The natural history of the interaction between bacterial symbionts and their hosts

Bacteria were first recognized as being commonly found as symbionts of insects from morphological and microscopy studies. A seminal synthesis was made by Anton Buchner, whose treatise on Endosymbioses of Animals with Plant Microorganisms detailed the presence of organs of host origin within the bodies of many insects that carry bacteria in large numbers, reviewed the means by which these bacteria were transmitted to the next generation, and made some comments on their function (Buchner, 1965). The examples given in Buchner's text are mainly of bacteria that are integrated into the anatomy and function of insects. Two different modes of transmission were observed. In tran-sovariol transmission, the bacteria were generally internalized within the insect, and passed from a female into her egg at the point of fertilization. In transovum transmission, material containing the bacteria were commonly present in gut diverticu-lae, and were physically placed onto the egg or in the vicinity of larvae, and then ingested by the larvae on hatching.

Aside from Buchner's work, the discovery of symbionts followed from two different lines of research. First, microscopy work found evidence of bacteria inside particular cells, rather than organs carrying bacteria. The inherited bacterium Wolbachia was first described in this way (Hertig and Wolbach, 1924; Hertig, 1936). This strand of discovery became particularly fruitful with the advent of electron microscopy, which revealed the presence of intracellular bacteria in many species. Rickettsia bacteria were likewise first described in this manner.

Aside from microscopy, inherited bacteria were also discovered from observation of their pheno-type, in particular maternally inherited sex-ratio biases and incompatibilities. Sporadic records of insect lines producing all-female broods were recorded in butterflies, woodlice, ladybirds, and fruit flies over the period from 1920 to 1950, where the trait was inherited down the female line (Simmonds, 1928; Vandel, 1941; Lus, 1947; Magni, 1952). Following the discovery of male-killing in the Drosophila willistoni group of flies (Malogolowkin, 1958), experimental work then established that the agents were infectious through microinjection rather than an established component of the fly genome (Malogolowkin et al., 1961), and the combination of antibiotic sensitivity of the trait with the inability of the agent to pass through filters of 450 nm gauge indicated that the causal agents were bacterial.

Aside from sex-ratio distortion, incompatibility between lines of particular insects from different populations was also ascribed to maternally inherited elements. In the work of Laven (1951), different mosquito lines were incompatible, but this incompatibility was associated with maternal line and independent of nuclear background. Microscopy and sensitivity of the trait to antibiotics demonstrated associations with maternally inherited bacteria (Yen and Barr, 1971). Inherited bacteria causing incompatibility have since been observed in many species.

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