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Find out more on how to host your own Frontiers Research Topic or contribute to one as an author by contacting the Frontiers Editorial Office: researchtopics@frontiersin.org 2 February 2017| Recent Advances in Symbiosis Resear ch Frontiers in Microbiology RECENT ADVANCES IN SYMBIOSIS RESEARCH: INTEGRATIVE APPROACHES The upside-down jellyfish Cassiopea xamachana lives in symbiosis with dinoflagellate algae in the genus Symbiodinium Photo credit: Erika Diaz-Almeyda, Department of Biology, Emory University, USA. Topic Editors: M. Pilar Francino, Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana-Salud Pública & Universitat de València & CIBER en Epidemiología y Salud Pública, Spain Mónica Medina, Pennsylvania State University, USA Traditionally, symbiosis research has been under- taken by researchers working independently of one another and often focused on a few cases of bipartite host-symbiont interactions. New model systems are emerging that will enable us to fill fundamental gaps in symbiosis research and the- ory, focusing on a broad range of symbiotic inter- actions and including a variety of multicellular hosts and their complex microbial communities. In this Research Topic, we invited researchers to contribute their work on diverse symbiotic net- works, since there are a large variety of symbi- oses with major roles in the proper functioning of terrestrial or aquatic ecosystems, and we wished the Topic to provide a venue for communicating findings across diverse taxonomic groups. A syn- thesis of recent investigations in symbiosis can impact areas such as agriculture, where a basic understanding of plant-microbe symbiosis will provide foundational information on the increas- ingly important issue of nitrogen fixation; climate change, where anthropogenic factors are threaten- ing the survival of marine symbiotic ecosystems such as coral reefs; animal and human health, where unbalances in host microbiomes are being increasingly associated with a wide range of diseases; and biotechnology, where process optimi- zation can be achieved through optimization of symbiotic partnerships. Overall, our vision was to produce a volume of works that will help define general principles of symbiosis within a new conceptual framework, in the road to finally establish symbiology as an overdue central discipline of biological science Citation: Francino, M. P., Medina, M., eds. (2017). Recent Advances in Symbiosis Research: Integrative Approaches. Lausanne: Frontiers Media. doi: 10.3389/978-2-88945-015-2 3 February 2017| Recent Advances in Symbiosis Resear ch Frontiers in Microbiology Table of Contents 05 Editorial: Recent Advances in Symbiosis Research: Integrative Approaches M. Pilar Francino and Mónica Medina Section 1. Plant-microbe symbioses: 07 The rhizosphere microbiota of plant invaders: an overview of recent advances in the microbiomics of invasive plants Vanessa C. Coats and Mary E. Rumpho 17 Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance Devin Coleman-Derr and Susannah G. Tringe 23 Convergence in mycorrhizal fungal communities due to drought, plant competition, parasitism, and susceptibility to herbivory: consequences for fungi and host plants Catherine A. Gehring, Rebecca C. Mueller, Kristin E. Haskins, Tine K. Rubow and Thomas G. Whitham 32 Expanding genomics of mycorrhizal symbiosis Alan Kuo, Annegret Kohler, Francis M. Martin and Igor V. Grigoriev 39 Nodule carbohydrate catabolism is enhanced in the Medicago truncatula A17- Sinorhizobium medicae WSM419 symbiosis Estíbaliz Larrainzar, Erena Gil-Quintana, Amaia Seminario, Cesar Arrese-Igor and Esther M. González 46 Nitrogen-fixing Rhizobium -legume symbiosis: are polyploidy and host peptide- governed symbiont differentiation general principles of endosymbiosis? Gergely Maróti and Éva Kondorosi 52 Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree Luis C. Mejía, Edward A. Herre, Jed P. Sparks, Klaus Winter, Milton N. García, Sunshine A. Van Bael, Joseph Stitt, Zi Shi, Yufan Zhang, Mark J. Guiltinan and Siela N. Maximova Section 2. Marine symbioses: 68 Microbial experimental evolution as a novel research approach in the Vibrionaceae and squid- Vibrio symbiosis William Soto and Michele K. Nishiguchi 82 Bacteria in Ostreococcus tauri cultures – friends, foes or hitchhikers? Sophie S. Abby, Marie Touchon, Aurelien De Jode, Nigel Grimsley and Gwenael Piganeau 92 Fungal association with sessile marine invertebrates Oded Yarden 4 February 2017| Recent Advances in Symbiosis Resear ch Frontiers in Microbiology 98 The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral–algal associations John E. Parkinson and Iliana B. Baums 117 Not just who, but how many: the importance of partner abundance in reef coral symbioses Ross Cunning and Andrew C. Baker 127 A genomic approach to coral-dinoflagellate symbiosis: studies of Acropora digitifera and Symbiodinium minutum Chuya Shinzato, Sutada Mungpakdee, Nori Satoh and Eiichi Shoguchi 144 Novel tools integrating metabolic and gene function to study the impact of the environment on coral symbiosis Mathieu Pernice and Oren Levy 150 The engine of the reef: photobiology of the coral–algal symbiosis Melissa S. Roth 172 Microbial diversity and activity in the Nematostella vectensis holobiont: insights from 16S rRNA gene sequencing, isolate genomes, and a pilot-scale survey of gene expression Jia Y. Har, Tim Helbig, Ju H. Lim, Samodha C. Fernando, Adam M. Reitzel, Kevin Penn and Janelle R. Thompson Section 3. Other animal-microbe symbioses: 194 Wolbachia is not all about sex: male-feminizing Wolbachia alters the leafhopper Zyginidia pullula transcriptome in a mainly sex-independent manner Hosseinali Asgharian, Peter L. Chang, Peter J. Mazzoglio and Ilaria Negri 204 Identification of overexpressed genes in Sodalis glossinidius inhabiting trypanosome-infected self-cured tsetse flies Illiassou Hamidou Soumana, Bernadette Tchicaya, Béatrice Loriod, Pascal Rihet and Anne Geiger 212 Microbial interactions and the ecology and evolution of Hawaiian Drosophilidae Timothy K. O’Connor, Parris T. Humphrey, Richard T. Lapoint, Noah K. Whiteman and Patrick M. O’Grady 220 Structural and functional changes in the gut microbiota associated to Clostridium difficile infection Ana E. Pérez-Cobas, Alejandro Artacho, Stephan J. Ott, Andrés Moya, María J. Gosalbes and Amparo Latorre Section 4. Novel theoretical and methodological approaches: 235 The symbiont side of symbiosis: do microbes really benefit? Justine R. Garcia and Nicole M. Gerardo 241 Production possibility frontiers in phototroph:heterotroph symbioses: trade- offs in allocating fixed carbon pools and the challenges these alternatives present for understanding the acquisition of intracellular habitats Malcolm S. Hill 252 Hidden state prediction: a modification of classic ancestral state reconstruction algorithms helps unravel complex symbioses Jesse R. R. Zaneveld and Rebecca L. V. Thurber 260 Symbiote transmission and maintenance of extra-genomic associations Benjamin M. Fitzpatrick EDITORIAL published: 31 August 2016 doi: 10.3389/fmicb.2016.01331 Frontiers in Microbiology | www.frontiersin.org August 2016 | Volume 7 | Article 1331 | Edited by: Suhelen Egan, University of New South Wales, Australia Reviewed by: Julie L. Meyer, University of Florida, USA *Correspondence: M. Pilar Francino mpfrancino@gmail.com Mónica Medina momedinamunoz@gmail.com Specialty section: This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology Received: 18 July 2016 Accepted: 11 August 2016 Published: 31 August 2016 Citation: Francino MP and Medina M (2016) Editorial: Recent Advances in Symbiosis Research: Integrative Approaches. Front. Microbiol. 7:1331. doi: 10.3389/fmicb.2016.01331 Editorial: Recent Advances in Symbiosis Research: Integrative Approaches M. Pilar Francino 1, 2, 3 * and Mónica Medina 4 * 1 Area of Genomics and Health, Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana-Salud Pública, València, Spain, 2 Unitat Mixta d’Investigació en Genòmica i Salut, FISABIO-Universitat de València, València, Spain, 3 CIBER en Epidemiología y Salud Pública, Madrid, Spain, 4 Department of Biology, Pennsylvania State University, University Park, PA, USA Keywords: microbiome, multicellular host, plant-microbe symbiosis, marine symbiosis, holobiont The Editorial on the Research Topic Recent Advances in Symbiosis Research: Integrative Approaches Symbiosis research is being transformed by new model systems and technologies that bring forth unexpected discoveries. Technological advances such as those stemming from Next Generation Sequencing enable detailed insights into the molecular bases of symbiotic relationships, and have revolutionized the study of complex microbial communities. As new data gathers, the need grows for a conceptual framework that helps organize and make sense of the information. Here, we present some ground-breaking works pushing the boundaries of our understanding of symbiosis in a variety of systems, as well as some state-of-the-art attempts at putting forward organizing principles for the whole of symbiology. Several works in the Topic address plant-microbe symbioses. All plants are home to a variety of microorganisms that inhabit nearly all their tissues, offering a variety of benefits. Rhizosphere microbial communities are particularly critical, as they provide access to limiting nutrients. Coats and Rumpho review how molecular biodiversity analyses have advanced our understanding of the rhizosphere microbiota of invasive plants, which enables the invasion of new ranges. Coleman-Derr and Tringe, on the other hand, focus on the microbiome of crop plants and its large potential for modulating plant responses to the stresses associated with climate change and use of suboptimal agricultural lands. The relationship between the rhizosphere microbiome and stress is further demonstrated by Gehring et al. Their research on ectomycorrhizal fungal communities associated with pinetrees reveals that biotic and abiotic stressors can result in similar patterns of symbiotic community disassembly, and, remarkably, that the less diverse communities that result may actually be beneficial to host trees under stressful conditions. Kuo et al., Larrainzar et al., and Maróti and Kondorosi rather focus on the biology of specific rhizosphere microbes and the mechanisms enabling their interactions with host plants. The role of foliar symbionts is addressed by Mejía et al., who demonstrate the effects of an endophytic fungus on genetic and phenotypic expression in the tropical tree Theobroma cacao Marine systems also provide innumerable examples of fascinating symbioses. Soto and Nishiguchi offer us a new twist on the classic squid- Vibrio model, proposing experimental evolution approaches to gain further insights into this system. Abby et al. and Yarden explore lesser-known associations, such as those among bacteria and planktonic microalgae and among fungi and various marine invertebrates. A number of works focus on corals and their associated microbes, the study of which has been fundamental to cement the concept of the holobiont —a multicellular host and its associated microbiome (Margulis, 1993). Corals have become the prime example 5 Francino and Medina Advances in Symbiosis Research of a living system that will not survive when the interactions among the species that compose it are disrupted, as is increasingly occurring in the context of climate change. Parkinson and Baums argue that the coral holobiont should be considered as a single unit of selection, because it is specific host/symbiont genotype combinations that determine its extended phenotype and capacity for survival. Cunning and Baker remind us that the success of coral symbioses may be determined not only by the genetic identity of the partners, but also by their relative abundance, which should depend on environmental conditions. From a more mechanistic perspective, Shinzato et al. demonstrate how genomic analyses can generate detailed knowledge about the molecular and cellular processes enabling the coral-dinoflagellate symbiosis. Pernice and Levy and Roth illustrate how other technologies complement genomic analyses to generate further insight into coral physiology and metabolism. Meanwhile, Har et al. employ a variety of “omic” approaches to characterize the microbiota of Nematostella vectensis , a new cnidarian model for the study of metazoan evolution and development. Insect symbioses also exemplify the varied interactions that can be established among microbes and animal hosts. Asgharian et al. revisit the many-faceted relationship between insects and Wolbachia , using transcriptomic techniques to show that the endosymbiont can have both sex-dependent and independent effects on its host. Hamidou Soumana et al. also exploit transcriptomics to explore the multi-level relationship among endosymbionts, trypanosomes and the tsetse fly. In turn, O’Connor et al. unveil that symbiotic microbes play a crucial role in shaping the complex interactions between the Hawaiian Drosophilidae and their host plants, hence contributing to their adaptive radiation. In spite of their importance, host-microbe associations are vulnerable. A notorious example is the disruption of the complex microbial community inhabiting the intestinal tract when assaulted by antibiotics, resulting in an increased vulnerability to infection by opportunistic pathogens. Pérez-Cobas et al. explore how antibiotic-induced changes in the gut microbiota relate to Clostridium difficile infection, and define microbial taxa and functions that might protect against colonization by this pathogen. While this approach illustrates the common perspective of analyzing host-microbe symbioses in terms of potential benefits to the host, García and Gerardo take the less-traveled road of considering what microbes have to gain from the symbiotic interaction. They conclude that symbionts may sometimes be more akin to prisoners or farmed crops than to equal partners. Therefore, researchers should determine whether symbionts have adaptations to evade capture by hosts, in addition to evaluating both costs and benefits of presumed mutualisms. A theoretical framework to analyze cost/benefit ratios is provided by Hill in the context of fixed-carbon allocation in phototroph/heterotroph symbioses, where endosymbionts may control the energy trade-offs faced within host cells. We close with two articles proposing new methodological and theoretical approaches to take forward the study of symbiotic systems. Zaneveld and Thurber demonstrate the application of ancestral state reconstruction for predicting the presence of unknown taxa and functions in microbial communities that are too complex to be wholy described experimentally. And, finally, Fitzpatrick raises the crucial issue of whether hosts and symbionts can truly coevolve when symbionts are not vertically transmitted, proposing linkage disequilibrium analysis as the correct framework to address this question. Reassuringly, this approach reveals that selection and population structure can generate covariance between host and symbiont traits, providing the basic requirement for the coevolution of the intricate symbiotic systems that pervade all realms of Life. AUTHOR CONTRIBUTIONS All authors listed, have made substantial, direct, and intellectual contribution to the work, and approved it for publication. FUNDING The authors were supported by grants NSF OCE 1442206 (MM) and MINECO SAF2012-31187 (MF) during writing of this manuscript. ACKNOWLEDGMENTS We thank the Frontiers editorial staff for their support and all of the authors and reviewers who participated in this Research Topic. REFERENCES Margulis, L. (1993). Symbiosis in Cell Evolution . New York, NY: W. H. Freeman. Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Copyright © 2016 Francino and Medina. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Frontiers in Microbiology | www.frontiersin.org August 2016 | Volume 7 | Article 1331 | 6 REVIEW ARTICLE published: 23 July 2014 doi: 10.3389/fmicb.2014.00368 The rhizosphere microbiota of plant invaders: an overview of recent advances in the microbiomics of invasive plants Vanessa C. Coats 1 and Mary E. Rumpho 2 * 1 Department of Molecular and Biomedical Sciences, University of Maine, Orono, ME, USA 2 Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT, USA Edited by: Monica Medina, Pennsylvania State University, USA Reviewed by: Scott Clingenpeel, DOE Joint Genome Institute, USA Detmer Sipkema, Wageningen University, Netherlands *Correspondence: Mary E. Rumpho, Department of Molecular and Cell Biology, University of Connecticut, 91 North Eagleville Road, Unit 3125, Storrs, CT 06269, USA e-mail: rumpho@uconn.edu Plants in terrestrial systems have evolved in direct association with microbes functioning as both agonists and antagonists of plant fitness and adaptability. As such, investigations that segregate plants and microbes provide only a limited scope of the biotic interactions that dictate plant community structure and composition in natural systems. Invasive plants provide an excellent working model to compare and contrast the effects of microbial communities associated with natural plant populations on plant fitness, adaptation, and fecundity. The last decade of DNA sequencing technology advancements opened the door to microbial community analysis, which has led to an increased awareness of the importance of an organism’s microbiome and the disease states associated with microbiome shifts. Employing microbiome analysis to study the symbiotic networks associated with invasive plants will help us to understand what microorganisms contribute to plant fitness in natural systems, how different soil microbial communities impact plant fitness and adaptability, specificity of host–microbe interactions in natural plant populations, and the selective pressures that dictate the structure of above-ground and below-ground biotic communities. This review discusses recent advances in invasive plant biology that have resulted from microbiome analyses as well as the microbial factors that direct plant fitness and adaptability in natural systems. Keywords: rhizosphere, microbiome, plant–microbe interactions, invasive plant, soil INTRODUCTION Symbiotic relationships shaped the origin, organization, and evolution of all life on Earth. Originally defined as “the living together of unlike named organisms” (de Bary, 1878), the term symbiosis has traditionally been applied to associations like mutu- alism, commensalism, and even parasitism (Parniske, 2008). More recent symbiosis research is expanding this definition to encom- pass a role of microbial symbiotic relationships in far-reaching themes of biology such as speciation, evolution, and coadapta- tion (Margulis, 1993; Klepzig et al., 2009; Carrapiço, 2010; Lankau, 2012). The association and close relationships of organisms that cohabitate are vital for the growth and development of all eukary- otic organisms (Carrapiço, 2010; McFall-Ngai et al., 2013). These associations ( = symbiotic networks of microorganisms) shape nat- ural landscapes and directly influence the evolutionary trajectory of individual species and entire ecosystems (Gilbert, 2002; Klepzig et al., 2009). Plant invasions are a global concern because they pose a direct threat to biodiversity and natural resource management, espe- cially in protected areas (i.e., public lands, refuges, conservations, etc.; Foxcroft et al., 2013). For a plant to be considered invasive (and not just naturalized) it must be non-native to the ecosys- tem in question and it must cause environmental damage (i.e., detrimental effects on native flora and fauna) or harm humans (Invasive Species Advisory Committee [ISAC], 2006). Invasive plant science represents a crossroads of diverse opinions derived from many economic, ecological and societal interest groups, and this has lead to disputes regarding the correct approach to inva- sive plant issues (Simberloff et al., 2013). To further complicate the issue, plant classification as “invasive” or “weedy” is often based more on human perceptions and opinions than on actual data regarding the economic, societal, or environmental impact of the plant taxon (Hayes and Barry, 2008). However, the envi- ronmental consensus supports severe ecological damage by plants deemed invasive in protected areas and significant reductions in the biodiversity of native species resulting from plant invasions. Comprehensive reviews of invasive plant impacts have covered the ecological effects of invaders (Pyšek et al., 2012), nutrient cycling modifications (Ehrenfeld, 2003; Liao et al., 2007), mechanisms of plant invasion (Levine et al., 2003), hybridization, and competi- tion (Vila et al., 2004). Synthesizing accurate predictions of the invasive potential of specific plant taxa has proven difficult and there is no universal trait that can be collectively applied to predict invasiveness (Rejmanek and Richardson, 1996; Richardson and Pysek, 2006; Hayes and Barry, 2008; Thompson and Davis, 2011; Morin et al., 2013). A standard approach is needed for accurate impact assessment and the development of a new global database suitable to make future predictions of problem taxa (Morin et al., 2013). The rhizosphere microbiome comprises the greatest diver- sity of microorganisms directly interacting with a given plant; therefore, it has a tremendous capacity to impact plant fitness and adaptation. Bacterial and fungal communities in the rhi- zosphere affect plant immunity (van Wees et al., 2008; Ronald www.frontiersin.org July 2014 | Volume 5 | Article 368 | 7 Coats and Rumpho Invasive plant rhizosphere microbiome and Shirasu, 2012), pathogen abundance (Berendsen et al., 2012), nutrient acquisition (Jones et al., 2009; Richardson et al., 2009), and stress tolerance (Doubkova et al., 2012; Marasco et al., 2012). Traditional hypotheses for plant invasion, such as enemy release hypothesis (ERH; Klironomonos, 2002; Mitchell and Power, 2003; Blumenthal, 2006; Liu and Stiling, 2006; Reinhart and Call- away, 2006; Blumenthal et al., 2009; Eschtruth and Battles, 2009), accumulation of local pathogens (ALP; Eppinga et al., 2006), enhanced mutualist hypothesis (EMH; Marler et al., 1999; Rein- hart and Callaway, 2004; Parker et al., 2006), and plant–soil feedbacks (Ehrenfeld, 2003; Ehrenfeld et al., 2005; Bever et al., 2012), all point directly to the rhizosphere microbiome, in its entirety, as the primary mediator of plant establishment and success. The study of soil microbial communities once relied on laboratory culture techniques, phospholipid fatty acid analy- sis (PFLA), denaturing gel gradient electrophoresis (DGGE), and terminal restriction fragment length polymorphism (TRFLP; Zhang and Xu, 2008; van Elsas and Boersma, 2011). Early on, culture-based approaches revealed “the great plate count anomaly” wherein only about 1% of visible microscopic cells can be cultured using conventional techniques (Staley and Konopka, 1985; Zhang and Xu, 2008; Stein and Nicol, 2011). The DNA technologies available today use genetic information to model the structure and composition of a microbial community (Ven- ter et al., 2004; Tringe and Rubin, 2005; Hugenholtz and Tyson, 2008; Kunin et al., 2008; Vakhlu et al., 2008; Marguerat and Bähler, 2009; Metzker, 2010; Wooley et al., 2010; Simon and Daniel, 2011; Sun et al., 2011; van Elsas and Boersma, 2011; Thomas et al., 2012; Yousuf et al., 2012; Bibby, 2013; Math- ieu et al., 2013). Capable of generating millions of base pairs in a matter of hours for only a few thousand dollars, the primary limitation to next-gen sequencing technologies is han- dling the expansive datasets and applying appropriate statistical analyses to address the biological questions at hand (Metzker, 2010). The link between the rhizosphere microbial community and invasive plant success has been studied for many years (Van der Putten et al., 2007; Pringle et al., 2009; Berendsen et al., 2012; Bakker et al., 2013). Invasive plants provide a unique per- spective to study the effects of the rhizosphere microbiome on plant fitness, the role evolutionary interactions play in struc- turing the plant ecology observed at present, and the potential for directed control and management of invasive plants. The aim of this review was to focus on recent insights into plant– microbe interactions in the rhizosphere of invasive plants. We were interested in studies that used a sequencing based approach to investigate the rhizosphere microbiome of invasive plants. Surprisingly, we found that few invasive plant scientists have moved beyond traditional methods of soil community analysis (i.e., DGGE) regardless of the increasing availability of next- gen sequencing platforms. We discuss the current microbiome data for invasive plants with regard to popular mechanisms of plant invasion (i.e., enemy release, novel symbiont, etc.). Particular attention has been given to rhizosphere microbiome analysis and what this methodology reveals about microbial symbiotic networks in the soil as contributing factors to the development and progression of plant invasions in terrestrial ecosystems. RHIZOSPHERE MICROBIOTA ARE A KEY COMPONENT OF PLANT FITNESS Over 400 million years ago, during the Paleozoic era, the evolution of land plants was made possible by a symbiosis between mycor- rhizal fungi and the common ancestor of land plants (Wang and Qiu, 2006; Humphreys et al., 2010). This association resulted in a fitness advantage and enhanced stress tolerance that was critical for the establishment of terrestrial plants (i.e., increased access to water and mineral nutrients). Evidence of microbial symbiosis is apparent in the oldest lineages of land plants, the liverworts. The arbuscular mycorrhizal (AM) symbioses of liverworts significantly promote photosynthetic C uptake, acquisition of P and N from the soil, growth, and asexual reproduction (Humphreys et al., 2010). Mycorrhizal symbioses undoubtedly demonstrate the importance of symbiotic relationships in terrestrial ecosystems and have been credited for stimulating the diversification of both plant hosts and fungal symbionts (Wang and Qiu, 2006). The soil microbial community constitutes a major portion of a plant’s symbiotic network. Soil is the greatest reservoir of microbes that affect plant growth, fitness, fecundity, and stress tolerance (reviewed by Buée et al., 2009; Faure et al., 2009; Lambers et al., 2009; Lugtenberg and Kamilova, 2009; Cha- parro et al., 2012; Doornbos et al., 2012; Bakker et al., 2013). All plants maintain a direct interaction with soil microbes in the rhizosphere, which is the soil compartment immediately surrounding the root wherein plant root exudates directly influ- ence the structure and function of the soil microbial community ( Figure 1 ; Hiltner, 1904; Hartmann et al., 2008). The sugars, amino acids, flavonoids, proteins, and fatty acids secreted by plant roots help to structure the associated soil microbiome (Badri et al., 2009; Dennis et al., 2010; Doornbos et al., 2012) and these exudates vary among plant species and between geno- types (Rovira, 1969; Micallef et al., 2009). The quantity and composition of root exudate fluctuates with plant developmen- tal stage and the proximity to neighboring species (Chaparro et al., 2012). Microbes growing in the nutrient rich rhizo- sphere produce molecular signals that promote plant fitness and growth (i.e., hormones) and can disrupt inter-plant com- munication in natural systems (Faure et al., 2009; Sanon et al., 2009). Microbes in the rhizosphere can provide a direct access to limit- ing nutrients (e.g., N 2 fixing symbiont) or increase the total surface area of the root system (e.g., mycorrhizal fungi). Many reviews have already covered the positive effects of beneficial root sym- bionts in the rhizosphere (Buée et al., 2009; Bakker et al., 2013), factors affecting rhizosphere microbial communities (Philippot et al., 2013), and the microbial effects on plant health (Berendsen et al., 2012; Berlec, 2012; Bever et al., 2012) and stress tolerance (Rodriguez et al., 2008). Antagonistic interactions derived from microbial pathogens play critical roles in determining the genetic structure and spa- tiotemporal abundance of a plant (Gilbert, 2002; Blumenthal et al., 2009). Pathogenic microbes impose selective pressures on a plant population that favor a specific genetic structure within the Frontiers in Microbiology | Microbial Symbioses July 2014 | Volume 5 | Article 368 | 8 Coats and Rumpho Invasive plant rhizosphere microbiome FIGURE 1 | An overview of plant–microbe interactions that occur in rhizosphere and bulk soils beneath a plant. The soil environment has a direct effect on the plant, the rhizosphere microclimate, and the microbial community in the bulk soil. Root exudates from the plant direct chemical signaling between the plant and the microbial symbiotic network in the soil matrix. Rhizobiota recognize root exudate signals and are recruited to the rhizoplane or root interior. Bulk soil microbes compete for space to colonize the rhizosphere, which results in a rhizosphere microbial community that is derived from the total microbial population in the bulk soil. The microenvironment in the rhizosphere includes the rhizosphere microbiome ( < 3–5 mm of the root), rhizoplane microbiome (at root–soil interface), and the interior root microbiome. Common symbiotic interactions in the root zone include mycorrhizal fungi, bacterial endophytes, and symbiont nodules. host plant community and this stimulates evolutionary change over time (Gilbert, 2002). In natural systems, pathogens medi- ate plant competition and affect spatiotemporal distribution of individuals within the plant community by creating inhabitable and uninhabitable areas within the ecosystem (Gilbert, 2002). The Janzen-Connell hypothesis postulated that pathogen and host densities are responsible for the observed distribution of a plant species by affecting the establishment success of seedlings (Packer and Clay, 2000). A high density of Pythium sp. in the soil beneath parental Prunus serotina trees was observed to pro- hibit the establishment of seedlings in the immediate vicinity (0–5 m), but not seedlings growing at greater distances (25– 30 m; Packer and Clay, 2000). Thus, pathogen accumulation beneath parent plants functions to promote seedling distribu- tion and reduce competition between the parent plant and its offspring. INVASIVE PLANTS DISRUPT NATIVE SYMBIOTIC NETWORKS The introduction of non-native plants can disrupt native sym- biotic networks in the soil and change local grazing patterns for insects and fauna (Elias et al., 2006; Klepzig et al., 2009). Introduced plants alter patterns of nutrient cycling (Laungani and Knops, 2009) and cause chemical changes in the soil envi- ronment (i.e., allelopathy; Cipollini et al., 2012). Often these non-native invaders bring novel traits to the environment that put native plants at a disadvantage (Van der Putten et al., 2007; Laungani and Knops, 2009; Perkins et al., 2011). Plant–microbe interactions may assist invasive plants with outcompeting native flora using mechanisms that include allelopathy-mediated sup- pression of native rhizosphere microbes and beneficial symbionts (Stinson et al., 2006; Callaway et al., 2008), the accumulation of native plant pathogens in the invaded soils (Mangla et al., 2008), and changes in nutrient cycling dynamics that favor the exotic plant (Ehrenfeld et al., 2001; Ehrenfeld, 2003; Laungani and Knops, 2009). Increased availability or access to vital nutrients provides a competitive advantage to invasive plants and facilitates signifi- cant biomass accumulation (Blumenthal, 2006; Blumenthal et al., 2009). Allelopathic plants are among the most aggressive invaders of non-native ecosystems because non-native plants with the ability to synthesize toxic chemicals are often at a competitive advan- tage (Lankau, 2012). Allaria petiolata (garlic mustard) produces allelopathic chemicals that target beneficial microbes like AM symbionts of native plants (Stinson et al., 2006; Callaway and Vivanco, 2007; Callaway et al., 2008). A. petiolata also demon- strated an increased production of toxic chemicals when growing in non-native regions that contain a greater competitive interspe- cific density, implicating the allelopathic effects as the primary invasive characteristic (Lankau, 2012). The introduction of novel allelochemicals into an environment affects the structure of the www.frontiersin.org July 2014 | Volume 5 | Article 368 | 9 Coats and Rumpho Invasive plant rhizosphere microbiome soil microbial community and the microbial biodiversity, espe- cially if these chemicals have antimicrobial activity or function as metal chelators (Inderjit et al., 2011). Soil microbes are the first line of defense toward novel chemicals in a native ecosys- tem. They mediate much of the allelopathic effect in ways as simple as the ability to degrade or detoxify compounds before they accumulate in the soil and inhibit native plant growth (Cipollini et al., 2012). Invasive plants outcompete native plants by accumulating large concentrations of native plant pathogens in the soil (Eppinga et al., 2006; Mangla et al., 2008). A release from microbial pathogens, insect pests, and herbivores of the native range is one mecha- nism behind the success of invasive plants (Klironomonos, 2002; Mitchell and Power, 2003; Reinhart and Callaway, 2006; Blumen- thal et al., 2009), but the distribution of pathogens in the invasive range is just as important for defining competition with native flora. Root exudates of Chromolaena odorata , a severely destructive tropical weed, concentrate Fusarium sp. spores to a level 25-times greater than that observed in the root zone of native plants (Mangla et al., 2008). Thus, these plants exacerbate and exploit the native biotic interactions and gain a competitive advantage. Many, but not all, invasive plants alter patterns of nutrient cycling in the invasive range (Perkins et al., 2011). Changes in the N cycling dynamics in the soil are a frequent consequence of inva- sive plant introduction (Ehrenfeld, 2003; Mack and D’Antonio, 2003; Laungani and Knops, 2009; Perkins et al., 2011). Non-native species can change the quality and quantity of leaf litter (Ehren- feld et al., 2001), modify local decomposition rates (Kourtev et al., 2002a; Elgersma et al., 2012), and disrupt local feedback mech- anisms in the soil system (Ehrenfeld et al., 2005). For example, Pinus strobus is an invader of N-poor grasslands that demonstrates a higher N residence