It’s all because of the holobiont

It’s conference season at the Molecular Ecologist. I went for the first time to a Gordon Research Conference (GRC). GRCs @GordonConf are well known for their efforts to foster an informal and inclusive atmosphere where frontier research in the biological, chemical, physical, and engineering sciences is discussed. Isolated venues and long breaks in the afternoons promote networking and give room for social activities and breakout sessions. Researchers are encouraged to present unpublished results and the contributions are off-record, that means that nobody is allowed to take photos, record sound or video, or share the presentations on social media. And here I am writing about it.

I attended the Animal-Microbe Symbioses Conference #GRCAnimalSymbioses. I went first and most of all because of the incredible line-up of presenters (almost 50% women). Second, I’ve heard that Gordon Research Conferences are especially family-friendly. I was not disappointed.

The subject-specific GRC on Animal-Microbe Symbioses was held the first time in 2015 with the subtitle ‘Identifying the Common Language of Host-Microbe Associations’ and chaired by Nicole Dubilier, the director of the Symbiosis Department at the Max Planck Institute for Marine Biology in Bremen, Germany. Next was Edward (Ned) Ruby, chairing the meeting on ‘Host-Microbe Associations at the Foundation of the Biosphere’ in 2017. More about Ned and squid and their wonderful symbioses at the Molecular Ecologist here. Hence, we were already attending the third meeting of a very successful sequence this year, chaired by Ute Hentschel and Angela Douglas on ‘Animal-Microbe Symbioses as Nested Ecosystems’. I am not going to share any unpublished results here but let me report on some exciting highlights of the conference.

What are nested ecosystems? During the very first session we learned that nature is made up of systems which are nested within systems (I am quoting Nicole Dubilier who moderated). Symbionts are nested within hosts, which are nested within communities, which are nested within ecosystems. The ultimate goal is to find out how individual parts interact, connect, and communicate with each other and with everything else. I cannot get the dancing yeti crabs out of my head that Shana Goffredi showed us:

Safety dance

Why are they doing that? They live in a cultivation mutualism (Watsuji et al. 2017)! If you put crabs in the lab on a shaker after they have died, their microbes will be just as happy as the ones living on the live dancers…  Jillian Petersen taught us that lucinid clams eat with their lungs, breathe with their skin, smell with their foot, and live upside down. Check out some of her cool outreach cartoons here! Do not suppose that we only discussed marine symbioses. We also heard about cutting edge symbiosis research on drosophila, ants, C. elegans, Paramecium (why do they have such a cute name in German?), placozoans, birds (there were enough bird researchers for a spontaneous breakout group), aphids, frogs, salamanders, bees, and many more. The very last session of the conference was reserved for Microbial Therapy, in other words, how to use microbiology for conservation, led by Raquel Peixoto, the master of heroes. She introduced all the speakers of her session as superheroes fighting hard to save their endangered host species. Jens Walter showed us an ecological perspective on how to modulate gut microbiota. Sean Leonard gave us some insight (and hope) how to help honey bees. Engineered symbionts can trigger RNA interference to protect honey bees from viruses and parasitic mites. The meeting was concluded by a mindblowing talk by Douglas Woodhams on how to use natural, skin-associated bacteria to help amphibians survive chytrid fungus disease outbreaks in the wild. After a massive die-off, some populations in Panama are recovering and seem to be more resistant than before the disease outbreak. Douglas and his team collected more than 7000 isolates of skin-associated bacteria with antifungal properties! A whole army of superheroes!

Photo taken and copyrighted by Dr. Benedict Yuen yuen@microbial-ecology.net
during our expedition in Costa Rica in March 2019

While it seems that some old and new concepts are helping us make breakthroughs in animal conservation, some other terms left me wondering. Many people at the conference were loud about holobionts. I felt a bit lonely and unconfident about speaking up. I could not fully grasp what the terms holobiont and hologenome mean and how they help us advance in science. While still at the conference, I organized a meeting at UC Davis to discuss the usefulness of these terms. What do these terms mean? When and why should we use them?

Seth Bordenstein has adopted the terms holobiont and hologenome (as well as phylosymbiosis, that I am not going to discuss today). He offers definitions and discussions of the terms on his blog. In brief, a holobiont is defined as the host and all of its microbial symbionts, including transient and stable members (Bordenstein and Theis 2015). Hologenomes are then defined as the genomes of all the taxa in the holobiont. Holobionts and hologenomes are single units of biological organization. This has then significant implications for host ecology and evolution. Hologenomic evolution is most easily understood by equating a gene in the nuclear genome to a microbe in the microbiome.

Figure 1 in Theis et al. 2016: https://msystems.asm.org/content/1/2/e00028-16

Seth Bordenstein and Kevin Theis’ publication has stirred up the community and resulted in a lively discussion. See some of the responses by Jonathan Eisen here, by Nancy Moran here, and by Angela Douglas here. I went back and found the term holobiont had been mentioned in an article by David Mindell in 1992 (Mindell 1992). He states that holobionts result from ancient symbioses of reticulate evolution; i.e., two species that merged (for example early eukaryotes incorporating mitochondria). This represents a form of merging that is different from interspecific hybridization. Then, I found a few more mentions, mostly in the coral and sponge community. For example, Forest Rohwer wrote a paper with Nancy Knowlton and others where he introduced the term holobiont in a figure to represent the coral animal, its associated zooxanthellae and bacteria as one unit, including also associated fungi, protozoa and algae (Rohwer et al. 2002).

I was leading the discussion on the subject about a week after the GRC meeting, but I was late that morning so my husband had to drive me to work by car to make the meeting on time. This spousal service caused us serious trouble (more about this later). The meeting itself was lively and enlightening. Would you call the community living on a tall tree (in the tropical rainforest) that is providing home to epiphytes, birds, ants, and mammals, that is pollinated by bats, and whose seeds are dispersed by agoutis a holobiont? This question came from Sonia Ghose, Ph.D. candidate in the Population Biology graduate group at UC Davis. She hit the nail on the head. A host and its associated microbes (microbiome) is more effectively viewed as an ecological community of organisms, each with its individual interests creating a broad range of interactions (from parasitic to mutualistic), patterns of transmission (vertical, horizontal), and levels of fidelity. If the whole community is to evolve as a unit, this would require high partner fidelity and synchronized mode of reproduction. As Douglas and Werren point out in 2016 (Douglas and Werren 2016): ‘We believe that the concepts and methods of ecology, genetics, and evolutionary biology will continue to provide a well-grounded intellectual framework for researching host-microbiome communities (…).’

Whale holobiont taken from
https://f1000research.com/articles/7-1664/v1

At the GRC, Brendan Bohannan talked about host microbiomes as metacommunities and how to use metacommunity ecology in microbiology to understand where the variation of microbiomes across hosts comes from. The host can be understood as a patch of habitat, and dispersal brings in new bacterial members. Some are lost with drift, and ecological selection sorts out the others. The whole results in a huge matrix where we find ourselves.

Many of the critics of the holobiont as a useful ‘new’ term in ecology and evolution were at the conference. I was not alone. They were just very quiet. I guess this conversation is not over yet. And yes, Gordon Research Conferences are very family-friendly. While I was nervous at first about schlepping my whole family to a forest in New England, they had a blast the whole week. Lots of family-friendly activities, outdoors, healthy food, and promises from other researcher parents that they will bring their families along next time.

References:

Bordenstein, Seth R., and Kevin R. Theis. 2015. “Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes.” PLoS Biology 13 (8): e1002226.

Douglas, Angela E., and John H. Werren. 2016. “Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts.” mBio 7 (2): e02099.

Mindell, D. P. 1992. “Phylogenetic Consequences of Symbioses: Eukarya and Eubacteria Are Not Monophyletic Taxa.” Bio Systems 27 (1): 53–62.

Rohwer, F., V. Seguritan, F. Azam, and N. Knowlton. 2002. “Diversity and Distribution of Coral-Associated Bacteria.” Marine Ecology Progress Series 243: 1–10.

Watsuji, Tomo-O, Remi Tsubaki, Chong Chen, Yukiko Nagai, Satoshi Nakagawa, Masahiro Yamamoto, Daisuke Nishiura, Takashi Toyofuku, and Ken Takai. 2017. “Cultivation Mutualism between a Deep-Sea Vent Galatheid Crab and Its Chemosynthetic Epibionts.” Deep Sea Research Part I: Oceanographic Research Papers 127: 13–20.

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