The Opposing Thumb

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Cretaceous Cooperation Continues

The Cretaceous, 145 to 66 million years ago, marks the definitive end of what used to be called the Age of Reptiles. Asteroid, superflu, volcanoes (super or just lots of regular)- something bad happened, and an estimated 75% of all living species disappeared. Martin Kaltenpoth and colleagues at the Max Planck Institute for Chemical Ecology in Jena have now identified a symbiosis between a group of hunting wasps and a genus of antibiotic producing bacteria that has survived the planet’s most famous mass extinction event, and continues to thrive.

The European Beowulf.

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The (marginally less threatening) European beewolf, a.k.a Philanthus pulcherrimus.

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© Martin Kaltenpoth, MPI Chemical Ecology.

Female beewolves sting and paralyze honeybees, and then drag them into nests dug in the sand or loose dirt, where individual brood cells hold one to six helpless, soon to be dead, bees. The trouble with these warm, humid subterranean nests is that they provide an ideal environment for mould formation. The beewolf thus faces the same problem as hunters, cooks and cannibal serial killers have struggled with before the advent of refrigeration: how to keep prey fresh. The paralyzed bees cannot rot during the eleven-day larval maturation period. The beewolf solution is the biological equivalent of saran wrap, as the mother embalms the dead or dying bee in a secretion that does not exhibit direct anti-mould effects, but by tightly wrapping the helpless bee, keeps humidity off the surface and thus blocks fungal growth.

A trickier problem is protecting the cocoons larvae spin, within which they will undergo metamorphosis. These must remain in the underground nest as long as 9 months, often including a lengthy winter diapause (hibernation). As the old saying goes, mouldy cocoons do not happy young beewolves make. Kaltenpoth, then at the University of Regensburg, had shown that Mamma wasp solves this problem by investing in a significant home improvement project.  After digging their nests, females extrude bacteria through their antennae, and proceed to paint the brood cell ceiling with them. Larvae then pick up the bacteria and incorporate them into the cocoons they spin.  The weaving of this bacteria rich secretion into the cocoon fabric effectively staves off fungal growth.  A detailed analysis of the protective symbionts indentified them as members of the Streptomyces, a family of Actinobaceria that is the source of over two thirds of the antibiotics currently used in the clinic. So it was not exactly a stretch to postulate that they would perform a similar function in the wasp cocoons and subsequent work led to the purification of nine separate compounds that directly blocked fungal and bacterial growth. A rolling stone gathers no moss, neither does an immobile cocoon soaked in antibiotics gather any mould.

In their latest work, the Kaltenpoth group has characterized the evolutionary history of this relationship. The three genera of beewolf, Philantus, Trachypus, and Philanthinus, all harbour closely related symbiotic Streptomyces bacteria, indicating that this cooperative arrangement is quite old. The same closely related group of Actinobacteria are found in association with beewolves over a wide geographic range, from Germany to the Ukraine, indicating a symbiotic relationship stable over space as well as time. What’s more, the presence of specialized structures in the wasp antennae for housing and then extruding the beneficial bacteria also attests to a long association- long enough for this intricate morphological adaptation to take place. In fact, detailed phylogenetic analysis points to an origin dating to sometime between 145 to 68 million years ago.

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Co-phylogenetic analysis of beewolf and Streptomyces diversification (from Kaltenpoth et al, 2014).

Actinobacteria in the soil giving rise to strains that colonize animal hosts is in no way restricted to the curious lives of hymenopterans, or to mutually beneficial arrangements- Mycobacterium tuberculosis, which kills 3 people every minute and currently inhabits an estimated one third of humans, most likely got its start as a mammalian pathogen in a similar fashion. The intriguing co-evolutionary pattern seen in the beewolf-Streptomyces symbiosis is that, to quote lead author Martin Kaltenpoth,  it “(…) indicates that while beewolves occasionally replace their bacteria, they always do so with the symbiont of another beewolf species.”

The wasps thus show a mixture of vertical and horizontal transmission of symbionts. Co-diversification of vertically transmitted symbionts and hosts are conceptually easy to understand for associations with intra-cellular bacteria, as seen with Wolbachia and their fruit fly hosts. But how have the wasps achieved this fidelity of transmission of an extra-cellular symbiont across generations, for 70 million years? Stable vertical passage of Streptmyces is guaranteed by the eclosing adult females ingesting bacteria from the cocoon casing as they are leaving it. But the phylogenetic analysis also clearly shows that horizontal transmission- in this case the passage of symbionts from related host species also occurs, though when and how this takes place is not clear. Just as fascinating, abundant soil Actinobacteria, potential opportunist piggybackers, are kept out of the cocoon altogether. This is even true when the females are experimentally colonized with non-symbiotic species that are able to survive in the antennal glands. Somehow the opportunistic bacteria are kept out of the gland secretions, and do not make it to the cocoon. How this specificity is achieved is a mystery. Immune mechanisms? Spacial segregation in the different gland compartments?

Keep your antennae up (apologies, that more or less wrote itself) for more news on the ancient affair of the wasp and the microbe.

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