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Molecular Ecology (2010) 19, 28–30 NEWS AND VIEWS PERSPECTIVE Insights into the history of the legumebetaproteobacterial symbiosis A N N E T T E A . A N G U S * and A N N M . H I R S C H * † *Department of Molecular, Cell and Developmental Biology, †Molecular Biology Institute, University of California-Los Angeles, 621 Charles E. Young Drive South, Los Angeles, CA 90095-1606, USA The interaction between legumes and rhizobia has been well studied in the context of a mutualistic, nitrogen-fixing symbiosis. The fitness of legumes, including important agricultural crops, is enhanced by the plants’ ability to develop symbiotic associations with certain soil bacteria that fix atmospheric nitrogen into a utilizable form, namely, ammonia, via a chemical reaction that only bacteria and archaea can perform. Of the bacteria, members of the alpha subclass of the protebacteria are the bestknown nitrogen-fixing symbionts of legumes. Recently, members of the beta subclass of the proteobacteria that induce nitrogen-fixing nodules on legume roots in a species-specific manner have been identified. In this issue, Bontemps et al. reveal that not only are these newly identified rhizobia novel in shifting the paradigm of our understanding of legume symbiosis, but also, based on symbiotic gene phylogenies, have a history that is both ancient and stable. Expanding our understanding of novel plant growth promoting rhizobia will be a valuable resource for incorporating alternative strategies of nitrogen fixation for enhancing plant growth. Keywords: Bacteria, Molecular Evolution, Microbial Evolution, Species Interactions Received 3 November 2009; revision received 8 November 2009; accepted 10 November 2009 Nitrogen fixation by bacteria is a process that promotes plant growth under nitrogen-deficient or nitrogen-limiting conditions. Nitrogen gas, which is abundant (c. 80% of our atmosphere) but highly unreactive, is reduced to ammonia through the action of the enzyme nitrogenase. Ammonia is incorporated into the plant’s metabolic pathways to build DNA and proteins for essential processes such as cellular growth and development. By themselves, plants are unable to fix nitrogen, but some plants benefit from their interaction with specialized bacteria that perform this energetically expensive feat, while associated with or housed within Correspondence: Ann M. Hirsch, Fax: (310) 206-5413; E-mail: [email protected] plant organs. Being housed within plant root nodules greatly enhances nitrogen fixation by providing the bacteria with an environment that not only supplies sufficient carbon, but also protects the oxygen-sensitive enzyme, nitrogenase. Molecular communication between plants and soil bacteria initiates the early events of nodulation, including recognition, aggregation ⁄ attachment of bacteria to plant roots, and root hair curling. Bacterial nod genes, induced by plant-derived compounds, are responsible for the synthesis of Nod factor, which is specifically recognized by the host legume. The nodulating bacteria often form biofilms on root surfaces during these early stages, which may be critical for successful nodule formation and nitrogen fixation in later stages. Recognition leads to further molecular signalling events, which ultimately lead to nodule development, bacterial entry, and ultimately differentiation of the bacteria into bacteroids surrounded by plant membrane. It is within these symbiosomes that rhizobia fix nitrogen. The nif genes, which are responsible for nitrogen fixation, are found only in prokaryote genomes and encompass both structural and regulatory genes that encode a functioning nitrogenase. In this issue, Bontemps et al. (2010) show that certain Burkholderia species, recently recognized as nitrogen-fixing symbionts of legumes and other crops such as coffee and maize (Estrada-De Los Santos et al. 2001; Moulin et al. 2001) have a much richer history than initially suspected. The authors’ research complements the developing hypothesis that the Burkholderia-legume symbiosis, although newly published, is in fact a well-defined and effective symbiosis that is common in nature (Chen et al. 2003, 2005; Sawada et al. 2003; Martı́nez-Aguilar et al. 2008). These earlier studies, which followed the initial publication of Burkholderia species as new symbionts of legumes (Moulin et al. 2001), hypothesized that nif and nod genes originated by horizontal gene transfer from alphaproteobacteria. Bontemps et al. (2010) expand on this idea with a comprehensive and in depth study of Mimosa-associated symbionts in the region native to the legume (Fig. 1), a 1800-km area in central Brazil. The authors found that Burkholderia species were the prevalent isolates from root nodules. In total, 47 different species of Mimosa were sampled, with 143 bacterial isolates originating from individual nodules on plant roots; 98% of these isolates were identified as Burkholderia (Fig. 2). It appears that these betaproteobacteria have a specific association with Mimosa given the abundance of Burkholderia isolates. Moreover, the type strain B. phymatum establishes nodules on roots of 30 of 31 Mimosa species. Sequencing of genes essential to symbiosis provides strong evidence that nodulation is not a new function among Burkholderia species. The breadth of the study (including 67 sampling sites in three regions in Brazil over various elevations) provided a solid foundation with 2010 Blackwell Publishing Ltd NEWS AND VIEWS: PERSPECTIVE 29 Fig. 1 A representative of one of the preferred legume symbionts (Mimosa humivagans) of many Burkholderia species. Mimosa species are rich in diversity in their native habitats in South America. Fig. 2 Light micrograph of a nodule section from Mimosa blanchetii growing in the Cerrado (Brazil) that illustrates the immunolocalization and identification of nitrogenase (dark-coloured cells) in Burkholderia strain JPY461 using a B. phymatum STM815-specific antibody. which phylogenetic comparisons were made. PCR amplification and sequencing of 16S rDNA, recA, nifH and nodC provided the raw data for phylogenetic analyses. The data showed that the isolated Burkholderia species represented specific groups that formed seven distinct clades. The majority of isolates belonged to clusters 5 and 6 (34% and 54%, respectively) and were spatially distinct because the clusters mapped correlatively to specific sampling sites according to elevation. However, the most exciting finding was the high congruence of sequences observed from the analysis of the symbiotic genes, which indicates a long and stable genetic history of nodulation and nitrogen fixation for Burkholderia. Only two alphaproteobacteria were isolated among the 141 isolates, and their symbiotic genes were very distant from those of Burkholderia. The high congruence within the clades of Burkholderia species and variance from the alphaproteobacteria provides strong evidence that horizontal gene transfer events occurred much longer ago than previously predicted. 2010 Blackwell Publishing Ltd By choosing both the nitrogen fixation-related gene nifH and the nodulation-related gene nodC, Bontemps et al. (2010) clearly separated the two symbiotic functions. Many bacteria fix nitrogen without nodulating their host, and nif genes are found in a number of unrelated bacterial groups. However, nodulation genes are restricted to internalized symbionts and confined to what traditionally have been called ‘rhizobia’. Interestingly, the authors demonstrate by phylogenetic analysis that Mimosa-associated Burkholderia acquired the nodulation gene nodC through horizontal gene transfer long ago. Furthermore, species from Mimosa and Burkholderia show specificity for each other, as determined by inoculation and coinoculation studies between various plant and bacterial species. Together, this work supports the hypothesis that the symbiosis is not only very old, but also highly specific. The study presented by Bontemps et al. (2010) provides compelling evidence that Mimosa and Burkholderia species have an ancient history of symbiotic coexistence. Not only does Mimosa develop these symbioses with the betaproteobacteria in their local region, but in other parts of the world, these legumes also prefer Burkholderia. In conclusion, this symbiosis has a history that goes further back than expected, as evidenced by deeply branched clades of genes involved in nodulation. It is perhaps an interesting juxtaposition that the betaprotebacteria, which were only recently reported as nodule-inducing rhizobia, have such a deep history of symbioses with legumes. The recent finding of betaproteobacteria as nitrogen-fixing symbionts along with the current study by Bontemps et al. (2010) opens up many possibilities to uncover the true diversity of Burkholderia species. References Bontemps C, Elliott GN, Simon MF et al. (2010) Burkholderia species are ancient symbionts of legumes. Molecular Ecology, 19, 44–52. Chen WM, Moulin L, Bontemps C et al. (2003) Legume symbiotic nitrogen fixation by b-proteobacteria is widespread in nature. Journal of Bacteriology, 185, 7266–7272. Chen WM, de Faria SM, Straliotto R et al. (2005) Proof that Burkholderia strains form effective symbiosis with legumes: a study of novel Mimosa-nodulating strains from South America. Applied and Environmental Microbiology, 71, 7461–7471. Estrada-De Los Santos P, Bustillos-Christales R, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Applied and Environmental Microbiology, 67, 2790– 2798. Martı́nez-Aguilar L, Dı́az R, Peña-Cabriales JJ et al. (2008) Multichromosomal genome structure and conformation of diazotrophy in novel plant-associated Burkholderia species. Applied and Environmental Microbiology, 74, 4574–4579. Moulin L, Munive A, Dreyfus B (2001) Nodulation of legumes by members of the b-subclass of proteobacteria. Nature, 411, 948– 950. Sawada H, Kuykendall LD, Young JM (2003) Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. Journal of General and Applied Microbiology, 49, 155–179. 30 N E W S A N D V I E W S : P E R S P E C T I V E Dr Hirsch has worked on biological nitrogen fixation for over 25 years, investigating the involvement of both plant and microbial partners in the symbiosis, especially bacterial attachment to the host. Dr Hirsch and her co-workers recently discovered that the core nodulation (nod) genes of Sinorhizobium meliloti, the nitrogen-fixing endosymbiont of alfalfa, are required for the establishment of mature biofilms. This result defines a new role for Nod factor in addition to its significance as a signaling molecule. The Hirsch lab also studies the beta- rhizobial strain Burkholderia tuberum, recently reported as inducing the development of nitrogen fixing on legume hosts. Current research centers on the sequencing and annotation of four plant-associated Burkholderia genomes as well as a search for B. tuberum mutants affected in attachment and nodule development ⁄ function. doi: 10.1111/j.1365-294X.2009.04459.x 2010 Blackwell Publishing Ltd