Is the Microbiota Species Specific? Cell paper weighs in.

A just published Cell paper, Gut Immune Maturation Depends on Colonization with a Host-Specific Microbiota, weighs in on the growing evidence that the gut microbiota is specific to a host. In this case, the study shows that non-native microbiotas, including human and rat, colonize a mouse gut, but those bacterial species do not work with the resident mouse cells to mount a proper immune response. Simply stated, you can put non-native microbes in an animal, but you dont get a fit animal back.

Highlights from the paper:

• Mouse and human microbiota differ in bacterial species, primarily within Firmicutes
• Human microbiota (HMb) colonized mice have a global immunodeficiency like GF mice
• HMb induced less T cell proliferation and activation than mouse microbiota (MMb)
• HMb mice are more susceptible to enteric and disseminated infection than MMb mic

Video link of the senior author and Harvard professor, Dennis Kasper, describing the paper:

This work contributes to an emerging body of literature that supports the hypothesis that a minor or major part of the assemblage of the OTUs in the microbiota interact with the host in a specific manner. The consequence of this specificity is that assemblages of bacteria in related species may actually change in composition over time in parallel with the phylogeny of the host species. Thus, the bacterial OTUs could be a general extension of the host's genes, and there is an evolutionary footprint in the changes in both. We saw this in Nasonia wasps (Evolution paper here) and have summarized other evidence in Box 1 of this review (Trends in Ecology and Evolution paper here).

All this makes me wonder how important symbiosis will turn out to be in speciation. If the pace of new discoveries is any indication, it is looking like the old ideas of the 80's and 90's (that symbionts do not assist speciation in any grand way) is going to be entirely reassessed.

Related Blog Posts:

• Speciation by symbiosis (April 26, 2012)
• Is the microbiome part of the organism or the environment? (May 11, 2012)

Science of a Superorganism - my article in Bare Essentials

Bare Essentials - A Free Online Magazine Promoting Life Science and Conservation:  Bare Essentials is an open access online journal that has a commitment to spreading scientific literacy along with some snazzy designs/layouts in their articles. The editor of Bare Essentials asked for a contribution on the relationships between the microbiota and evolution. The article, entitled Science of a Superorganism, is downloadable here.

BE has progressive principles that deserve giving a shot out to, including an affiliation with the Australian Zoo Wildlife Warriors, a conservationist organization that was established in 2002 by the late Steve Irwin and his wife Terri Irwin to involve and educate others in the protection of injured, threatened or endangered wildlife. From the Bare Essentials website:

"Beyond our online resources and publication, we help co-ordinate fundraising opportunities for our conservation partners inviting individuals, groups and sponsors to affiliate with and help raise awareness for preservation efforts through our Wildlife Warriors Initiative."

Spotlighting the Stories of the Microbiota: There's so much to say about the microbiota that it was impossible to cover all the work that should be covered; and there are many good articles already out there. My approach was to boil down the basics and shine the lights on the importance of the microbiota for the general audience. I included topics such as how microbes weigh over 5000x more than humans do on the planet, how microbes make you attractive to mosquitoes, how women's hands are microbial dirtier than men's hands, among others.

I also tried to pick up some of the things that my student is studying on gut microbiota and evolution. Here are two more scientific points that are touched upon towards the end of the Bare Essentials piece but dont get much real estate in the article:

1. First, the influence of gut bacteria on animal speciation is one of the major foci of our lab's research. We are studying how changes in the number and types of gut bacteria change during the process of animal speciation, and how the gut bacterial community may in fact cause speciation events by reducing interbreeding between two animal species. Recently we published a paper in the journal Evolution in which we showed that gut bacteria in closely related species of insects, Nasonia parasitoid wasps, increases in diversity over development from larvae to pupae and adults. The gut bacteria essentially becomes more diverse by colonization of new bacterial types as the insects develop, similar to what happens within humans in which an infant rapidly accumulates different species of bacteria over the course of their first year. 
2. We also test whether diet or animal genes have a more important impact on the composition of the types and abundance of bacterial species in their guts. If diet affects the gut microbiota, then by rearing closely related species on the same diet, the null hypothesis would be that all three species harbor the same types of bacteria. We did not observe this. Instead, what we observed is that when the Nasonia wasps were reared on the same diet (fleshfly hosts), the bacterial communities became slightly different in each of the wasp species; and the relationships of these slightly different gut communities between the Nasonia species parallels the relationships of the Nasonia chromosomal genes (see conceptual figure below based on findings in the Evolution paper). Therefore, we conclude that bacterial communities diverge in parallel with the wasp's genes over evolutionary time-frames that span the formation of new species. The implications are significant. In particular, a host's bacterial population is not transient or unstable. Instead, it is species-specific at some levels and likely selected for by the immune system to perform functions within the host that may be slightly different from the functions in closely-related host species. What happens to these bacterial communities in hybrids and how the bacteria affect hybrid problems such as mortality between Nasonia species is what we currently have our heads buried in.

The figure above by Robert Brucker and I shows the codivergence between the genes of the wasp on the left and their gut microbial communities on the right. The three Nasonia species differ in their wing sizes and the fleshfly host on the bottom is Sarcophaga bullata. The bolded colors on the circular trees indicate the different types of bacterial species present in the insects.

The Story Behind Our New Review: "Speciation by Symbiosis"

This post is a behind-the-scenes look at our new review, entitled Speciation by Symbiosis, by graduate student Robert Brucker and I. The review is online today in Trends in Ecology and Evolution. If anyone needs a copy, Ill happily send you one. Here are four points that motivated us to write the review.

1. The study of microbial symbionts in speciation has an interesting history: One of the central questions in evolutionary biology remains how do new species arise. What types of genes and evolutionary forces spur one species to split into two, ultimately to form the 1.8 million species on the planet? While we clearly have answers today that shed some light on these questions, debate remains about what types of heritable factors are important in promoting speciation. Specifically, these factors include two possibilities: (i) the genes on an organism's chromosomes versus (ii) the microbial symbionts that inhabit that same organism. The controversy over this topic actually began a century ago among evolutionary biologists and geneticists.  The main demarcation in the debate was best represented by two books, one of which was nearly forgotten to history and is the inspiration for the review, as well as our grant (press release) from the National Science Foundation's Dimensions of Biodiversity Program.

The forgotten book and the famous book that complements it are:

• by microbiologist Ivan Wallin - Symbionticism and the Origin of Species (1927), and 
• by geneticist Theodosius Dobzhansky - Genetics and the Origin of Species (1937)

Given the uncanny similarities in titles and the time frame of their publications, I think it is likely that Dobzhansky "copied"  Wallin's title and replaced Symbionticism (meaning intracellular symbioses with microorganisms) with the word Genetics.

A 1920 photo of Ivan E. Wallin. Wallin was a professor in the Department of Anatomy at the Univ. of Colorado Medical School, Boulder and was most well known for recognizing that mitochondria as bacteria. Credit: Archives, University of Colorado at Boulder Libraries. Colorado, U.o. (1920) Junior Class. In College of Liberal Arts, Univ of Colorado, Boulder.

2. Ivan Wallin's Hypothesis Was Ahead of His Time: Wallin’s central thesis was that the universality of bacterial-derived organelles (i.e., mitochondria) reflected the importance of bacterial symbionts as building blocks of evolutionary change and ultimately new species. Despite Wallin’s effort to put microbial symbiosis into the mainstream of evolutionary biology in the early 1900's, it was Dobzhansky’s work that would have a lasting influence. From the Biological Species Concept to the Dobzhansky-Muller-Bateson model of postzygotic isolation, Dobzhansky et al laid a solid foundation for the study of the genetics of speciation. Experimental and theoretical investigations of symbiont-assisted speciation were far and few between as speciation genetics took off in the 80's and 90's by many science idols of mine.

 

3. Today's biotechnology and thinking are up to the task: With the advent of high throughput sequencing techniques that make the identification of bacterial symbionts simple, and today's recognition of microbial symbiosis as a requirement for complex eukaryotes, Wallin’s ideas on the symbiotic origin of species are primed for a full reassessment. Indeed, the emergence of the bacterial symbiont Wolbachia in topical discussions of speciation (book chapter) was a beginning to reviving Wallin’s silenced ideas. The emerging story supported by the latest science in our review is that biologists have even farther to go with symbiont-assisted speciation. It appears to be almost a given that studies of the general microbial community of animals and plants will reveal even grander ways in which microorganisms act as causative agents of their host's speciation.

  

4. A new phase in the study of symbiont-assited speciation is happening now: Our article begins begins with a rich, historical controversy in evolution and genetics. Where that debate goes in the future is up for scientific discourse and experimentation. Rob Brucker (@liveinsymbiosis) and I suggest in the review that the current evidence for symbiont-induced speciation is far more solid than many speciation geneticists appreciate, and a new phase of speciation by symbiosis is likely to spur many exciting new insights.

We suggest that as studies of microbe-assisted speciation march forward, Ivan Wallin should be recognized for his pioneering and imaginative work on the microbial basis of speciation. Here is arguably his greatest quote:

“It is a rather startling proposal that bacteria, the organisms which are popularly associated with disease, may represent the fundamental causative factor in the origin of species.” (Ivan E. Wallin, 1927)