Pathogenicity and Biotechnological Applications of the Genus Burkholderia
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Cent. Eur. J. Biol.• 6(6) • 2011 • 997-1005 DOI: 10.2478/s11535-011-0072-2 Central European Journal of Biology Pathogenicity and biotechnological applications of the genus Burkholderia Mini-Review Patrizia Paganin, Silvia Tabacchioni, Luigi Chiarini* ENEA, C.R. Casaccia, Technical Unit for Sustainable Development and Innovation of Agro-industrial System, 00123 Rome, Italy Received 06 May 2011; Accepted 20 August 2011 Abstract: Bacteria belonging to the genus Burkholderia are well known for their adaptability to habitats as diverse as freshwater sediments, lungs of cystic fibrosis patients and plant tissues. This genus includes also plant, animal and human pathogenic species, such asBurkholderia glumae, Burkholderia pseudomallei and the Burkholderia cepacia complex. Over the past few years, several newly discovered non-pathogenic plant associated Burkholderia species have raised particular interest for their potential use in plant growth promotion, biocontrol of plant pathogens, phytoremediation and xenobiotics degradation. Highlights from recent studies on the taxonomy, ecology and pathogenicity of different species of the Burkholderia genus are presented with the aim to evaluate their potential use in biotechnology. Keywords: Burkholderia • Burkholderia cepacia complex • Pathogenicity • Biotechnology • Diazotrophs • Genomics • Transcriptomics © Versita Sp. z o.o. 1. Introduction complex [1,3]. The latter is a group of 17 species, widely distributed in the environment, able to promote For the past two decades, research on species of the plant-growth and to antagonize plant pathogens, but genus Burkholderia has been steadily expanding, so it is also reported to contain opportunistic human that the genus Burkholderia currently comprises more pathogens, so that any biotechnological application is, than 60 species, isolated from remarkably diverse at least temporarily, not allowed. Nevertheless, in recent ecological niches such as river water, soil, freshwater years, a growing number of new Burkholderia species sediments and plant rhizosphere, and including also have been discovered and reported as nitrogen fixing, human, animal and plant pathogens [1]. The natural non pathogenic plant-growth promoting bacteria, thus diversity of members of this genus indicates that the being proposed as candidates for biotechnological range of interactions between these bacteria and their applications [4]. hosts is very complex, diverse, and, often, contradictory. Over the past few years, sequencing of more than The ecological and metabolic versatility of this genus 35 Burkholderia genomes has made available to the ranges from the ability to proliferate in lungs of cystic scientific community a huge amount of data that can fibrosis (CF) patients causing often mortal infections significantly contribute to better define the pathogenicity to that of growing inside plant tissues as obligate and the biotechnological potential of the different endosymbionts, from the ability to degrade recalcitrant Burkholderia species and help clarify the genetic basis xenobiotic compounds to that to protect crop plants by of the great ability of members of this genus to adapt synthesizing antifungal compounds. to extremely diverse habitats. This article presents Since the establishment of this genus [2], research highlights from recent studies on the taxonomy, ecology has been focused primarily on two highly pathogenic and pathogenicity of different species of the Burkholderia species such as B. mallei and B. pseudomallei and genus with the aim to evaluate their potential use for on species belonging to the so-called B. cepacia biotechnological applications. * E-mail: [email protected] 997 Pathogenicity and biotechnological applications of the genus Burkholderia 2. Taxonomy and ecology due to their epidemiological and sanitary features. B. thailandensis, the third and last member of this Burkholderia is a phylogenetically coherent genus subgroup, is non pathogenic for humans and was within the β-proteobacterial subphylum, which was previously described as a non pathogenic variant of first described by Yabuuchi and colleagues (1992) [2] B. pseudomallei [8]. by transferring seven species from the Pseudomonas The so-called phytopathogenic subgroup includes genus, with Burkholderia cepacia as the type species. some well known and wide spread plant pathogens Since then, more than 50 validly named species and such as B. andropogonis, B. glumae, and B. plantarii. candidate species have been added to this genus. So B. glumae is an emerging seed-borne rice pathogen far, the most comprehensive phylogenetic analysis of in many areas around the world and is known to be Burkholderia species are based on 16S rRNA, recA and the etiologic agent of the so-called panicle blight, which acdS genes [5]. They all point out that there are two can cause severe crop yield losses as high as 40% [9]. main lineages in this genus: one is composed largely B. andropogonis has been long known as the causal of pathogens, whereas the other includes mainly agent of several plant diseases such as stripe disease environmental isolates that may form non-pathogenic of sorghum and leaf spot of velvet bean, and more associations with plants. recently it has been described as the cause of brown The first lineage includes human, animal and plant leaf spot of citrus [10]. It is remarkable that B. rhizoxinica pathogens (Burkholderia cepacia complex (BCC) and B. endofungorum, endosymbiotic bacteria, which species, B. mallei, B. pseudomallei, B. plantarii, live within the cells of the fungus Rhizopus microsporus B. gladioli, B. glumae, etc.). Three minor subgroups and produce the causal agent of rice seedling blight, are also recognizable, corresponding to BCC, rhizoxin, and the toxic cyclopeptide rhizonin, do not B. pseudomallei group and plant-pathogens group. group with the other endosymbiotic species of the The BCC is a collection of genetically distinct but non-pathogenic cluster, but are very close to the phenotypically similar bacteria that belong to at least pathogenic species B. mallei and B. pseudomallei as 17 species [1]. BCC species have been isolated well as to B. caryophylli, a parasitic endophytic species from a variety of natural habitats such as plant infecting vascular plants [11]. It is worth noting that rhizosphere, soil and river water and from several recently B. rhizoxinica and B. endofungorum have urban environments such as playgrounds and athletic also been recovered from clinical specimens, probably fields, and although first described as the causal agent as a consequence of patient infection by the fungus of onion rot, they have generally useful properties for Rhizopus [12]. biocontrol, bioremediation and plant growth promotion The second and more recently established [6]. However, BCC bacteria are also recognized as lineage in the genus Burkholderia comprises more important opportunistic pathogens that can cause than 25 related environmental species, which in most variable lung infections in cystic fibrosis patients, which cases are non-pathogenic and have been found to result in asymptomatic carriage, chronic infection be associated with plants [4]. Several interesting or ‘cepacia syndrome’, which is characterized by a properties found in members of this cluster include rapid decline in lung function and can include invasive (i) the strong catabolic potential to degrade aromatic disease and death. compounds, with B. xenovorans being the best known B. pseudomallei and B. mallei are two highly example; (ii) the potential to increase plant nutrient pathogenic bacteria, responsible for melioidosis and availability via nitrogen fixation and/or phosphate glanders, respectively [3,7]. Melioidosis, which affects solubilisation, as demonstrated for B. unamae, humans, is endemic in Southern Asia and northern B. tropica, and B. silvatlantica; (iii) the ability to Australia, and its etiological agent, B. pseudomallei, colonize the rhizosphere or the internal intercellular is an environmental saprophyte that is commonly spaces in several plants and promote plant growth, as found in wet soils and stagnant waters throughout the is the case for B. kururiensis and B. phytofirmans; and endemic regions [3]. B. mallei, the etiological agent of (iv) the ability to form symbiotic interactions with plants glanders, cannot persist in the environment outside as occurs, for example, with B. tuberum, B. phymatum, its equine host. Horses are the primary carriers of B. mimosarum, B. nodosa, and B. sabiae, and disease and are largely responsible for transmitting with mosses, as reported for B. megapolitana and the infection to healthy animals and humans [3]. These B. bryophila. Although root-nodule symbionts, like two species are phylogenetically very similar and have pathogens, form an intimate association with their nearly identical 16S ribosomal DNA sequences. They eukaryotic hosts, all the symbiotic Burkholderia isolates have been defined as separate species essentially belong to the non-pathogenic lineage. 998 P. Paganin et al. 3. Pathogenicity of Burkholderia infections, than with mounting a potent acute infection species [15]. All BCC species can be isolated from clinical The most important Burkholderia species in terms of samples as well as from the natural environment, which pathogenic potential are B. mallei, B. pseudomallei and could be acting as a constant “reservoir” for infectious the BCC species [13]. B. mallei and B. pseudomallei BCC pathogens [16]. Furthermore, most BCC species have