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The purpose of this blog is to provide perspectives on and information about symbiotic systems, to increase the awareness of these symbioses in the general public, and to engage readers in conversation and dialog.  We encourage the participation of the International Symbiosis Society's membership in crafting blog posts and/or suggesting topics to cover.  If you would like to become a contributor, or would like to nominate someone, please email the vice president for the website or the webmaster.
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  • 12 Mar 2014 8:58 AM | Anonymous

     

    by Nicole Gerardo (lab link)


    For the past year and a half, I have had the fortune to learn from a great teacher. She did not teach me the difference between adaptive and innate immunity, or how to do a headstand in yoga, or how to make a soufflé. She instead reminded me of the beauty of our discipline, and she inspired me to expect more from my students.


    Over the course of the last four semesters at Emory University in Atlanta, Georgia, I have worked alongside Diane Kempler, who teaches ceramics to undergraduate students. We began a collaborative effort to incorporate scientific concepts into the ceramics studio. In the first semester, I taught the students about basic concepts of symbiosis and exposed them to images of many of the natural systems that symbiosis researchers eventually begin to consider routine. Yes, it’s true that squid actually glow. Yes, it’s true that fungus can infect an ant’s brain. Yes, it’s true that there are solar-powered sea slugs. Wait, what is routine about any of this? What we study, in the eyes of art students, business majors and undergraduates who thought ceramics would be an “easy A” can inspire awe. Students have made pieces based on coral symbioses, where the dinoflagellate symbionts are now on the outside, remaining hidden no more. They have made totem poles of aphids and bacteria and lichens -- so, so many lichens. It turns out ceramics is a perfect medium for making the delicate lichen layers. Who knew? I certainly did not.


    We have expanded the breadth of the scientific focus to include partnerships between student artists and scientists on campus. Other assignments have focused on microscopic images, with students starting in the introductory biology laboratory and ending up in the studio near the kiln. For the final assignment of this semester, we are delving into public art. Students are making pieces to be placed in a local community garden. The assignment is to make the unseen world of the garden seen to the many garden visitors who walk unknowingly amongst a complex microscopic world.


    Assessment of whether the students are learning science has been difficult as they are coming into this experience with extremely diverse knowledge bases. Many students, however, have had the opportunity to appreciate some aspect of the natural world that they had not been exposed to before. My hope is that they also appreciate the practice of science that underlies that knowledge.


    Unfortunately, Emory University is closing its Visual Arts Department, making this a piece of reflection rather than a starting point. However, there is much to take away from this and to build upon. Recently, Diane herself has created a whole series of pieces inspired by cordyceps fungi. In my mind, these pieces represent one of the finest legacies of this experience. And, I have changed my own teaching in the biology classroom in subtle ways. Diane entices her students, many of whom have never touched clay before, to work hard, to learn and to create works of art. These students, when pushed, find abilities that they did not know they had. I can strive to do the same for my students as well.  



    Above and left, living lichens; Above and right, artwork by Emily Pardue incorporating lichens.


    -------------------------------------------------------


    Nicole Gerardo is an Assistant Professor in the Department of Biology at Emory University. Her research focuses on the evolutionary ecology of interactions between microbes and their insect hosts.

  • 07 Oct 2013 3:39 PM | Anonymous

    by Seth Bordenstein (lab and blog)

    ----------------------------------

    View From 32,000 Feet


    Darwin and the 20th century pioneers of biology would have been astonished to see the countless roles that microbes play in shaping eukaryotic life. From the origins of eukaryotic cells to pharmaceutical products, Life as we know it would be unrecognizable without microbes. Integrating microbes into all facets of the life sciences today is a vision that is not only driven by exciting questions at the perimeters of the biological disciplines, but one that seems more achievable today than ever before, at least from a our vantage point within the symbiosis field.


    Let us briefly look backwards in order to look forwards. The fusion of evolutionary biology and Mendelian genetics spurred a modern synthesis in which the biologist sees the world through a refined set of filters: the genome is stably inherited, subject to natural selection, and defines who we are as individuals and how species arise from descent with genetic modification. Yet there is a transformation occurring today in our capacity to understand who we are beyond our nuclear genes. Indeed, biologists take the archetypal examples of mitochondria, chloroplasts, and endosymbionts for granted, but the science of the microbiome has emerged in the last decade to massively widen the recognition, if not scope, of Life's dependency on microbes. One luminary in our field lost to history, Prof. Ivan E. Wallin, remarked in 1927:

    "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"

    Below I will summarize our most recent foray into speciation by symbiosis. This post is far too small to give a full and fair treatment of the topic, and I apologize to my colleagues in advance for not citing their work.


    From Many Genes and Microbes, One Species


    Approaches to studying the gut microbiome in animals have largely been diet- and disease-centric. Relatively little is known about the comparative structure and evolution of bacterial communities among closely-related host species, but this knowledge gap is starting to change. For instance, as speciation events progress from incipient to complete stages, does divergence in the composition of the host-associated microbial communities parallel the divergence of the host's nuclear genes? (Brucker and Bordenstein 2012a link) We hypothesized that if host phylogenetic relationships, in part, structure gut microbial communities, then related species of animals reared on the same diet will not acquire the same microbiome, but instead host species-specific communities of microbes. We discovered that the gut microbiome was indeed different between closely related species of insects reared on the same diet, and the constituents and composition of the bacterial communities in each species changed in parallel with the genomic relationships of the host species (Brucker & Bordenstein 2012b, link) - a pattern we have since termed "phylosymbiosis" (Brucker and Bordenstein 2013 link, and Figure 1 below).The significance of phylosymbiosis is also evident in primates (Ochman et al. 2010, link) and hydra (Franzenburg et al. 2013, link).




    Figure 1.Phylosymbiosis. Like phylogenomics, phylosymbiosis is a total microbiome metric that retains an ancestral signal of the host's evolution. (a) The central prediction is that divergence in host genes is positively correlated with differentiation of the microbiome. (b) Parallel dendrograms between the host phylogeny and the microbiome relationships is one test of phylosymbiosis (c) Schematic of a real data example from our model study system.



    We recently tested the hypothesis that the gut microbiome assists animal speciation, even in the well-studied Nasonia genus where nuclear speciation QTLs were genetically mapped to chromosomes. First, we demonstrated that gut bacterial diversity in F2 hybrids goes markedly awry in comparison to that of pure species controls (Bordenstein and Brucker 2013, Science, link). Second, curing this altered gut microbiota eliminated hybrid lethality (Figure 2), the misexpression of immune genes associated with hybrid lethality, and marker ratio distortions away from Mendelian inheritance for speciation QTLs. Finally, we recapitulated hybrid lethality in germ-free hybrids by orally inoculating them with resident strains of the dominant bacteria within species. Thus, in a series of "gain" and "loss" microbiome experiments, we demonstrated that reproductive isolation in this genus is not dependent solely on genetic divergence, but also on the interactions between the host genome and gut microbiome. It is enticing to speculate that this phenomenon will be common in animals since they all have a gut microbiome that is increasingly seen to affect numerous aspects of fitness. Time and experimentation will tell. A simple experiment would be to test if hybrid inviability can be cured in diverse germ-free systems.


    Speciation by symbiosis has been subject to healthy skepticism. For example, one interpretation of the data above is that the gut microbiome is just an environmentally conferred stress on the wasps’ fitness, and hybrids are hyper-susceptible to this stress. So the presumed stress of microbiome colonization on hybrid wasps can be compared to a predator eating hybrids more than the vigorous parentals that escape predator detection. However, in this argument, the microbiome is seen as purely extrinsic to the host. Like all metazoans, Nasonia's gut microbiome is inevitable and plays a large beneficial role in host fitness - survival and reproduction. Thus, removal or suppression of the microbiome in Nasonia is quite maladaptive, causing a ~15% decrease in survival from egg to pupal stages (Brucker and Bordenstein, 2012, link) and delayed development into adulthood by two to three days. Thus, in contrast to an extrinsic predator, the narrative here is that microbiome is essential for within-species fitness. Similar to a beneficial set of genes, the microbiome is also causal to reproductive isolation in hybrids, much like the way a classical geneticist studies speciation genes that are adaptive within species but break down in hybrids.




    Figure 2. Hybrid lethality in Nasonia. Top: Non-hybrid 3rd instar larva. Bottom: Hybrid 3rd instar larva that is melanized and dead.


    The Gravity of Symbiosis


    The term "holobiont" is used to define the host and its collection of beneficial symbionts. It does not differentiate intracellular or extracellular symbionts as it is a lens to view the individual as an engineered collection of organisms. Therefore, the term "hologenome" naturally follows as a definition of the total genetic material of the holobiont. The hologenome emphasizes that the animal’s genome, mitochondria and beneficial microbiome are an aggregate of genes that together form a unit of natural selection (Zilber-Rosenberg and Rosenberg, 2008, link). To be historically accurate, the term hologenome was originally and independently proposed in 1994 by Richard Jefferson in a seminar on PCR technology (YouTube link). The evidence motivating these terms spans the essential roles of the microbiome in eukaryotic fitness (McFall-Ngai et al, 2013, link), including digestion, immunity, olfaction, organ and neuronal development, etc.


    However, the hologenome concept is controversial, perhaps more so than the holobiont. These terms are gaining attention but are still rather new to biology and should be subject to questions. Some view the individual solely through the refined filter of the nuclear genome. In this case, the microbiome is purely extrinsic to the host animal and therefore unable to co-evolve sensu stricto with the host genome. In order for the microbiome to change in parallel with the host genome, stability of the two genomic units by vertical transmission or host selectivity in microbiome community structure is required. Current evidence specifies multiple paths for stability that we must delve much further into.  For example, maternal microbial transmission may be universal in animals for some fraction of the microbiome (Funkhouser and Bordenstein, 2013, link) and specificity provided by the host immune system can further cement the essential foundation for host-microbiome stability and co-cladogenesis (as evident in phylosymbiosis).


    In Nasonia, the phylosymbiotic associations of parental host genes and microbes are both required for fitness within species, but are in negative epistasis in hybrids undefined comparable to nuclear-nuclear and cytonuclear gene interactions that function normally within species but cause hybrid incompatibilities.  In this light, the discovery of the phylosymbiotic gut microbiome can be understood as part of a co-adapted unit, which functions normally within species, but breaks down in hybrids between species.


    Of particular relevance is that the vital fitness traits conferred by the gut microbiome within species blurs the lines between what biologists conventionally define as the environment or the organism. And perhaps this point is the most salient. Intrinsic and extrinsic views of the microbiome are largely semantic filters placed on our definition of the individual. Nature may not care about this linguistic argument. What matters is stability of the associations, no matter if we define them as intrinsic genome-by-genome or extrinsic gene-by-environment interactions. Today, it is convention that mitochondria represent anciently acquired bacteria that have a fully integrated partnership with the animal genome. The continuum of symbiosis stretches from these obligate relationships of endosymbionts to the host farming the microbiome.


    I extend my thanks to the ISS board for asking me to write this blog post and for you reading it. I look forward to reading your future posts and extending this social medium to the symbiosis community.


    Warmest regards,


    Seth

    --------------------------

    Dr. Seth Bordenstein is an invited blogger for the International Symbiosis Society.  He is an Associate Professor at Vanderbilt University in the Departments of Biological Sciences and Pathology, Microbiology, and Immunology, where he studies the interactions between viruses, bacteria, and their animal hosts. 


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