How Many Genomes Does It Take to Change a Light Bulb?

by Elio

The cedar aphid and a TEM of a cell containing two endo-
symbiotic bacteria. Courtesy of A. Latorre and J. M. Gosalbes.

Let me rephrase that. How many genomes does it take for an aphid to make tryptophan? If you thought it was one, you'd be wrong: the answer is two, neither being the aphid’s. Remember that aphids live off plant sap that is poor in some amino acids? And that they get some of the missing amino acids from the metabolism of an endosymbiont, Buchnera aphidicola? That’s true enough, but it turns out that in the cedar aphid, Cinara cedri, the resident Buchnera has lost its ability to supply the host with tryptophan. According to investigators from the University of Valencia, Spain, this Buchnera carries the trpEG genes on a plasmid, but lacks trpDCBA, the remaining genes of the pathway.

The predicted biosynthesis pathway and tryptophan flux. Source

This genic foursome is located on the chromosome of another symbiont, Candidatus Serratia symbiotica. (To remind you, Candidatus means that the bacterium has not yet been cultivated. In Roman times, candidatus referred to a soldier awaiting promotion.) Both symbionts are present in about the same number within specialized cells, the bacteriocytes. Why this division of labor? This is grist for the evolutionist’s mill. We invite your views.

Such a complementation of metabolic abilities is far from unique to this aphid. An even more pervasive example of division of labor is seen in a sap-feeding insect, the leafhopper known as the glassy-winged sharpshooter (Homalodisca coagulata). According to McCutcheon and Moran, bacterial endosymbionts act as separate biochemical supply houses. (We discussed an earlier 2006 report from Moran and others here.) As determined by their coding capacities, one of the symbionts, Sulcia muelleri, a member of the Bacteroidetes, provides nine amino acids plus a gene for fatty acid synthesis. This is pretty sporty of this organism, because its highly reduced genome (a mere 245,530 bp) encodes a paltry 228 protein genes. The other symbiont, the γ-proteobacterium Baumannia cicadellinicola, supplies two amino acids and a gemisch of fatty acids, coenzymes, purines, pyrimidines, plus a collection of other metabolites.

The metabolic contributions of Sulcia and Baumannia to the glassy-winged sharpshooter.
The major constituents of the sap are shown in green, above. The large colored arrows
show compounds produced by the symbionts and needed by the host; the small colored
arrows indicate hypothesized sharing between symbionts. Source

Pierce’s disease of grapevines, caused by
the bacterium Xylella fastidiosa, which is
transmitted by a symbiont-carrying glassy-
winged sharpshooter. Source

This story matters to wine makers and wine drinkers because the sharpshooter carries the bacterium Xylella fastidiosa, the agent of the grape vine killing Pierce’s disease. Click here for more on symbioses between sap-feeding insects and bacteria.

Examples of multiple-partner symbioses range across phyla. A marine worm, the oligochete Olavius algarvensis, lacks a mouth, gut, and nephridia (kidney-like organs). To make a living, this worm needs the work of no less than four symbiotic bacteria. These symbionts oxidize sulfur, reduce sulfate, and fix carbon, thus providing the host with varied sources of nutrients.

Olavius algarvensis, a gutless worm
that shuttles its symbiotic bacteria
to optimal energy sources in the
upper oxygen-rich and the lower
oxygen-depleted coastal sediments.
In exchange, the microbes provide
their worm host with fixed carbon
and all the amino acids and vitamins
it needs. Source

The symbionts also participate in recycling of the worm's waste products, which may be how the worms make do without an excretory system—a unique skill among this group of animals. (Fig. 5)

Lynn Margulis once called ours the Symbiotic Planet and wrote a book by that title. Hardly an overstatement! This would be a good time to read the review on symbiosis as an adaptive process by Nancy Moran.

Comments

[Mark O. Martin]

Bravo, Elio. I now know what paper my students will be dissecting in detail during discussion section in a week or two. Many thanks!

You essay got me thinking. John Donne wrote:

"No man is an island entire of itself; every man
is a piece of the continent, a part of the main;
if a clod be washed away by the sea, Europe
is the less, as well as if a promontory were, as
well as any manner of thy friends or of thine
own were; any man's death diminishes me,
because I am involved in mankind.
And therefore never send to know for whom
the bell tolls; it tolls for thee. "

And it is absolutely true that no microbe is an island, either. Genomic or otherwise.

We are all part of a metaorganism, it sure seems. This paper is another piece of the puzzle.

-Mark Martin