Aphid adornment: Lateral gene transfer from fungi to aphids.

Carotenoids are integral components of animal biochemistry. These organic compounds, characterized by long hydrocarbon chains and loops, are used in photoreception, antioxidation, the immune system, and for ornamental coloration. There are over 800 known carotenoid compounds found in nature. They absorb varying wavelengths of blue and green light, causing tissue containing large quantities of carotenoids to appear green, yellow, orange, or red. This absorptive property is what makes carotenoids crucial for vision and coloration in animals.

However, there is a snag. Animals cannot produce their own carotenoids. Their genomes lack the enzymes necessary to synthesize carotenoids from smaller hydrocarbons, and therefore they must ingest carotenoids from organisms that can. Certain bacteria, archea, plants, and fungi are all capable of producing specific carotenoids. By adding these organisms to their diet, animals can fulfill their carotenoid needs.

One animal that takes advantage of carotenoid coloration is the pea aphid, Acyrthosiphon pisum. There are two primary color morphs of this aphid species, green and red (see below). The green aphid morph has large quantities of greenish-yellow carotenoids: alpha-, beta-, and gamma-carotene. The red aphid has decreased amounts of those carotenoids, and instead has gobs of the red carotenoid, torulene.

Color morphs of the pea aphid, A. pisum, and the carotenoids predominately responsible for the color variation. Adapted from Moran and Jarvik, 2010.

This polymorphism is of great ecological significance for the aphid. Parasitoid wasps prefer to lay their eggs in green aphids, and carnivorous ladybugs prefer to eat red aphids. If there is a spike in wasp parasitism, the red morphs become more predominant. If there is a spike in ladybug predation, then the green morphs become more common. By maintaining the genetic diversity of both color morphs in an aphid population, that population can guard against being wiped out by a temporal increase in parasites or predators.

However, this polymorphic color variation seen in aphids presents an interesting question. Where are the aphids getting their carotenoids? The plant phloem sap that aphids suck out of leaves is low in carotenoids, and the carotenoids produced by aphid host plants do not match those found in the aphids. In addition, the endosymbiotic bacteria within the aphids cannot be the source of the carotenoids, as there are no carotenoid biosynthesis genes in their genomes.

However, researchers were surprised to discover that the aphid’s red-green color polymorphism is inherited in a classic Mendelian autosomal manner (remember your Punnett squares, kids?), with the red allele dominant to the green allele. This indicates that the genes responsible for carotenoid-based colorations in these aphids are located within their own genomes! A search of the newly published pea aphid genome revealed the presence of several carotenoid synthases, cyclases, and desaturases. This suite of carotenoid biosynthesis genes is capable of producing the colored carotenoids necessary for the red and green aphid color morphs. A mutation in one allele of these genes prevents the production of the red carotenoid, torulene, resulting in the green aphid color morph.

These are the first carotenoid biosynthesis genes found in an animal. Indeed, no other known animal genome, including several other insect genomes, contain homologues to these genes: so where did they come from?

Carotenoid synthesis genes from various organisms. Adapted from Moran and Jarvik, 2010.

A gene tree containing the aphid carotenoid genes, as well as similar genes from bacteria, plants, and fungi can bee seen to the left. The aphid genes (blue) are completely nested within fungal carotenoid biosynthesis genes (brown). Therefore, at some point in aphid evolution, the genes for carotenoid biosynthesis were transfered from a fungi directly into the aphids genome. It is likely that a similar event occurred from bacteria (black) to plants (green) as well. The possible mechanisms for such gene transfers, especially between two eukaryotes, are poorly understood at this point.

Earlier, I wrote about a similar case of lateral gene transfer from algae to a sea slug. That was the first known transfer of genes between multicellular organisms. This new example in aphids lends support to the notion that these lateral gene transfers are more common in eukaryotes that once though. It may turn out, as genome sequencing increases at exponential rates, that the eukaryotic tree of life actually resembles (to some extent) the interconnected gene web seen in bacteria.

References:

  • Moran, N., & Jarvik, T. (2010). Lateral Transfer of Genes from Fungi Underlies Carotenoid Production in Aphids Science, 328 (5978), 624-627 DOI: 10.1126/science.1187113

Hat tip to Microecos for tweeting this.

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Michael Bok is a graduate student studying the visual system of mantis shrimp.

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