphids. (b) Shortfall of essential amino acids required for aphid growth in phloem sap of eight plants (i)–(viii). The total amino acid concentration of each phloem sample is: (i) 169 mM; (ii) 204 mM; (iii) 207 mM; (iv) 273 mM; (v) 280 mM; (vi) 327 mM; (vii) 460 mM; (viii) 490 mM. The proportion of the shortfall met by Buchnera-derived amino acids is shown above each bar; note that glycine is a non-essential amino acid and any shortfall can be met by aphid metabolism (ala, alanine; asx, aspartic acid and asparagine; glx, glutamic acid and glutamine; gly, glycine; ser, serine; tyr, tyrosine; arg, arginine; ile, isoleucine; leu, leucine; lys, lysine; met, methionine; phe, phenylalanine; thr, threonine; trp, tryptophan; val, valine).

Figure 2

Mean amino acid composition of V. faba phloem sap (abbreviations for amino acids are provided in the legend to figure 1).

Figure 3

The pea aphid on chemically defined diets. (a) Mean RGR of two- to seven-day-old aphids on the standard diet containing all protein amino acids (S) and diets from which one essential amino acid was deleted (Fo, Io, etc). ANOVA: diet: F₁₀₃₈₆=5.20, 0.01>p>0.001; antibiotic treatment: F₁₃₈₆=1219, p<0.001; interaction: F₁₀₃₈₆=2.77, 0.01>p>0.001. The error terms are not shown for clarity and are provided in electronic supplementary material 3. (Fo, phenylalanine; Io, isoleucine; Ko, lysine; Lo, leucine; Mo, methionine; Ro, arginine; To, threonine; Vo, valine; Wo, tryptophan). (b) Contribution of Buchnera-derived amino acids to the protein growth of the aphids (abbreviations for amino acids are provided in the legend to figure 1).