The association between plant sap feeding insects and their intracellular bacterial symbionts

The symbiotic bacteria provide nutrients to their insect hosts

Various insects possess beneficial microorganisms housed in specialized cells called bacteriocytes.  Most of these microorganisms have a nutritional role. In plant sap feeding insects, the microorganisms provide essential amino acids.  For example, the pea aphid obtains 4 x its total nitrogen requirement from the phloem sap of its host plant Vicia faba (fava bean), but the essential amino acid content is very low (see Figure). 

Amino acid requirement for protein growth of the fourth (final) larval stadium of the pea aphid larvae.  The requirement for most non-essential amino acids (other than glycine) is met from the diet of phloem sap, but the greater part of the essential amino acid requirement is met by the symbiotic bacterium Buchnera (the endogenous source).

Nutritional interactions across the interface between the Buchnera bacteria and bacteriocyte 

The supply of essential amino acids from Buchnera bacteria to the aphid host is founded on dynamic interactions between the bacterial cells and bacteriocyte (the aphid cell that houses the bacteria). 

By annotation of the genomes of the pea aphid and its Buchnera symbiont, quantitative transcriptomics and proteomics of the bacteriocyte, together with metabolomics and metabolic modeling, we have inferred that 58 metabolites are transferred between the partners (Wilson et al. 2010Poliakov et al. 2011, Macdonald et al. 2012, Russell et al. 2013).

Figure Metabolite exchange across the symbiotic interface of the pea aphid-Buchnera symbiosis. Number of transferred metabolites, inferred from metabolic modeling. Macdonald et al. 2012.

The 33 inputs to Buchnera include all the nutrients required by Buchnera for growth and the precursors for the synthesis of essential amino acids released back to the host.  Metabolic exchange is substantial because Buchnera is metabolically-fastidious, and the biosynthetic pathways for 5 of the 10 EAAs are shared between Buchnera and aphid with shuttling of intermediates between the partners exchange across the symbiotic interface.

Figure Shared biosynthesis of the essential amino acid isoleucine between Buchnera and insect, with aphid cystathione-gamma-lyase (CGL) and branched chain aminotransferase (BCAT) predicted to mediate the reactions  of ‘missing’ Buchnera  IlvA and IlvE. For further details, see Wilson et al. 2010 and Russell et al. 2013.

We have also demonstrated nitrogen recycling in the aphid-Buchnera symbiosis, i.e. that host nitrogenous waste (ammonia) is utilized in the synthesis of essential amino acids.  However, nitrogen recycling is mediated by host enzymes, specifically transaminases e.g. BCAT, that utilize carbon skeleton that can be synthesized only by the Buchnera symbiont. 

Figure Alternative scenarios of symbiotic nitrogen recycling involving an intracellular symbiont (green). Microbial symbionts in various animals are hypothesized to recycle nitrogen, but Buchnera is very limited capacity for ammonia assimilation.  In the pea aphid, the bacteriocyte incorporates waste ammonia via glutamine synthetase/glutamate synthase (GS/GOGAT) and linked transaminases into symbiont-derived carbon skeletons to generate essential amino acids (specifically the three branched chain amino acids and phenylalanine).  Further details in Macdonald et al. 2012.