Friday, October 18, 2013

Guest Blog Post On The Story Behind A New Phylosymbiosis Paper

Below is a guest blog post by Soeren Franzenburg (Twitter: @naturfokussiert) who recently migrated from Kiel/Germany to do a postdoc at Cornell University on animal-microbe symbioses in Angela Douglas' laboratory. When Soeren's paper came out, my jaw dropped to the table. Without hesitation, it is one of the best papers that I've read all year. It is a major contribution to an emerging theme in biology that the host genome, and specifically the immune system, "farm" the microbiome from the environment in specific ways. Hat tip to Greg Hurst @TheLadybirdman for the analogy of hosts farming the microbes from the heterogenous environment into their bodies.

If you're interested in microbial ecology, microbiomes, evolution, immunity, the hologenome concept, speciation, phylosymbiosis and more, this story is one you want to keep up on.  I have also gotten to know one of the senior authors on the paper, Thomas Bosch, over the last few months. It seems that conferences in evolutionary biology, the microbiome, or symbiosis might want to capture this emerging theme with a symposia on the genome-microbiome interface.

Finally, if anyone wants to write a guest blog post on the story behind their recent publication, do not hesitate to get in touch and we'll set it up.

The story behind: “Distinct antimicrobial peptide expression determines host species-specific bacterial associations”

Seth asked me, if I would like to write a guest blog post about my paper “Distinct antimicrobial peptide expression determines host species-specific bacterial associations” which was recently published in PNAS. Since the job of a scientist should not only be to perform research, but also to communicate science to a broader audience, I gladly accepted this challenge.

Picture of Hydra (Source: Wikipedia)
In this publication, we investigated the mechanisms underlying the assembly of bacterial communities associated with seven closely related species of the freshwater cnidarian Hydra.

It became increasingly evident in the past years that bacterial associates are essential for the host’s health, as supported by severe fitness disadvantages in axenic or certain gnotobiotic animals. As a consequence it would be advantageous for a host to actively select for suitable bacterial associates and maintain a defined host-bacterial homeostasis. This ability should be genetically fixed in the host’s genome. If the host’s genotype matters for microbiota composition, closer related host species should be colonized by more similar bacterial communities compared to distantly related species. This recapitulation of host phylogeny by microbiota compositions was recently termed a phylosymbiotic relationship.

However, besides host phylogeny, diet was shown to be one major determinants of microbiota composition in the wild and distantly related species with similar lifestyles can show convergence in their microbial communities. That is why observing phylosymbiotic host-microbe relationships and investigating the underlying host-mechanisms relies on studies with closely-related host-organisms and very well controlled environmental conditions, including diet. These issues were also discussed recently in a scientific Google+ Hangout, organized by Seth.

In our recent paper, we were able to show phylosymbiotic host-microbe relationships in seven species of the freshwater cnidarian Hydra. The studied species were separately reared in simple, water containing plastic-dished for up to 30 years under identical environmental conditions, including standardized diet. Nevertheless, their microbial composition differed substantially and revealed a highly phylosymbiotic pattern. Impressively, after three decades of identical cultivation, each species still maintained its specific, bacterial fingerprint.

Subsequently, we were able to pinpoint a group of species-specific antimicrobial peptides, called arminins, as critical determinants of the microbiota assembly. When axenic Hydra polyps were inoculated with bacterial communities characteristic for different Hydra species, the recipient host selected for bacterial taxa resembling its native microbiota, just like in an elegant reciprocal microbiota transfer experiments between zebrafish and mice conducted by Rawls et al. (2006). However, arminin loss-of-function polyps significantly lost this selective potential and ended up with untypical bacterial communities. When inoculated with their native bacterial colonizers, control- and arminin deficient Hydra were colonized equally, indicating that the species-specific microbiota is partially resistant to the antimicrobial peptides expressed by its host. Thus, the host’s immune system indeed plays a major role in selecting the bacterial associates. Since Hydra is a phylogenetically old organism, these observations are likely to be valid for more complex animals as well.

The paper ends with a short perspective on the role of symbiosis in speciation. Several studies have shown that the microbiota can act as a “metabolic organ”, allowing the host to feed on otherwise insufficient diet. For example, the symbiotic bacterium Buchnera provides its aphid host with essential amino acids, allowing the utilization of nutrient poor phloem sap as food source. Generally, changing the microbial partners can confer new traits to the host much faster than evolution of the host genome alone. These traits might open a new ecological niche and thus accelerate sympatric speciation.

The crucial question is: How do animals change their microbial partners? Our publication indicates that changes in fast evolving antimicrobial peptides are sufficient to drastically alter host-associated bacterial communities. Coupling fast evolving genes with the adaptive potential of changed bacterial partners could be a potential promoter for speciation.

Congrats to Soren et al for such a wonderful piece of symbiosis work.

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