Mutualism within animal cells insect mycetocyte symbioses

In mycetocyte symbioses between microorganisms and insects, the maternally inherited microorganisms are found within the cytoplasm of specialized cells, mycetocytes, and the interaction is unquestionably mutualistic. It is required by the insects for the nutritional benefits the microorganisms bring, as key providers of essential amino acids, lipids and vitamins, and is required by the microorganisms for their very existence (Douglas, 1998). The symbioses are found in a wide variety of types of insect, and are universally or near-universally present in cockroaches, hom-opterans, bed bugs, sucking lice, tsetse flies, lyctid beetles and camponotid ants. They have evolved independently in different groups of microorganisms and their insect partners, but in effectively all cases the insects live their lives on nutritionally poor or unbalanced diets: phloem sap, vertebrate blood, wood and so on. Mostly the symbionts are various sorts of bacteria, although in some insects yeasts are involved.

Amongst these symbioses, most is known by far about the interactions between aphids and bacteria in the genus Buchnera (Douglas, 1998). The mycetocytes are found in the hemocoel of the aphids and the bacteria occupy around 60% of the mycetocyte cytoplasm. The bacteria cannot be brought into culture in the laboratory and have never been found other than in aphid mycetocytes, but the extent and nature of the benefit they bring to the aphids can be studied by removing the Buchnera by treating the aphids with antibiotics. Such 'aposymbiotic' aphids grow very slowly and develop into adults that produce few or no offspring. The most fundamental function performed by the bacteria is to produce essential amino acids that are absent in phloem sap from nonessential amino acids like glutamate, and antibiotic treatment confirms that the aphids cannot do this alone. In addition, though, the Buchnera seem to provide other benefits, since symbiotic aphids still outperform aposymbiotic aphids when the latter are provided with all the essential amino acids, but establishing further nutritional functions has proved elusive.

aphids and Buchnera ...

. provide an ecological and evolutionary link

The aphid-Buchnera interaction also provides an excellent example of how an intimate association between mutu-alists may link them at both the ecological and the evolutionary level. The Buchnera are transmitted transovarially, that is, they are passed by a mother to her offspring in her eggs. Hence, an aphid lineage supports a corresponding single Buchnera lineage, and this is no doubt the reason for the strictly congruent phylogenies of aphid and Buchnera species: each aphid species has its own Buchnera species (see, for example, Figure 13.12). Moreover, these molecular studies, which allow the Buchnera phylogeny to be reconstructed, also suggest that the aphids acquired Buchnera just once in their evolutionary history, apparently between 160 and 280 million years ago, after the divergence from the main aphid lineage of the only two aphid families not to have a mycetocyte symbiosis, the phylloxerids and the adelgids (Moran et al., 1993). Providing a final twist, the only other aphids without Buchnera (in the family Hormaphididae) appear to have lost them secondarily in their evolutionary history, but they do instead host symbiotic yeasts (Douglas, 1998). It seems more likely that the yeasts competitively displaced the bacteria than that the bacteria were first lost and the yeasts subsequently acquired.

Lastly, Douglas (1998) also points out that whereas all Homoptera that feed on nutritionally deficient phloem sap have mycetocyte symbioses, including the aphids described above, those that have switched secondarily in their evolutionary history to feeding on intact plant cells have lost the symbiosis. This, then, is an illustration from a comparative, evolutionary perspective that even in clearly mutualistic symbioses like these, the benefit is a net benefit. Once the insects' requirements are reduced, as in a switch of diet, the balance of the costs and benefits of the sym-bionts is also changed. In this case, the costs clearly outweigh the benefits on a changed diet: those insects that lost their symbionts have been favored by natural selection.

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