Common Features of Environmental and Potentially Beneficial Plant-Associated Burkholderia
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Microb Ecol (2012) 63:249–266 DOI 10.1007/s00248-011-9929-1 MINIREVIEW Common Features of Environmental and Potentially Beneficial Plant-Associated Burkholderia Zulma Rocío Suárez-Moreno & Jesús Caballero-Mellado & Bruna G. Coutinho & Lucia Mendonça-Previato & Euan K. James & Vittorio Venturi Received: 28 March 2011 /Accepted: 1 August 2011 /Published online: 18 August 2011 # Springer Science+Business Media, LLC 2011 Abstract The genus Burkholderia comprises more than 60 highlighted the division of the genus into two main clusters, species isolated from a wide range of niches. Although they as suggested by phylogenetical analyses. The first cluster have been shown to be diverse and ubiquitously distributed, includes human, animal, and plant pathogens, such as most studies have thus far focused on the pathogenic Burkholderia glumae, Burkholderia pseudomallei,and species due to their clinical importance. However, the Burkholderia mallei, as well as the 17 defined species of increasing number of recently described Burkholderia the Burkholderia cepacia complex, while the other, more species associated with plants or with the environment has recently established cluster comprises more than 30 non- pathogenic species, which in most cases have been found to Jesús Caballero-Mellado deceased be associated with plants, and thus might be considered to be potentially beneficial. Several species from the latter Z. R. Suárez-Moreno : B. G. Coutinho : V. Venturi (*) Bacteriology Group, International Centre for group share characteristics that are of use when associating Genetic Engineering & Biotechnology, with plants, such as a quorum sensing system, the presence Padriciano 99, of nitrogen fixation and/or nodulation genes, and the ability 34149 Trieste, Italy to degrade aromatic compounds. This review examines the e-mail: [email protected] commonalities in this growing subgroup of Burkholderia Z. R. Suárez-Moreno species and discusses their prospective biotechnological University of Medicine and Dentistry of New Jersey, applications. 225 Warren Street, Newark, NJ 07103, USA J. Caballero-Mellado Introduction Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Burkholderia was first proposed as a genus in 1992 by Ap Postal 565-A Cuernavaca, Morelos, México Yabuuchi et al., and it comprised several species that had L. Mendonça-Previato been originally classified as Pseudomonas and Bacilli Instituto de Biofísica Carlos Chagas Filho, Centro de Ciências da [161]. It was named after the American phytopathologist Saúde, Universidade Federal do Rio de Janeiro, Walter Burkholder, who, in 1942, described the first Bloco G, 21944-970, Cidade Universitária, Ilha do Fundão, “ ” Rio de Janeiro, RJ, Brazil Burkholderia species, Phytomonas caryophylli and Phy- tomonas alliicola, as pathogens of carnation and onion, E. K. James respectively [23]. In 1950, Burkholder reported that the EPI Division, The James Hutton Institute, causal agent of sour skin in onion was Pseudomonas cepacia Invergowrie, Dundee DD2 5DA, UK [22], and this species would then become the type species of the current genus, acquiring several names through the years, B. G. Coutinho such as the “eugonic oxidizers group 1” [97], Pseudomonas The Capes Foundation, kingii [73], and Pseudomonas multivorans [135], but with Ministry of Education of Brazil, Cx postal 250, the name P. cepacia finally being revived as it had priority Brasilia, DF 70.040-020, Brazil according to taxonomic rules [11]. 250 Z.R. Suárez-Moreno et al. For a number of years, these bacteria continued to be Today, the Burkholderia genus comprises 62 validly recognized as members of the non-fluorescent pseudomo- described species, and their taxonomy has been continu- nads. In 1966, comprehensive studies of the pseudomonads ously revised. Phylogenetic trees inferred from independent were performed that highlighted the overall similarity of the gene sequence analysis (16S rRNA, recA, gyrB, rpoB, so-called mallei–pseudomallei group by comparing several acdS) have repeatedly shown divisions within the genus phenotypic traits [118, 135]. Palleroni and co-workers with significant bootstrap values (>90) [57, 105, 110, 111, recognized the taxonomic heterogeneity among the pseu- 140]. Taken together, these analyses suggest two main domonads and delineated five species homology groups clusters may be distinguished within the genus Burkholde- based on rRNA–DNA hybridization experiments [108]. ria (Fig. 1). One cluster comprises the B. cepacia complex This led to the subdivision of the genus Pseudomonas into (BCC), the “pseudomallei” group, and plant pathogens, as five well-defined rRNA homology groups, warranting at well as endosymbiotic species from phytopathogenic fungi, least five independent generic designations. Later, polypha- whereas the second cluster contains non-pathogenic Bur- sic taxonomy analyses, including 16S rRNA sequence data, kholderia species associated with plants and/or the envi- DNA–DNA hybridization, and fatty acid analysis, provided ronment. This clustering is consistent with groupings sufficient grounds for the creation of the Burkholderia derived from multilocus sequence typing and whole genus to accommodate the seven species of the rRNA genome analysis, in which species from the plant- group II (P. cepacia, P. caryophylli, Pseudomonas gladioli, associated nitrogen-fixing group (e.g., Burkholderia xen- Pseudomonas mallei, Pseudomonas pseudomallei, Pseudo- ovorans) are located at a distance from the BCC and monas solanacearum, and Pseudomonas picketti)[55, 161]. pseudomallei group species [133, 145, 151]. These internal In the early 1980s, strains of B. cepacia were being divisions appear to reflect interactions with their respective increasingly recovered from cultures of respiratory tract hosts, as most species included in the BCC have shown specimens from cystic fibrosis patients [69]. Further studies pathogenic interactions with their hosts, while most species revealed that while some patients might remain infected from the “plant-associated nitrogen-fixing” clade are with B. cepacia for prolonged periods without obvious reported to be beneficial to theirs [19]. symptoms, others would succumb to a rapidly progressive The non-pathogenic plant-associated species could, necrotizing pneumonia and sepsis, which was denominated therefore, constitute a single clade which contains closely cepacia syndrome (CS). Polyphasic taxonomy studies related species. Burkholderia from this group are mostly revealed that B. cepacia was actually made up of five associated beneficially with plants, although some species closely related but distinct genomic species referred to as the may also survive in sediments and bulk soil [81]. Burkholderia cepacia complex (BCC). Each species was Remarkably, several species from this group can convert initially designated as a genomovar, but they later acquired atmospheric nitrogen to ammonia via biological nitrogen binomial species names [148]. Currently, the BCC complex fixation (BNF) [50, 90]. In addition, most of them are is comprised of 17 species that share 98–100% similarity in catabolically versatile enabling them to degrade recalcitrant their 16S rRNA, and 94–95% in their recA gene sequences compounds, and thus to survive in environments with [151, 152]. Owing to their clinical importance, the BCC limited nutrient availability. Some species are able to complex, as well as other pathogenic Burkholderia spp., promote plant growth, while others are proposed for such as B. mallei and B. pseudomallei, have been the subject biotechnological uses, such as phytoremediation and of numerous reviews [35, 54, 79, 85, 86]. biocontrol. This group will henceforth be referred to as Burkholderia species had thus gained considerable the “plant-beneficial-environmental (PBE) Burkholderia importance owing to their pathogenicity, but two findings cluster”, and their features will be reviewed here with a had a strong impact on their ecological perception: (1) the special emphasis on plant–bacterial interactions. The main identification of nitrogen fixation in Burkholderia species characteristics of this group of species are summarized in other than Burkholderia vietnamiensis (which belongs to Table 1. the BCC), such as “ Burkholderia brasilensis” M130 [9] and Burkholderia kururiensis [50, 162]; and (2) the description of legume-nodulating Burkholderia [98] and Figure 1 Updated phylogenetic tree based on 16S rRNA sequencesb of the recognized species of the Burkholderia genus. Sequences from their subsequent characterization as genuine endosymbionts type strains were aligned and the sequence of Pandoraea norimber- [98]. These two discoveries, together with the increased gensis LMG 13019 was used as an outgroup (bar=0·005 nucleotide exploration of plant growth-promoting rhizobacteria substitutions per nucleotide position). The evolutionary distances were (PGPR), led to the characterization of a considerable computed using the maximum likelihood method and the evolutionary history was inferred using the neighbor-joining method. Numbers at number of Burkholderia species, both from the rhizosphere branch nodes are bootstrap values. Red—the pathogenic Burkholderia and/or the plant interior, many of them diazotrophs and /or clade; green—plant-associated beneficial and environmental (PBE) legume nodulators [19]. group Beneficial Burkholderia 251 252 Table 1 Main characteristics of the plant-associated beneficial and environmental (PBE) Burkholderia group Species Isolated from Host Relevant