Lessons from studying insect symbioses

Abstract

As in mammals, insect health is strongly influenced by the composition and activities of resident microorganisms. However, the microbiota of insects is generally less diverse than that of mammals, allowing microbial function in insects to be coupled to individual, identified microbial species. This trait of insect symbioses facilitates our understanding of the mechanisms that promote insect-microbial coexistence and the processes by which the microbiota affect insect well-being. As a result, insects are potentially ideal models to study various aspects of interactions between the host and its resident microorganisms that would be impractical or unfeasible in mammals and to generate hypotheses for subsequent testing in mammalian models.

Figure 1

The Insect IMD Pathway and Persistence of Resident Microorganisms. The IMD (Immune Deficiency) pathway is triggered by binding of bacterial peptidoglycan (PGN) to the peptidoglycan recognition protein PGRP-LC (dashed vertical line). The resultant activation of the NF-κB transcription factor Relish leads to the upregulated expression of anti-microbial peptide (AMP) genes. Positive interactions (blue), negative interactions (red) (A) Resident microorganisms in the Drosophila gut activate the IMD pathway, but expression of AMPs is repressed by the transcription factor Caudal. (B) The IMD pathway in bacteriocytes (insect cells bearing symbiotic bacteria) of the Glossina tsetse fly and weevil Sitophilus is activated, but the immunoreactivity of bacteriocytes is dampened by the very high expression of the IMD-responsive gene PGRP-LB. PGRP-LB is a PGN-amidase that degrades the PGN ligand, thereby down-regulating the IMD pathway.

Figure 2

Coevolution of Amino Acid Biosynthesis in Plant Sap-Feeding Insects and their Bacterial Symbionts (A) In the symbiosis between the pea aphid and Buchnera bacteria, the Buchnera (but not aphid) has lost the capacity to synthesize eight amino acids (red), and the aphid (but not Buchnera) has lost the capacity to synthesize arginine (blue) relative to the ancestral condition (E. coli, a relative of Buchnera, and a generalized insect, respectively). The one-reaction synthesis of glycine from serine is retained by both partners. Cysteine is synthesized by different pathways in the two partners (from methionine in the aphid, from serine in Buchnera). (B) Spittlebugs, cicadas and sharpshooters bear two bacterial symbionts, Sulcia and an auxiliary symbiont with complementary amino acid biosynthetic capabilities. The amino acids produced by each bacterium are made available to both the insect host and the alternative bacterium. Both bacteria require the ten non-essential amino acids from the host. [ala:alanine; arg: arginine; asn: asparagine; asp: aspartate; cys: cysteine; gln: glutamaine; glu: glutamate; gly: glycine; his: histidine; ile: isoleucine; leu: leucine; lys: lysine; met: methionine; phe: phenylalanine; pro: proline; ser: serine; thr: threonine; trp: tryptophan; tyr: tyrosine; val: valine].