The elimination of intracellular microorganisms from insects: an analysis of antibiotic-treatment in the pea aphid (Acyrthosiphon pisum)

Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.

Evolutionary studies suggest that 200-250 million years ago an aphid ancestor was infected with a free-living eubacterium. The latter became established within aphid cells. Host and endosymbiont (genus Buchnera) became interdependent and unable to survive without each other. The growth of Buchnera became integrated with that of the aphids, which acquired the endosymbionts from their mothers before birth. Speciation of host lineages was paralleled by divergence of associated endosymbiont lineages, resulting in parallel evolution of Buchnera and aphids. Present day Buchnera retains many of the properties of its free-living ancestor, containing genes for proteins involved in DNA replication, transcription, and translation, as well as chaperonins and proteins involved in secretion, energy-yielding metabolism, and amino acid biosynthesis. Some of these processes are also observed in isolated endosymbiont cells. Genetic and physiological studies indicate that Buchnera can synthesize methionine, cysteine, and tryptophan and supply these amino acids to the aphid host. In the case of some fast-growing species of aphids, the overproduction of tryptophan by Buchnera involves plasmid-amplification of the gene coding for anthranilate synthase, the first enzyme of the tryptophan biosynthetic pathway. These recent studies provide a beginning in our understanding of Buchnera and its role in the endosymbiosis with aphids.

1. Non-pathogenic microorganisms, known as mycetocyte symbionts, are located in specialized 'mycetocyte' cells of many insects that feed on nutritionally unbalanced or poor diets. The insects include cockroaches, Cimicidae and Lygaeidae (Heteroptera), the Homoptera, Anoplura, the Diptera Pupiparia, some formicine ants and many beetles. 2. Most mycetocyte symbionts are prokaryotes and a great diversity of forms has been described. None has been cultured in vitro and their taxonomic position is obscure. Yeasts have been reported in Cerambycidae and Anobiidae (Coleoptera) and a few planthoppers. They are culturable and those in anobiids have been assigned to the genus Torulopsis. 3. The mycetocyte cells may be associated with the gut, lie free in the abdominal haemocoel or be embedded in the fat body of the insect. The mycetocytes are large polyploid cells which rarely divide and the symbionts are restricted to their cytoplasm. 4. The mycetocyte symbionts are transmitted maternally from one insect generation to the next. In many beetles (Anobiidae, Cerambycidae, Chrysomelidae and cleonine Curculionidae), the microoganisms are smeared onto the eggs and consumed by the hatching larvae. In other insects, they are transferred from mycetocytes to oocytes in the ovary, a process known as transovarial transmission. The details of transmission in the different insect groups vary with the age of the mother (adult, larva or embryo) at which symbiont transfer to the ovary is initiated; whether isolated symbionts or intact mycetocytes are transferred; and the site of entry of symbionts to the egg (anterior, posterior or apolar). 5. Within an individual insect, the biomass of symbionts varies in a regular fashion with age, weight and sex of the insect. Suppression of symbiont growth rate and lysis of 'excess' microorganisms may contribute to the regulation of symbionts (including freshly-isolated preparations of unculturable forms) are used to investigate interactions between the partners. However, some methods to obtain aposymbiotic insects (e.g. antibiotics and lysozyme) deleteriously affect certain insects and aposymbionts may differ from the symbiont-containing stocks from which they were derived. 7. The mycetocyte symbionts have been proposed to synthesize various nutrients required by the insect. The symbionts of beetles and haematophagous insects may provide B vitamins and those in cockroaches and the Homoptera essential amino acids. The role of symbionts in the sterol nutrition of insects is equivocal. 8. Mycetocyte symbionts may have evolved from gut symbionts or guest microorganisms. The association is monophyletic in cockroaches but polyphyletic in many groups, including the sucking lice, beetles and scale insects.(ABSTRACT TRUNCATED AT 400 WORDS)