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- W2803025488 abstract "The First International Conference on Holobionts was organized by the French National Network on Environmental Genomics (GDR GE) and Metaprogramme Meta-omics and Microbial ecosystems (MEM-INRA) under the patronage of three French institutions, namely the National Centre for Scientific Research (CNRS), the National Institute for Agricultural Research (INRA) and the National Museum of Natural History (MNHN). The meeting took place in the magnificent amphitheatre – built in 1788 by order of the famous French naturalist Georges-Louis Leclerc, comte de Buffon (1707–1788) – in the botanical garden of MNHN. This meeting brought together more than 200 scientists of 20 nationalities, highlighting the success of this first conference (Fig. 1). Eight eminent keynote speakers were invited to share their expertise on the holobiont field and 39 selected oral communications acted as plenary speakers. In addition, 60 posters were presented during several poster sessions, which took place under a pavilion near the large glasshouse of the MNHN. The conference format alternated plenary discussions and poster sessions, which strongly stimulated dialogues and debates between researchers working on different ecosystems and biological models (e.g. human, animals, corals, insects, plants and their respective microbiota). A definition of the holobiont notion was presented by Eugene Rosenberg (Tel Aviv University, Tel Aviv, Israel) who inaugurated the conference. A holobiont associates an individual host and its microbiota, while hologenome represents the entire metagenome of a holobiont (Zilber-Rosenberg & Rosenberg, 2008; Theis et al., 2016). This definition does not impose any restriction on the phylogenetic origin of holobiont-constituting organisms, neither on the relationships established between them, nor on the dynamics of holobiont assembly. To this definition of holobiont, we added the ones of microbiota and microbiome, due to some ambiguities in the scientific literature. The microbiota is the assemblage of microorganisms present in a defined environment, and the microbiome refers to the entire habitat (biome suffix), including the microorganisms (bacteria, archaea, eukaryotes, and viruses), their genomes (i.e. genes), and the surrounding environmental conditions (Marchesi & Ravel, 2015). There is some debate over the ome suffix, some in the field limit the definition of microbiome to the collection of genes and genomes of a microbiota, but the term metagenome already describes this. Participants at this meeting supported and encouraged the use of a biome-rooted definition of microbiome, which is important for integrating all environmental factors and constraints in the ecological and evolutionary investigations on holobionts. The meeting sessions considered evolutionary, ecological, functional and applied issues related to holobiont systems. These topics included assembly and transmission of holobiont components, evolution and selection processes in holobionts, acquired functional capacities of the holobiont as compared to those of each individual component, metabolic interactions between host and microbiota, as well as microbiota-associated host diseases and engineering of microbiota for improving host health. During the conference, the holobiont scientific community expressed the will and curiosity to compare and share approaches and results obtained in a wide diversity of holobionts living in different ecosystems, and all the different sessions exemplified plant-related researches on holobionts. A strength of the holobiont concept is that it highlights the complexity of host–microbiota interactions as a challenge and a new imperative for the scientific community (McFall-Ngai et al., 2013; Van der Heijden et al., 2015; Vandenkoornhuyse et al., 2015). For over a century, plant scientists have considered plant–microbiota interactions as a central issue for understanding plant development and health. In older publications, the term microflora was used rather than microbiota. Therefore, plant science can be said to have been engaged in holobiont-related studies before the claim of the holobiont concept. Lorenz Hiltner (1862–1923), who directed the Bavarian Agriculture-Botanical Institute in Munich (Germany), could be considered as a pioneer of plant–microbiota studies. A synthesis of Hiltner's research was published by Hartmann et al. (2008) to commemorate the 100th anniversary of Hiltner's proposition and the definition of the term ‘rhizosphere’ in 1904. At that time, Hiltner claimed that plant health and nutrition are substantially dependent on the composition of the rhizosphere microbiota. Hiltner's view was supported by experiments on biological nitrogen fixation, a function provided by symbiosis, and some others on the selection of beneficial microbiota by plants, through rhizosphere exudates. He also proposed to improve plant health by engineering plant microbiota via the inoculation of beneficial bacteria. Hiltner's followers (see examples in Selosse et al., 2004; Dessaux et al., 2016) deeply investigated interdependency between the plants and microbiota, as well as their applications for enhancing plant health and yield. By positioning microbiota at the heart of plant life, especially when plants are considered in natural ecosystems, Hiltner's heritage facilitated acceptance and the promotion of the holobiont concept by the plant scientific community. The long and ancient history of research on mycorrhizal and bacterial symbioses and plant growth promoting rhizobacteria are among the most outstanding examples of this acceptancy (e.g. Smith & Read, 2008). Omics approaches include (meta)genomics, (meta)barcoding, (meta)transcriptomics, (meta)proteomics and metabolomics (Joly & Faure, 2015). Omics strongly contributed to the move to propel the holobiont to the front line of research, not only because of a rapid and deep access to diversity, function and evolution of microbiota, but also because of the opportunity to obtain insights into holobiont systems in nonmodel organisms. The Holobionts conference allowed us to jump from one branch of the tree of life to another, from plants to insects, from mammals, including humans, to corals, and from archaea and bacteria to viruses. Three large groups of hosts appeared as equally important in holobiont studies, mammals, plants and invertebrates; while microbiota encompassed eukaryotic microbes, bacteria, archaea and viruses. Aside from the diversity of host-associated microbiota, three other major issues were discussed: transmission and assembly of microbiota; evolution and adaptation of holobionts; and holobiont (dis)functioning and health. Microbiota assembly processes and the role of the host in microbiota selection remain fascinating areas of research. Peter Mergaert (CNRS-University Paris-Saclay, Gif-sur-Yvette, France) highlighted the role of host anti-microbial peptides as a common tool-box in plants and insects (Mergaert et al., 2017). Haichar Feth el Zahar (CNRS-University of Lyon, Villeurbanne, France) pointed out that plant exudates can exert a selective pressure on microbiota, resulting in plants exhibiting contrasting nutrient resource strategies; Haichar Feth el Zahar stressed the importance of stable-isotope probing approaches to decipher trophic interactions between plants and the microbiome (Haichar et al., 2016; Guyonnet et al., 2017). Etienne Yergeau (INRS-Institut Armand-Frappier, Laval, Canada) manipulated willow-associated microbiota to increase shoot and root biomass and evaluate holobiont efficiency in phytoremediation of polluted soils by crude oil and metals (Bell et al., 2014). Nathan Vannier (University of Rennes, Rennes, France) highlighted that clonal plants, such as Glechoma hederacea, can be used as a promising model to address key issues on microbiota assembly and transmission over several generations (Vannier et al., 2016). Stéphane Hacquard and Paul Shulze-Lefert (Max Planck Institute for Plant Breeding Research, Cologne, Germany) stressed the importance of microbe–microbe interactions for maintaining equilibrium in plant microbiota (Hacquard et al., 2016; Hacquard, 2017). They also reported that up to 60% of the Arabidopsis thaliana microbiota can be cultured on medium plates, particularly because Proteobacteria dominated the analysed microbiota; hence testing microbiota assembly and function using reconstituted microbiota with isolated strains sounds a very promising approach, which deserves to be put back into the spotlight (Bai et al., 2015). Such an approach should not make us forget the role that could be played by noncultured populations of microbiota. The dynamics of host–microbiota associations was also addressed for different arthropod lineages by Sylvain Charlat (CNRS-University of Lyon, Villeurbanne, France), Didier Bouchon (CNRS-University of Poitiers, Poitiers, France) and Alejandro Manzano-Marin (University of Valencia, Paterna, Spain), highlighting the complex patterns of inheritance of microbiota to the host through vertical but also horizontal transmission and of persistence of the associations over evolutionary timescales (Bouchon et al., 2016; Bailly-Bechet et al., 2017; Manzano-Marín et al., 2017). How holobiont and holobiont-constituents evolve was strongly debated during this meeting and remains an unresolved issue. Some researchers argued that the holobiont constitutes a unit of selection (Bordenstein & Theis, 2015; Theis et al., 2016), while others defended the view that holobiont evolution is no more than a case of levels of selection (Moran & Sloan, 2015; Douglas & Werren, 2016). Marc-André Selosse (MNHN, Paris, France) presented arguments related to neutral evolution as a driver of inter-dependency, which may explain why mircobiota act both in plants and in animals as developmental signals for immunity maturation, as well as the extreme genetic reduction in some endosymbiontic mitochondria and plastids (Selosse et al., 2014). Holobiont functioning is another key-theme in holobiont studies. What are the holobiont functional traits that result from the microbiota and host assembly, and how are those traits contributing to holobiont adaptation in a changing environment? What is the microbiota status (diversity, abundance, functional traits) in a healthy host, and what is the role of microbiota in host defence and host disorders? How can we engineer microbiota for curing or preventing diseases in hosts or for neutralizing hosts that are disease vectors? These issues have been addressed in several biological models from humans to plants and from terrestrial insects to marine crustaceans. Jeroen Raes (Catholic University of Leuven, Leuven, Belgium), Joël Doré (INRA, Jouy-en-Josas, France) and Kevin Theis (Wayne State University, Detroit, MI, USA) presented different approaches of research on humans such as large population studies and disorders-centred studies; they also proposed a vision of a future medicine taking into account the holobiont concept and environmental microbiota (Bordenstein & Theis, 2015; Doré et al., 2017; Vandeputte et al., 2017). Kostas Bourtzis (University of Patras, Agrinio, Greece) presented novel strategies for controlling human-disease vector species based on the release of symbiont-infected individuals that induce sterility in uninfected ones (Zhang et al., 2016); an approach that could be considered for limiting dissemination of some plant diseases. Manuel Blouin (INRA-AgroSup Dijon-University of Burgundy, Dijon, France) revealed a significant interaction between plants and earthworms on the structure and functioning (nitrogen cycle) of soil microbiota (Puga-Freitas et al., 2015). This suggests interactions between plant and earthworm holobionts for recruiting microbiota that contributes to organic matter recycling and mineral nutrition. Stéphane Hacquard and Paul Shulze-Lefert exemplified trade-offs between nutrition and protection in the plant host. The fungus endophyte Colletotrichum tofieldiae transfers the macronutrient phosphorus to A. thaliana shoots, promotes plant growth, and increases fertility only under phosphorus-deficient conditions, whereas defence responses are activated under phosphate-sufficient conditions (Hacquard et al., 2016; Hiruma et al., 2016). Early career scientists (who represented about half of the participants) were very active during this conference, and two poster prizes rewarded their investment in this new research avenue. The New Phytologist prize awarded the PhD work of Chloé Groh (CNRS-University of Strasbourg, Strasbourg, France) who combined omics for investigating the role of isoprenoids in plant host–microbiota interactions. The Holobiont prize was awarded for the work of Benoit Perez-Lamarque (Ecole Normale Supérieure, Paris, France) which was dedicated to the development of new methods to model host–microbiota co-evolutionary processes. The success of the first International Conference on Holobionts propelled the scientific committee to push the organization of the next edition in 2019. There is no doubt that no one will work alone in holobiont studies in future. The Holobionts conference on which this paper is based was mainly supported by CNRS, INRA, and MNHN. The authors thank all organizers and other participants of the Paris Holobionts conference for their input and discussion." @default.
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- W2803025488 title "Holobiont: a conceptual framework to explore the eco-evolutionary and functional implications of host-microbiota interactions in all ecosystems" @default.
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