A Bug in a Bug in a Bug

by Elio

A mealybug, Planococcus citri. Mealybugs are so
called because they’re covered with a white powdery
substance. Source.

Rattling around inside my head for some time has been the reported discovery that there are bacteria that live within other bacteria. To me, this is an honest-to-goodness gee-whiz piece of microbial lore. Made me wonder why the story had not been followed up on. Could be because you have to go to mealybugs to find these eccentrics. But now I'm happy to report that someone has. A recent paper by the discoverer of this phenomenon, entomologist Carol von Dohlen, and the endosymbiont expert John McCutcheon has the tantalizing title of An Interdependent Metabolic Patchwork in the Nested Symbiosis of Mealybugs. Note that this blog is especially receptive to the allure of parasites within parasites (the ‘nested parasites’ or matryoshka dolls). As evidence, see also other of our stories about endosymbioses with complex metabolic relationships (click here and here).

Artificially colorized TEM of Planococcus citri
bacteriocytes. Tremblaya cells are colored dark
blue, Moranella cells are red, the mealybug cyto-
plasm is grey, and the mealybug nucleus is green.
Bar = 2.33 μm. Source.

First the players. The insect in question is the citrus pest mealybug, Planococcus citri. Like aphids and other insects that feed on the amino-acid poor phloem sap of plants, mealybugs require endosymbiotic bacteria to provide them these essential nutrients. They carry these working partners in the cytoplasm of specialized cells, the bacteriocytes. As for the bacteria, the ‘host’ is β-proteobacterium Candidatus Tremblaya princeps, called Candidatus because it cannot be grown in the lab. Its name won’t be italicized until this rule changes. It better, because T. princeps (I use italics in defiance) will never be able to grow independently as it has the smallest of all known cellular genomes: 139 kb. Living inside of it is the newly named γ-proteobacterium, Moranella endobia (also a ‘candidatus,’ but we’ll dispense with that.) The genus name honors the famed endosymbioticist Nancy Moran. The host Tremblaya cells are quite large, 10-20 μm wide; nested within are the Moranella, each 3-6 μm long and with a Gram-negative-like double membrane structure. Moranella has the audacity to possess a genome about four times larger than that of its host, a case, ostensibly, of genomic chutzpah.

Source.

The Tremblaya genome is really scrubby and lacks genes that one would think essential, such as those encoding aminoacyl tRNA synthetases (a first among bacteria!) and release factors. No way will it ever be coaxed into making colonies on agar plates. To survive, such a cell depends on other genomes, including here that of its endosymbiotic partner. Although Tremblaya devotes some 22% of its genome to amino acid biosynthesis, it does not have the genes for any complete pathway. Many of the missing genes are found in the Moranella, which doesn’t have the genes for entire pathways either. So, these genomes must work together. For example, the synthesis of tryptophan and threonine requires genes from both bacteria. In addition, pathways for phenylalanine, arginine, and isoleucine synthesis may require genes from the mealybug as well. An example of the chemical Ping-Pong being played here: compounds in the tryptophan pathway shuttle from Tremblaya to Moranella at three distinct steps, being passed of necessity back to Tremblaya twice in between. When it comes to getting the job done, it seems that having the genes in two physically-separated genomes matters little. Having the two cytoplasms nested makes for the easy and fast exchange of metabolites. The least we can say about this business is that the metabolites that move back and forth won’t be lost to the surrounding mealybug cytoplasm.

Now for the big picture. Endosymbioses come in all sorts of surprising variations. Some bacteria live inside mitochondria (former bacteria), others reside within nuclei, and some share their host with another bacterial partner. But in most of the known cases of dual endosymbionts of insects, each symbiont on its own contributes to the host a growth factor, be it an amino acid, a fatty acid, or a vitamin. In one case we described recently, the genes for tryptophan biosynthesis were also divvied up between two (not nested) endosymbiotic bacteria and each does only part of the job. But the Tremblaya/Moranella duo goes further than that. How do the intermediates get exchanged? Is there a set of sophisticated transport systems? A search for transporter genes in the two bacteria was only partly successful for Moranella and totally unsuccessful for Tremblaya. I’d dearly love to know what is going on in that ‘periplasm.’

Now that you have swallowed all this strangeness, you might well ask if we are talking about endosymbionts or about organelles. Tremblaya’s reduced genome falls within the size range typical of mitochondria and plastids. As Patrick Keeling points out in a commentary accompanying the paper, organelles are known to share biochemical pathways between them in much the same fashion as in the story here told. For instance, in some apicomplexan protists, heme is made partly in the mitochondria, partly in the non-photosynthetic plastids, and perhaps partly in the cytosol. So, what is news for the bacterial symbionts is old hat in the world of organelles. Is there a message somewhere?

What are the next experiments you’d like to see done with these mealybug bugs?

McCutcheon JP, & von Dohlen CD (2011). An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Current Biology : CB, 21 (16), 1366-72 PMID: 21835622

Comments

[Blind Bat]

wow, who would have thought there was so much going on with bacteria!

[Randall Flagg]

Even after reading the original article, I don't think I do understand the difference between these and organelles? Aside from "prokaryotes aren't supposed to have them." (...so they promptly turn around and have some, just to show the futility of taxonomic rules in microorganisms.) If these get proclaimed a species, does that mean mitochondria are ("Still?") as well?

Gotta love organisms that break the rules.

You correctly point out the problem with trying to neatly distinguish bacterial endosymbionts and organelles. One could argue that the two look different in EM thin sections or in other ways, but not enough work has been done to make this into a serviceable distinction. I see two possibilities: A. the two will turn out to be distinct by some set of criteria yet to be fully worked out, or, B. there is a continuum from typical organelles to typical bacteria. At this time, I think it's up in the air. But we'll agree, won't we, that the subject is fascinating, right?
Elio

[Nathan Fisher]

"What are the next experiments you’d like to see done with these mealybug bugs?"

Can this system of interdependence be targeted for pesticide action? And if so, would resistance emerge less frequency than for other pesticides?

[Panic Attacks]

Such an interesting article about bacteria. Living inside, within, and partnering with other bacteria - it's no wonder that they have the ability to reproduce so fast.

I am no expert when it comes to these matters but reading your blog does help me learn more about things that are very interesting. Thank you for sharing.

[allen laskin]

Since Thanksgiving is not too far away, this post made me think of "turducken." See http://en.wikipedia.org/wiki/Turducken

Allen Laskin

[John Ireland]

I have to admit that I linked to this article right away, we are covering endosymbiosis in my General Bio class right now and these are great examples of this underappreciated way of life.

[Alex Wild]

"What are the next experiments you’d like to see done with these mealybug bugs?"

As an ant guy I'd take a look up a trophic level, of course. Ants that depend heavily on honeydew often have their own endosymbionts (like Blochmannia in carpenter ants), and it may be possible for the symbioses inside the mealybug to have consequences as far away as the gut ecology of honeydew-feeding insects.

Learn something new every day. Many thanks.

Elio

[Barry]

Right on! genomes are not islands. This reminds me of Elysia chlorotica (I think you posted a blog entry?) who is born with genes from Vaucharia's nucleus, in its own nucleus to help its acquired Vaucharia chloroplasts to produce chlorophyl becuse the chloroplasts no longer have all the genes for it.

and i recall we were having a discussion about how this evolves because the proteins need tags to guide them across membranes but at some point they have to travell in the opposite direction if their genes transfer to another host.

all very confusing.

Speaking of Matrayoshka, i'm reminded that we've found that a host of eukaryotes are nested inside each other: there is a dinoflagelate which contains remains of a haptophyte which contains remains of a rhodophyte which contains remains of a cyanobacteria!

from "Tracing the Thread of Plastid Diversity through the Tapestry of Life", Charles F. Delwiche

"The best case for a true tertiary
plastid is in the fucoxanthin-containing dinoflagellates
Gymnodinium breve, Gymnodinium galatheanum, and Gy-
rodininium aureolum. In these taxa the plastids have both a pigmentation and ultrastructure reminiscent of the plastids of haptophytes (or “coccolithophorids”), a group ofmarine algae with calcareous scales that have secondaryplastids. A recent molecular phylogenetic study has confirmed that these plastids are derived from haptophytes (T. Tengs, O. J. Dahlberg, K. Shalchian-Tabrizi, C. Delwiche, D. Klaveness, K. Rudi, and K. S. Jakobsen, unpublished manuscript), and as there is no evidence of a nucleomorph or other endosymbiont nucleus, these plastids seem to be true tertiary organelles."

Now it would be great if some of these Gymnodinium were zooxanthellae in other organisms or if the zooxanthellae also contained Haptophyte matryoyoshka. this article suggests to me that it's possible:

http://www.redorbit.com/news/science/8568/comparison_of_phylogenies_based_on_nuclearencoded_ssu_rdna

what fun! I knew back in high school that Margulis was onto something