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Cow-like Mealybug Home to Sexy Symbiotic Machine

The views expressed are those of the author and are not necessarily those of Scientific American.


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Mealybugs and their myrmecoid herders. Photo by Ron Hemberger, courtesy J. McCutcheon. Used with permission.

If it goes around on six legs, it doesn’t get much dowdier than the mealybug 1. Powdery, bovine, and frightening if you find them binging on your gardenias, these wax-shedding roving syringes are one of many mosquito-like parasites that plague plants. Yes, sexy, mealybugs are not — unless you look inside them.

There, you will find a finely tuned engine for turning sugary, protein-poor tree sap into something nourishing enough to support mealybug, symbiotic bacterium, and the symbiotic bacterium that lives inside the symbiotic bacterium. You read that right. Mealybugs have nested bacterial helpers.

Mealybugs are soft unarmored insects in the taxon Hemiptera, the true bugs. Along with mealybugs, the group includes aphids, cicadas, leafhoppers, planthoppers, psyllids, scale insects, spiuttlebugs, and whiteflies. True bugs are defined by their special mouthparts, which are bunched into siphon tubes or probosci called rostra (sing. rostrum, lit. “beak”), used (usually) for drinking plant fluids. Many of them have half-hardened wings as well, the origin of the name for the group. Mealybugs, as mentioned, also tap plant juices and, also like mosquitoes, carry plant diseases.

Interestingly, mealybug males look nothing like mealybug females. Though the females are stout and redoubtable, the males are svelte and ephemeral. You’d never guess by looking they were a pair; Jack Spratt et al. come to mind. Males undergo a complete transformation to a wasp-like form in adulthood, whereupon they stop eating, and exist only to fly to females to help make little mealybugs. Then they snuff it, as Monty Python would say.

The females retain their nymphal appearance and grow no wings, fatten themselves up throughout life, and secrete protective curls of wax through densely-distributed dermal glands, producing the mealy, powdery mess for which they are named.

Mealybugus femalus, with waxy outer coating. If you look carefully, you can see their cute little tan antennae at left. Creative Commons Christian Fischer. Click image for link and license.

Like most insects in Hemiptera, mealybugs pierce plant cells with their siphoning mouthparts, attempt to avoid getting blown off the plant by the resulting gusher of pressurized plant fluids 2, and in the process, act as living filters for phloem sap. Sap is rich in sugars, which is good. But it is very low in protein, which is bad. That means you need to filter a whole lot of sap to get the protein you need to make mealy goodness, thereby excreting a lot of uneeded sugar solution in the process (a substance called honeydew that is often capitalized upon by aphid- and mealybug-herding ants, as in the photo at top), or come up with some way to MacGyver some proteins out of what you can filter from the sap. Or both. Mealybugs have gone with both.

Scientists have known for some time that most insects who eat plant sap partner with bacterial symbionts to make up for their protein-poor diet. Job Number One for the symbionts is to help make amino acids, the building blocks of proteins. Mealybugs need help in order to produce 10 amino acids they can’t make on their own.

Mealybugs aren’t the only ones with an amino acid problem. Humans are unable to synthesize about eight of the 21 or so amino acids, which we must get from our diet. Some plants are extremely poor sources of particular amino acids. This is why people subsisting on a diet of only corn — which, when untreated by lime, is deficient in the amino acid lysine — can develop the nutrient-deficiency disease pellagra. We get around this by eating meat, eggs, or dairy — which, being animal protein, already contain all the amino acids we need — or by varying our plant sources of protein 3.

Mealybugs, on the other hand, are stuck with a diet of sap followed by more sap. Since this diet can’t provide those 10 amino acids, their bacterial symbionts must. But the way in which citrus mealybugs do this is stunningly different. Inside the citrus mealybug, Planococcus citri, live two bacteria: Moranella endobia, a gammaproteobacterium, and Tremblaya princeps, a betaproteobacterium 4. Moranella lives inside Tremblaya. This is completely unprecedented for insect symbionts.

Nested symbionts: The medium-gray and medium-sized blob is Tremblaya, while the four light, speckled cells are Moranella nestled within it. Photo courtesy Carol von Dohlen; Utah State University

What is more, Tremblaya has the smallest cellular genome yet found — just 139,000 base pairs — and it is four times smaller than the genome of the bacteria that live inside it. This extends to gene content — the genome of innermost symbiont contains 452 genes, while its host bacterium contains a mere 140 genes, the smallest number on record for a cellular being.

Just how stripped down is Tremblaya? It has no functional aminoacyl-tRNA synthetases, the enzymes that make the molecules that are the backbone of protein synthesis by delivering amino acids to corresponding messenger RNA codons in the presence of ribosomes. It’s missing many essential genes for amino acid synthesis, though its two partners seem to have most of those missing.

It’s also missing proteins for translation release factors unique to bacteria, making it unlikely the mealybug is supplying these. Unless, that is, the genes have been transferred to the host as some mitochondrial (themselves the product of a very ancient bacterial symbiosis) genes have, and are reimported, but no other precedent for this exists.

This spartan genome blows the organism most often held up as the smallest cellular genome — Mycoplasma genitalium, the cause of non-specific genital disease and subject of the first attempt at synthetic life — out of the water, and in fact many other bacterial symbionts or parasites have of late. M. genitalium‘s genome size is on the order of Moranella‘s as you can see below. For further comparison, the largest viruses — the mimi- and mamaviruses — have genomes over 1 million base pairs long.

Of course, parasites and symbionts share an advantage: they can rely on their hosts to provide the products of many essential genes for replication and protein-production, and can thus shed duplicate genes like so much unwanted baggage. Now they not only don’t have to expend energy to make proteins out of these genes, they can also compact their genome over time through fortuitous deletions, which means they don’t even have to go to the trouble and expense of replicating the genes for these proteins themselves. The result, over time, is genome reduction and compaction.

In the case of Tremblaya, it has a double advantage: it is both a symbiont and a host. Thus it has two genomes from which to mooch gene products, allowing it to farm out its genomics to both host and endosymbiont. On top of that, its endosymbiont is another bacterium, which means it can rely on Moranella for the bacterial versions of many important proteins (the mealybug host is eukaryotic — so cannot provide essential bacterial forms of many proteins for things like DNA replication that bacteria do differently than eukaryotes). So perhaps there is little reason to be surprised that its genome is so diminutive 5.

This is not to say Tremblaya is slacking. Although the Moranella genome is much larger overall, Tremblaya is doing much more of the amino acid synthesis. Its genome codes for 29 genes involved in amino acid synthesis, compared to 15 in Moranella.

And here’s the second bombshell about the citrus mealybug’s dual symbiosis, and the one reported in this month’s Current biology in work done by the University of Montana’s John McCutcheon and Utah State’s Carol von Dohlen: no single amino acid synthesis pathway is complete in either organism. In all other studied insect multi-species symbioses (presumably two bacteria living within insect host cells, but not nested one inside another), complete or near-complete pathways for individual amino acids have been preserved within individual bacteria. In citrus mealybug, the intermediates of amino acid synthesis shuttle back and forth between symbionts and host like a Plinko chip in action.

What’s more, there’s little overlap in genes for metabolic pathways; that is, each partner seems to have got one intermediate molecule/step covered, and so the other two have dropped it from their genomes.

It’s a mystery how all this shuffling and shuttling takes place. How do the molecules move about? In most instances, cells have to expend energy in the form of ATP to move large molecules in and out of cells through specific transport proteins which much be made individually, specifically, and expensively for nearly every protein. But here, active protein transporters don’t seem to be involved — a Tremblaya genomic search turned up code for none.

This leads to an incredible hypothesis, the researchers suggest: Tremblaya may blow up (well, technically lyse) some of its internal bacterial herd in order to supply the gene products it is missing in one easy, all-encompassing step. So long as most Moranella continue to replicate unmolested, it is of no concern to them, presumably, if a bit of the herd is culled. It’s a bit like — forgive another cow metaphor — cattle ranching.

Alternatively, some Moranella cells may occasionally blow up on their own, which would achieve the same end. Incidentally, the honeydew-feeding ants that ranch mealybugs and aphids several rungs up the ladder are also possibly not above occasionally thinning the herd, if you know what I mean, for protein supplementation purposes.

When Lynn Margulis (Carl Sagan’s ex-wife and a renowned biologist in her own right) first advanced the now well-accepted endosymbiotic theory that chloroplasts and mitochondria were the result of ancient bacterial engulfments by primitive eukaryotic cells, it is my understanding most biologists thought she was kinda nuts. Now, we are finding endosymbiosis in various stages of completion is not only common, it’s rampant in many distantly-related kinds of algae, corals, chemosynthetic deep-sea vent creatures, plant-sucking insects, and probably in some other groups I’m not as familiar with as well (protists?).

But the sort of nested symbiotic protein synthesis pinball we see in otherwise mundane-seeming mealybugs is something else indeed. How many more outlandish symbiotic setups will we find, if only we look? Life’s story just gets better — and weirder — all the time.

ResearchBlogging.org
McCutcheon, J., & von Dohlen, C. (2011). An Interdependent Metabolic Patchwork in the Nested Symbiosis of Mealybugs Current Biology DOI: 10.1016/j.cub.2011.06.051

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1 You might make an argument for the closely-related scale insects, which, after maturity, turn into permanently-attached parasites that can neither move nor see, but at that point, I’d argue, they’re essentially a potted plant.

2 I don’t know if this could actually happen, but I do know these insects don’t have to suck because the internal pressure of the sugar-transporting tissue called phloem that parasitic insects tap forces the sap (phloem contents) out. I also know that scientists wishing to study this pressure once did so by allowing aphids to latch on, then slicing their bodies off with lasers, leaving their straw-like mouthparts in place. The sap continued to flow though them, allowing scientists to measure the pressure under a variety of environmental conditions without disturbing the plant.

“Do you expect me to drink?”

“NO, Mr. Aphid, I expect you to DIE!”

3 This is why people make such a big deal about foods that are “complete” sources of protein like quinoa, which means the plant is a good source all of the amino acids we can’t make ourselves.

4 Proteobacteria (named after the shape-shifting god Proteus) are Gram-negative bacteria that encompass a huge variety of form and function. This includes pathogens like plague, cholera and Salmonella, purple bacteria that photosynthesize, and the myxobacteria, a group of bacterial slime molds. You can see how the proteobacteria fit into all the rest of the bacteria here.

5 There is one other oddity about the Tremblaya genome: it is relatively gene-sparse compared to most super-compact parasite/symbiont bacterial genomes, as you can see from the coding density column above. Bacteria are already super-gene dense compared to eukaryotes; while our bloated genomes are only 1.5 to 2 percent functional genes (the rest is “non-coding”), most bacterial chromosomes, built for replication efficiency and speed, are 80-90 percent genes. Bacterial parasites and symbionts typically achieve 93-97 percent. Tremblaya sits at 72.9 percent. But when a new parasitism or symbiotic event takes place, it may take a while for redundant genes to become inactive and the genome pared down to the minimum gene set that is stable/allowable in the new configuration. Tremblaya may, in fact, be in the process of a second genome reduction thanks to recent Moranella introduction, explaning its relatively gene sparse genome compared to its size.

Jennifer Frazer About the Author: Jennifer Frazer is a AAAS Science Journalism Award-winning science writer. She has degrees in biology, plant pathology/mycology, and science writing, and has spent many happy hours studying life in situ.
Nature Blog Network
Follow on Twitter @JenniferFrazer.

The views expressed are those of the author and are not necessarily those of Scientific American.





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