Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes

My essay with Seth Bordenstein (Symbionticism) is out in PLoS Biology.

doi: 10.1371/journal.pbio.1002226

Abstract: Groundbreaking research on the universality and diversity of microorganisms is now challenging the life sciences to upgrade fundamental theories that once seemed untouchable. To fully appreciate the change that the field is now undergoing, one has to place the epochs and foundational principles of Darwin, Mendel, and the modern synthesis in light of the current advances that are enabling a new vision for the central importance of microbiology. Animals and plants are no longer heralded as autonomous entities but rather as biomolecular networks composed of the host plus its associated microbes, i.e., “holobionts.” As such, their collective genomes forge a “hologenome,” and models of animal and plant biology that do not account for these intergenomic associations are incomplete. Here, we integrate these concepts into historical and contemporary visions of biology and summarize a predictive and refutable framework for their evaluation. Specifically, we present ten principles that clarify and append what these concepts are and are not, explain how they both support and extend existing theory in the life sciences, and discuss their potential ramifications for the multifaceted approaches of zoology and botany. We anticipate that the conceptual and evidence-based foundation provided in this essay will serve as a roadmap for hypothesis-driven, experimentally validated research on holobionts and their hologenomes, thereby catalyzing the continued fusion of biology’s subdisciplines. At a time when symbiotic microbes are recognized as fundamental to all aspects of animal and plant biology, the holobiont and hologenome concepts afford a holistic view of biological complexity that is consistent with the generally reductionist approaches of biology.

See the Vanderbilt University press release: The pronoun ‘I’ is becoming obsolete

Symbiotic bacteria appear to mediate hyena social odors

Our new paper is out in the Proceedings of the National Academy of Sciences

doi:

Abstract: All animals harbor beneficial microbes. One way these microbes can benefit their animal hosts is by increasing the diversity and efficacy of communication signals available to the hosts. The fermentation hypothesis for mammalian chemical communication posits that bacteria in the scent glands of mammals generate odorous metabolites used by their hosts for communication and that variation in host chemical signals is a product of underlying variation in the bacterial communities inhabiting the scent glands. An effective test of this hypothesis would require accurate surveys of the bacterial communities in mammals’ scent glands and complementary data on the odorant profiles of scent secretions—both of which have been historically lacking. Here we use next-generation sequencing to survey deeply the bacterial communities in the scent glands of wild spotted and striped hyenas. We show that these communities are dominated by fermentative bacteria and that the structures of these communities covary with the volatile fatty acid profiles of scent secretions in both hyena species. The bacterial and volatile fatty acid profiles of secretions differ between spotted and striped hyenas, and both profiles vary with sex and reproductive state among spotted hyenas within a single social group. Our results strongly support the fermentation hypothesis for chemical communication, suggesting that symbiotic bacteria underlie species-specific odors in both spotted and striped hyenas and further underlie sex and reproductive state-specific odors among spotted hyenas. We anticipate that the fermentation hypothesis for chemical communication will prove broadly applicable among scent-marking mammals as others use the technical and analytical approaches used here.

Nature: http://www.nature.com/news/smelly-microbes-help-hyenas-to-communicate-1.14141

Science: http://news.sciencemag.org/biology/2013/11/scienceshot-dont-blame-hyena-its-stink

National Geographic: http://newswatch.nationalgeographic.com/2013/11/11/bacteria-power-social-lives-of-hyenas/

LiveScience: http://www.livescience.com/41108-hyenas-microbe-communication.html

Original papers proposing the fermentation hypothesis for mammalian chemical communication

Gorman, M. L. 1976. A mechanism for individual recognition by odour in Herpestes auropunctatus, doi:10.1016/S0003-3472(76)80107-8

Albone, E. S., Eglinton, G., Walker, J. M. & Ware, G. C. 1974. The anal sac secretion of the red fox (Vulpes vulpes); its chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo), doi:10.1016/0024-3205(74)90069-1

Review papers discussing a more general symbiotic hypothesis for animal chemical communication

Archie, E. A. & Theis, K. R. 2011. Animal behaviour meets microbial ecology, doi:10.1016/j.anbehav.2011.05.029

Davis, T., Crippen, T., Hofstetter, R. & Tomberlin, J. 2013. Microbial volatile emissions as insect semiochemicals, doi:10.1007/s10886-013-0306-z

Foundations

Quote

So if we drop a mouse in a blender, we get more ‘bacterial’ than ‘mouse’ genomes. By a factor of nearly a hundred! This is the new wisdom. But it’s wrong. We definitely get more ‘microbiont’ than ‘macrobiont’ genomes. But the mouse is not the macrobiome. The mouse is the sum of these genomes – the holobiont expressing the hologenome – and it is that sum that contributes to the success of the mouse under evolutionary selection.

– Richard Jefferson

Nothing in biology makes sense except in the light of evolution.

– Theodosius Dobzhansky

There is grandeur in this view of life, with its several powers, having been originally breathed into a few forms or into one; and that, whilst this planet has gone cycling on according to the fixed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been, and are being, evolved.

– Charles Darwin