Join 3,572 readers in helping fund MetaFilter (Hide)


The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes.
October 22, 2012 6:46 AM   Subscribe

One of the many problems farmers of various kinds of legumes need to deal with is the pea aphid. They reproduce incredibly fast and live by sucking the sap out of the plants, an electron micrograph of one in action. However, while they are terrifying parasites of legumes, they have their own yet more horrific parasites, a parasitoid wasp. Here is a really nice close up picture of one doing its thing, a video of the act, and here is a brain meltingly horrific video of a dissection of the mummified aftermath 8 days later. Essentially, these wasps deposit their eggs in a pea aphid and the growing larva feeds on it, developing there for about a week, and then consuming the host from the inside out like a Xenomorph. When it’s done, the wasp larva dries the aphid’s cuticle into a papery brittle shell and an adult wasp emerges from the aphid mummy. Legume farmers love them, and you can even order their mummies online these days. However, farmers noticed that the wasps didn't work as effectively on all of the aphids, and so researchers went to work figuring out why. It turns out that all aphids have a primary bacterial endosymbiont living inside their cells, in addition to and just like a mitochondria, and that many have some combination of five other secondary endosymbionts. Interestingly, two of those other five, Hamiltonella defensa and Serratia symbiotica have been shown to confer varying levels of resistance to the parasitoid wasp, allowing the aphid to survive infection. However, it turns out that there is yet one more layer to this story,

The relationship these endosymbionts have with the aphid, as well as the primary endosymbiont, is hard to classify as they confer a fitness cost in the absence of the wasp but a significant fitness boost when the wasps are around and trying to infect the aphids. At least for H. defensa, the reason why some strains are fully parasitic and provide no protection against the wasps while others are at least plausibly commensal and do provide protection, is a bacterial virus that infects the endosymbiont, even while it is inside the eukaryotic aphid cell. To understand why it will require a bit of knowledge of how some bacteriophages work. Most bacterial viruses, also known as bacteriophages, have a clear dividing line between two strategies. The simplest and most virulent phages will always immediately shut down their host’s metabolism upon infection and replace it with their own. Within a short period of time, generally between 20 and 80 minutes, the phage will have used the host cell to replicate its genome, build new viral particles, packed those particles with the genome and lysed the cell; setting loose 30-3000 new inert infectious particles. These are known as obligately lytic phages. Most phages however, use a mix of this strategy and another one known as lysogeny. These temperate phages will, at the beginning, decide to either virulently infect, producing particles at the total expense of the host, or hide in the host’s genome and inactivate all of its many host lethal genes. Generally it does this by expressing a transcriptional repressor that prevents expression of everything but the repressor, which incidentally protects the host from subsequent infection by related phages. However, some temperate phages will allow for expression of a genomic cassette that will perform some function of benefit to their host - they might as well since they are completely dependent on their host's wellbeing while in this stage of their life cycle.

It turns out that there is a temperate bacteriophage called APSE, which is common in H. defensa populations in the aphids, that encodes for a cassette of genes that causes H. defensa to attack the wasp larvae with vicious toxins while the phage hides in the genome of its bacterial host. This makes for a really fascinatingly complex system of interdependencies for each of the agents involved. The phage, the bacterial symbiont, and the aphid are all each united in their interdependent need to combat the wasp that kills all three when it succeeds. However, at the same time, both the phage and the bacteria are dependent on the wasp to apply pressure on the aphid to keep them around - otherwise the aphid would cure itself of both creatures that would then be free-loading. Additionally, the wasp the bacteria, and the phage are all completely dependent on the aphid’s sap sucking ability to sustain them, and the aphid is totally dependent on the farmer to continue growing legumes in massive vulnerable monocultures. Furthermore the farmer and the legumes are dependent on the wasp to combat the aphid and largely helpless against the bacteria and the phage. At the same time, despite all of the interlocking incentives toward cooperation, there are also incentives towards each of these agents cheating each other. The farmer has an incentive to ‘cheat’ and save money by neglecting to buy aphid mummies every so often, because they still benefit from the fitness cost caused by the aphid not rejecting the bacteria or the bacteria rejecting the phage. Similarly, the aphid has an incentive to cheat both the bacteria and the phage to cure itself of them and bet on the farmer not buying aphid mummies full of wasps that year. The bacteria also has an incentive to cheat the aphid by curing itself of the phage, and also bet on the farmer not buying mummies that year itself.

Oliver KM, Degnan PH, Hunter MS, & Moran NA. 2009. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325(5943); 992-4. [REQUIRES FREE REGISTRATION]
Bacteriophages are known to carry key virulence factors for pathogenic bacteria, but their roles in symbiotic bacteria are less well understood. The heritable symbiont Hamiltonella defensa protects the aphid Acyrthosiphon pisum from attack by the parasitoid Aphidius ervi by killing developing wasp larvae. In a controlled genetic background, we show that a toxin-encoding bacteriophage is required to produce the protective phenotype. Phage loss occurs repeatedly in laboratory-held H. defensa–infected aphid clonal lines, resulting in increased susceptibility to parasitism in each instance. Our results show that these mobile genetic elements can endow a bacterial symbiont with benefits that extend to the animal host. Thus, phages vector ecologically important traits, such as defense against parasitoids, within and among symbiont and animal host lineages.

Moran NA, Degnan PH, Santos SR, Dunbar HE, & Ochman H. 2005. The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. PNAS USA, 102(47); 16919-26.
Aphids maintain mutualistic symbioses involving consortia of coinherited organisms. All possess a primary endosymbiont, Buchnera, which compensates for dietary deficiencies; many also contain secondary symbionts, such as Hamiltonella defensa, which confers defense against natural enemies. Genome sequences of uncultivable secondary symbionts have been refractory to analysis due to the difficulties of isolating adequate DNA samples. By amplifying DNA from hemolymph of infected pea aphids, we obtained a set of genomic sequences of H. defensa and an associated bacteriophage. H. defensa harbors two type III secretion systems, related to those that mediate host cell entry by enteric pathogens. The phage, called APSE-2, is a close relative of the previously sequenced APSE-1 but contains intact homologs of the gene encoding cytolethal distending toxin (cdtB), which interrupts the eukaryotic cell cycle and which is known from a variety of mammalian pathogens. The cdtB homolog is highly expressed, and its genomic position corresponds to that of a homolog of stx (encoding Shiga-toxin) within APSE-1. APSE-2 genomes were consistently abundant in infected pea aphids, and related phages were found in all tested isolates of H. defensa, from numerous insect species. Based on their ubiquity and abundance, these phages appear to be an obligate component of the H. defensa life cycle. We propose that, in these mutualistic symbionts, phage-borne toxin genes provide defense to the aphid host and are a basis for the observed protection against eukaryotic parasites.

This post is deeply endebted to one made on Moselio Schaechter's blog Small Things Considered, which is no doubt more clearly written.
posted by Blasdelb (50 comments total) 71 users marked this as a favorite

 
It's parasites all the way down.
posted by Ice Cream Socialist at 6:53 AM on October 22, 2012 [10 favorites]


How very intelligently designed!

Do I even have to add "hamburger"?
posted by Skeptic at 6:53 AM on October 22, 2012 [2 favorites]


Another parasitoid wasp, but this one goes for a more mechanical approach.
posted by curious nu at 6:54 AM on October 22, 2012


Genomic cassette? Please. Transcription is far more authentic on genomic vinyl
posted by theodolite at 7:00 AM on October 22, 2012 [4 favorites]


"How very intelligently designed!"

You say that jokingly, but I think the many complex and beautiful stories like this one that couldn't possibly fit into a narrative of 'everything was PERFECT until those two assholes ate some fruit' are among the strongest and most easily explained arguments against a straightfoward and simplistic creation narrative. In my last position, I was in a region where I interacted with creationists aware of agriculture a surprising amout and I usually made sure to bring up exactly this and ask how it could possibly fit.
posted by Blasdelb at 7:01 AM on October 22, 2012 [9 favorites]


Nightmare fuel.
posted by Sternmeyer at 7:01 AM on October 22, 2012


This is fascinating, thanks for the detailed, easy-to-follow description.
posted by odinsdream at 7:03 AM on October 22, 2012 [1 favorite]


These Walking Dead posts should have spoiler alerts!
posted by Skygazer at 7:03 AM on October 22, 2012 [1 favorite]


here is a brain meltingly horrific video of a dissection of the mummified aftermath 8 days later.

I've heard of these wasps before and knew what they did, but never saw a video of it so I didn't realize the relative size of the larvae. HowTF was that aphid still alive??
posted by DU at 7:03 AM on October 22, 2012


Well I'm going to go live in a completely sterile environment, who's with me?
posted by The Whelk at 7:03 AM on October 22, 2012 [7 favorites]


So, naturalists observe, a flea
Hath smaller fleas that on him prey;
And these have smaller still to bit 'em;
And so proceed ad infinitum.

posted by foleypt at 7:04 AM on October 22, 2012 [4 favorites]


And the next Scott Westerfeld vampire series just got a lot more complicated.
posted by kyrademon at 7:05 AM on October 22, 2012


"Nightmare fuel."

I'm reminded of something metaBugs once said on the green,

"Also: you need to do far, far better than talking about scabs to gross out a biologist. We can show you stuff that'll make you ashamed to be organic."
posted by Blasdelb at 7:05 AM on October 22, 2012 [7 favorites]


Man, this is like the plot of one of those epic series (e.g. Game of Thrones) where I can never keep all the characters and their ulterior motives straight. I love it when Blasdelb procrastinates on his real work!
posted by Quietgal at 7:08 AM on October 22, 2012 [4 favorites]


I am reminded of Dawkin's observation that Nature is neither good nor bad, only piteously indifferent - which sort of makes the idea that man is a creation of God and not nature not exactly a bad invention.
posted by three blind mice at 7:09 AM on October 22, 2012


Wow. Man, nature is complicated. Also, the levels of attack/defend/reattack/redefend going on are just infinitely recursive.
posted by rmd1023 at 7:09 AM on October 22, 2012 [1 favorite]


" I've heard of these wasps before and knew what they did, but never saw a video of it so I didn't realize the relative size of the larvae. HowTF was that aphid still alive??"

Don't worry, that unfortunate aphid is about as dead as dead can possibly be. The undulating creature extracted from the aphid carapace is the nearly completed wasp that just consumed the aphid from the inside out.
posted by Blasdelb at 7:12 AM on October 22, 2012


Right, I get the wriggling is the wasp larva. But from the video description: The aphid would have probably been alive for the next day until the wasp pupated...

So it must have been alive shortly before the dissection, but consisted only of a head and a wasp-containment sack.
posted by DU at 7:14 AM on October 22, 2012


This is a wonderful post. I love nature. I love how she has had billions of years, and nothing at all to do with them besides figure out ways to make more babies.
posted by agentofselection at 7:19 AM on October 22, 2012 [3 favorites]


That is a pretty odd description, perhaps by reasonably ideosyncratic definitions of alive, or referring to the wasp inside? My understanding is that the aphids slow down and are largely inert except for the wasp consuming them pretty quickly in infection.
posted by Blasdelb at 7:21 AM on October 22, 2012


I got the flu to keep my tapeworm from getting too big. I got my tapeworm to keep me from getting too big.
posted by The 10th Regiment of Foot at 7:25 AM on October 22, 2012 [1 favorite]


If there's this much complexity in the interactions between one parasitoid and their host, it's worth remembering that there are loads and loads of species of parasitoid wasp (this is just one - big - family of them), and we're finding more and more of them all the time.
posted by cromagnon at 7:26 AM on October 22, 2012


Neat. As always, brings to mind Bloodchild.
posted by Iris Gambol at 7:32 AM on October 22, 2012 [3 favorites]


Nature is creepy and disturbing, and must be cleansed with Holy Fire so that it may be made pure and worthy in the sight of God. Burn everything, my children, all must burn for the gates of heaven are opened by fire.
posted by aramaic at 7:59 AM on October 22, 2012 [4 favorites]


inception noise
posted by en forme de poire at 8:06 AM on October 22, 2012


The first author on that science paper was my Entomology professor = ). Incredible research, parasitoids deserve the world they own.
posted by Buckt at 8:06 AM on October 22, 2012


"Parasites. Why'd it have to be parasites?"
posted by The Ultimate Olympian at 8:07 AM on October 22, 2012 [1 favorite]


"inception noise"

Now in button form
posted by Blasdelb at 8:09 AM on October 22, 2012


Damn nature, you... FUCKING AMAZING!
posted by symbioid at 8:18 AM on October 22, 2012


aramaic, try bleach!
posted by echo target at 8:25 AM on October 22, 2012 [3 favorites]


There is a metaphor for Capitalism and the Worker's Revolution here. Workers of the World Unite! You have nothing to lose but Capitalist ovipositors!
posted by GenjiandProust at 8:30 AM on October 22, 2012 [2 favorites]


This makes for a really fascinatingly complex system of interdependencies for each of the agents involved. The phage, the bacterial symbiont, and the aphid are all each united in their interdependent need to combat the wasp that kills all three when it succeeds. However, at the same time, both the phage and the bacteria are dependent on the wasp to apply pressure on the aphid to keep them around - otherwise the aphid would cure itself of both creatures that would then be free-loading.
This reminds me of politics. Or interdepartmental squabbles in a giant company. And it seems like a pretty good argument to me that neither nature nor mankind's most complicated projects are "intelligently designed" by anyone at all. Which explains a lot about life, really.
posted by Western Infidels at 8:42 AM on October 22, 2012 [1 favorite]


Birds, bird-feeders, squirrels, those who put up bird feeders, and bird feeder manufacturers.

AAAHHAAAhAAAAHAAAAA
posted by seanmpuckett at 9:08 AM on October 22, 2012 [1 favorite]


Isn't there one of these wasps that feeds on BMSBs? Because I'm all about anything that'll eat those stupid, annoying pests.
posted by valkyryn at 9:13 AM on October 22, 2012


Someone explain to me why I'm less freaked out by these things than I am by Fig Wasps?

On one hand, we have evil bastards that eat their host from the inside out, leaving a brain wandering around until it finally figures out that its abdomen is hollow.

On the other hand, we have fruit flies and a fig.

But the fig wasps just freak me the fuck out.
posted by sodium lights the horizon at 9:19 AM on October 22, 2012


It's turtles all the way down...
posted by deadbilly at 9:52 AM on October 22, 2012


Someone explain to me why I'm less freaked out by these things than I am by Fig Wasps?

Hmm, fig wasps, I've never heard of those...

In figs of this sort, the crunchy bits in the fruit contain both seeds and wasps.

wat

(Still, I don't think anything compares with that emerald cockroach wasp, which bites off the tops of the cockroach's antenna and then steers it like a horse into the specially prepared death-den)
posted by curious nu at 10:24 AM on October 22, 2012 [3 favorites]


Don't be scared of fig wasps! They couldn't even sting you, and it's one of nature's best cases of mutualism.
posted by Buckt at 10:40 AM on October 22, 2012


curious nu: In figs of this sort, the crunchy bits in the fruit contain both seeds and wasps.

wat


Do we actually get figs like that in the US? Cause, I need to know if I can ever eat figs again.
posted by Mitrovarr at 11:02 AM on October 22, 2012 [1 favorite]


"We can show you stuff that'll make you ashamed to be organic."

Traumatic insemination.

Parasitic suicide.

Explosive disease transmission.

I think most of these have been featured here before, morbid lot that we are.
posted by cromagnon at 11:05 AM on October 22, 2012 [3 favorites]


Do we have any idea how the phage spreads to new H. defensa individuals? My very basic knowledge is that a phage will lyse its host to release copies of itself, and then the copies inject DNA/RNA through the cell wall of new victims. But APSE would have to somehow get outside the aphid cell as well, then get into another aphid cell before reaching another H. defensa host. Unless it only infects new hosts within the same aphid cell?
posted by vasi at 11:20 AM on October 22, 2012


Game over, man! Game over!
posted by ostranenie at 1:08 PM on October 22, 2012


Yo dawg, I heard you like fleas...
posted by ostranenie at 1:13 PM on October 22, 2012


Watching that aphid video led me to this...

Watch a Caterpillar give birth to maggots, on the INTERNET

I can't stop itching!
posted by The Power Nap at 1:58 PM on October 22, 2012 [1 favorite]


David Attenborough produced a series about insect life for the BBC not too long ago, it was full of this sort of tasteful nugget. I remember watching it from between my fingers thinking just how much it would mess with anyone's idea of a benevolent god. "There's a divinity that shapes our ends, Rough-hew them how we will," yeah, with ruthless ironic sadism if you're a wasp or a spider.
posted by glasseyes at 2:48 PM on October 22, 2012


Power Nap, I've seen that vid on here before and I'm pretty sure it's special effects, not the real deal.

this post is awesome BTW.
posted by rebent at 3:09 PM on October 22, 2012


glasseyes: that might be “Life in the Undergrowth”, and if not, LitU is worth watching anyway.
posted by hattifattener at 7:25 PM on October 22, 2012


This is a great series of posts, Blasdelb.

Wikipedia on Buchnera mentions another relationship in this web:
"Buchnera also increases the transmission of plant viruses by producing symbionin, a protein that binds to the viral coat and protects it inside the aphid. This makes it more likely that the virion will survive and be able to infect another plant when the aphid next feeds."

Hm, is it useful to the Buchnera that these plant viruses get propagated?

Also: "[Chaperonins] are overproduced in several parasitic bacteria and are implicated in at least 2 types of endocytobiosis: in amoebae and in aphids."
posted by away for regrooving at 1:28 AM on October 23, 2012


Someone explain to me why I'm less freaked out by these things than I am by Fig Wasps?

On one hand, we have evil bastards that eat their host from the inside out, leaving a brain wandering around until it finally figures out that its abdomen is hollow.

On the other hand, we have fruit flies and a fig yt .

But the fig wasps just freak me the fuck out.


Is it possible you have Trypophobia, or something related?
posted by YAMWAK at 2:29 AM on October 23, 2012


GUYS I FEEL LIKE SOMETHING IS CRAWLING ON THE BACK OF MY NECK CAN SOMEONE CHECK FOR ME PLEASE
posted by rmless at 9:24 AM on October 23, 2012


« Older Maurice Sendak's (probable) inspiration....   |   Like folk enthusiasts and fiel... Newer »


This thread has been archived and is closed to new comments