Synthesizing symbiosis, if possible with multiple partners

Over 300 delegates with diverse interests in the evolution, ecology, physiology, genomics, and molecular biology of symbiosis came together for the 6th International Symbiosis Society (ISS6) Congress http://people.bu.edu/iss/ held at the University of Wisconsin–Madison. The University of Wisconsin recently hired a number of new faculty members with a common research interest in symbiosis and all of the talks were held in their new Microbial Sciences Building, highlighting the University of Wisconsin’s commitment to symbiosis research. This report provides a brief overview of selected ISS6 talks and posters involving a wide range of research questions and research systems on autotrophic and heterotrophic organisms. In addition to N-fixing and mycorrhizal symbioses, a wide range of systems were discussed in which plants and other photosynthetic organisms serve as microbial hosts, food sources for animals, symbionts of animals and as participants in multitrophic interactions. Cross-cutting themes across all symbiotic systems were the tension between conflict and cooperation, communication between partners, exchange of metabolites, specificity of symbioses, evolution and host defense. ‘…plants can preferentially allocate resources to the more mutualistic AMF symbiont, but only when there is spatial separation from less mutualistic, cheater taxa.’ Barbara Schulz and colleagues (University of Braunschweig, Germany) addressed the question of what circumstances cause a single root endophytic fungus to become a mutualist or a pathogen. In experimental inoculations with the fungus Phialocelphala fortinii, they showed that the effects of infection depended on the species of host plant and on its health. Thus the outcome of symbiosis may vary with host identity and host environment. Catherine Masson-Boivin (INRA, France) and colleagues addressed the general question of what traits or genes distinguish mutualistic symbionts from free-living or pathogenic relatives. Most rhizobia are alpha-proteobacteria, but several disparate beta-proteobacteria have recently been shown to elicit host nodule formation and nitrogen fixation. Using an experimental evolution approach, they were able to produce strains of a common soil pathogen (Ralstonia solanacearum) that were able to elicit nodule formation by the plant although not yet develop nitrogen-fixing bacteroids. Therefore, gene transfer can produce novel symbionts that grow in a common environment with pre-existing symbionts. Sometimes a symbiont requires a partner in a three-way interaction. Two very different, complex multispecies interactions were described in grass hosts. Christian Hertweck (HKI Jena, Germany) discussed the role of rhizoxin produced by the fungus Rhizopus microsporus as the causative agent of rice seedling blight (Partida-Martinez & Hertweck, 2005). Through a series of experiments, he demonstrated conclusively that the rhizoxins were produced by endosymbiotic Burkolderia. Further, fungal spore production did not occur in the absence of the endosymbiont, illustrating its complete dependence on the bacterial symbiont. Mustafa Morsy and colleagues (Noble Foundation, OK, USA) presented an analogous interaction where heat tolerance of the grass Dichanthelium lanuginosum, which grows in geothermal hotspring soils, is based on infection by the endophytic fungus Curvularia protuberata. They showed that the endophytic fungus is infected by a virus, and that curing of the virus eliminates thermotolerance of the host grass (Marquez et al., 2007). Other symbiotic associations should be examined for even smaller, essential partners. A last tripartite symbiosis is the mountain pine beetle and its two fungal symbionts (Ophiostoma montium and Grosmannia clavigera), which supplement the beetle’s nutrient-poor phloem resources. The fungi are, in turn, dispersed and inoculated into new host trees by the beetle. Pine beetle outbreaks have devastating impacts on southern and western pine forests. Plant root systems exist in an extraordinarily diverse soil environment filled with microbial mutualists, pathogens, and saprophytes. Mycorrhizal symbioses are an important component of ISS meetings, although the 2009 meeting conflicted with an international congress in Brazil. In a symposium on the microbial symbiont impacts on communities and ecosystems, Jim Bever (Indiana University, USA) discussed the ecological consequences of diversity of arbuscular mycorrhizal fungi (AMF). In a variety of glasshouse and field experiments, he demonstrated that different AMF species have different effects on plant growth, defense compounds, and soil aggregation. He also posed a solution to a dilemma found in many symbiotic systems – invasion by cheaters that use host resources without benefit in return (Douglas, 2008). His data show that plants can preferentially allocate resources to the more mutualistic AMF symbiont, but only when there is spatial separation from less mutualistic, cheater taxa (Bever et al., 2009). Kataynza Turnau (Jagiellonian University, Poland) also discussed the importance of mycorrhizal symbioses in the conservation of endangered plant species and in the survival of plant species in stressful, human-impacted habitats such as mine spoils. The symbiotic N-fixing soil actinomycete Frankia and its host plants occur worldwide as a primary source of the world’s fixed N. Many actinorhizal plants are invasive, far beyond their native ranges, yet readily nodulate and fix N. This raises the question of specificity and whether introduced species bring their symbionts or utilize resident symbionts. Jeff Dawson (University of Illinois, USA) described the spatial distribution of Frankia in the soil of a dune/swale community with several distinct genera and families of host plants. PCR amplification of 16S rDNA sequences demonstrated clustering of strains by host phylogeny. But, unexpectedly, they found that nodulation was promoted by actinorhizal plants in general, including hosts supporting divergent Frankia strains, suggesting that the mechanisms of host specificity and host nodulation are distinct. The richness of the research presented at the congress on interactions in the rhizosphere was clear, with the two New Phytologist poster prizes being awarded to two students working on this topic: Cara Haney (Stanford University, CA, USA), for her work on plant flotillin-like proteins required for symbiosis with N2-fixing bacteria; and Allison Schwartz (University of Los Angeles, USA), for her investigations on a strain of plant growth promoting Bacillus simplex on Lotus japonicus. The large- and small-scale distribution patterns of highly diverse symbiotic systems were considered. Francois Lutzoni (Duke University, NC, USA) discussed the global distribution of lichenized fungi to gain insights into the various origins and evolutionary history of lichen symbiosis. David Richardson (St Mary’s University, Halifax, Canada) described a Canadian lichen, Degelia plumbea, that produces ascospores only and so needs to steal its photosynthetic symbiont from local asexual lichen species. Marc-André Selosse (Centre d’Ecologie Fonctionnelle et Evolutive, Montpellier, France) covered the evolution of ericoid-type mycorrhizas using ITS sequencing and microscopy, but also N and C isotope analyses to infer their functional role for host plants. Many symbiotic systems can only be understood in the context of natural enemies of the host. The fungus-farming ants and their actinomycete bacteria that protect the fungal colony from pathogens are an excellent example of the multiple layers of complexity that exist in many symbioses. Michael Poulson (University of Wisconsin, USA) presented evidence that ant colonies rear a single clone in their fungal garden and just a single strain of the antibiotic-producing bacterium. While genetic uniformity of the fungus may not impart any costs for the ants because of protection by the symbiotic bacteria, one could expect greater diversity of bacterial strains to provide greater antibiotic diversity and better protection to the fungal colony (Currie et al., 2003). In an ant–plant system where ants form domatia on the plant and protect their host from herbivores, Rumsais Blatrix (Centre d’Ecologie Fonctionnelle et Evolutive, Montpellier, France) demonstrated that host defense was based on specific chemical communication from the host plant to ant defenders when active defense is required. Several presentations focused on the seed-transmitted endophytes of grasses. Grass endophytes represent a tritrophic symbiotic system predicated on protection of host plants. Chris Schardl (University of Kentucky, USA) discussed alkaloid synthesis gene clusters among Neotyphodium endophyte strains. Endophytes produce four classes of alkaloids in total but no single strain produces more than three. He suggested that while alkaloids mediate host protection, they are costly and subject to frequency-dependent selection such that a single strain or species encompasses more genetic diversity for alkaloid production than any one isolate. Keith Clay (Indiana University, USA) presented experimental data on the role of endophyte alkaloids in host protection from herbivores and the population dynamic consequences of that protection. Jennifer Rudgers (Rice University, TX, USA) considered the impacts of grass endophytes on community and ecosystem processes. In the globally distributed tall fescue, endophyte infection had dramatic effects on arthropod community composition and abundance. The tremendous diversity of plant–endophyte associations beyond the grasses was highlighted by Elizabeth Arnold (University of Arizona, USA), who described her work on a wide range of nonsystemic fungal endophytes from higher plants and lichens, and their varied phylogenetic origins (Rodriguez et al., 2009). The genome sequences of three legumes (Lotus japonicus, Glycine max (soybean) and Medicago truncatula) have been obtained recently, promoting rapid progress in understanding the genetics and biochemistry of symbiotic nitrogen fixation. Michael Udvardi (Noble Foundation, OK, USA) explained how a number of mutagenesis approaches, such as tilling, insertion mutagenesis, and fast neutron bombardment, are being developed in M. truncatula to understand nutrient exchange between the partners. The scale of genetic resources available for M. truncatula means that it is becoming a model not only for symbiotic nitrogen fixation, but also for the AMF symbiosis. Gary Stacey (University of Missouri, USA) reported on efforts to harvest soybean root hairs, which represent single cells, coupled to a broad transcriptomic, proteomic, metabolomic and small RNA analysis, aimed at understanding the earliest stages of interaction between partners. The development of nitrogen-fixing bacteroids in legume nodules was the focus of several other talks. Recent research in the Poole laboratory (John Innes Centre, Norwich, UK) has revealed that rhizobia in legume nodules shut down aliphatic amino acid biosynthesis and become dependent on the host for their supply, the so-called ‘symbiotic auxotrophy’ (Prell et al., 2009). In some respects, this resembles the obligate Buchnera–aphid symbiosis, where the aphid provides Buchnera with many nonessential amino acids in return for essential amino acids. Sandy Macdonald (University of York, UK) also proposed that waste ammonia from the aphid is not excreted, but is instead recycled back into essential amino acids by Buchnera. These findings highlight the increasing metabolic interdependence from rhizobia to Buchnera and true organelles. The interaction between plant roots and soil microorganisms is a critical determinant of plant productivity. Many of the key plant–microbe interactions occur in the rhizosphere (the soil region adjacent to plant roots). Jorge Vivanco (Colorado State University, USA) showed that Arabidopsis thaliana and M. truncatula maintain very different types of soil fungal biodiversity. When each plant was transferred into soil in which the other plant had been grown for many generations, there was a steep decline in fungal biomass, taking at least three generations of planting to reverse. This is very interesting from the perspective of how introduced plants, such as Centaurea maculosa, can become weeds because microbial populations in the new environment do not limit plant growth (Callaway et al., 2003). Focusing on one of the earliest steps in colonization, Anne Hirsch (UCLA, USA) reported that the common nod genes (nodDABC) are essential for biofilm formation of Sinorhizobium meliloti on alfalfa roots. Furthermore, these genes are induced during biofilm formation mostly independently of the root flavonoid inducer luteolin. This raises the question of whether nod gene induction by flavonoids is more important for maintenance of infection threads than at the first stages of contact with the root. We still know very little about how bacteria grow down infection threads, and what controls this. Graham Walker (University of Illinois, USA) highlighted a number of genes, such as bacA, bluB and a new RNAase (SMc01113), that are essential for bacteroid development. The role of BacA is still elusive, although it is known to alter very long-chain fatty acid insertion into the lipopolysaccharidic layer, as well as peptide uptake. BluB is required for B12 synthesis, which is essential for ribonucleotide reductase in nodules, but not in free-living bacteria (Campbell et al., 2006). This is likely to be the result of the greater oxidative stress encountered in the nodule as suggested by pioneering work in the Walker laboratory. Again, this protein appears to be absolutely essential in the developing bacteroid, probably because of the greater stress encountered in the nodule. A novel signaling dependent on cAMP synthesis by CyaD1, CyaD2 and CyaR has been discovered by Jacques Batut in S. meliloti. cAMP probably binds to a transcriptional regulator (Csr), which appears to regulate more than a hundred genes. This pathway is induced by nodule or leaf extracts, but not root extracts, and appears to limit the number of infection threads initiated. Overall recent studies of the legume–Rhizobium symbiosis have highlighted the importance of the signaling events as bacteria invade the plant and establish N2-fixing bacteroids. We understand the first (nod factor synthesis and perception by the plant) and last steps (N2 fixation biochemistry) best, but the steps in between remain elusive. From the standpoint of symbiosis, though, this is a very interesting transition from free-living bacteria into symbionts. Historically, research in symbiosis has been balkanized, with limited cross-communication across system-specific research programs. An important outcome of the ISS6 meeting was the emergence of common themes, tools and research questions applicable across a diversity of symbiotic systems. In a session on how to teach symbiosis, attendees showed each other their own symbiotic models. It was clear that, enriched by these cross-links between all models, research on symbiosis is poised to take a steep upward trajectory. We’ll see this at the next meeting in Kraków, Poland, 2012!

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