Microb Ecol (2012) 63:249–266 DOI 10.1007/s00248-011-9929-1

MINIREVIEW

Common Features of Environmental and Potentially Beneficial Plant-Associated

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, 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 , such as most studies have thus far focused on the pathogenic Burkholderia glumae, Burkholderia pseudomallei,and species due to their clinical importance. However, the , 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 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 continued to be Today, the Burkholderia genus comprises 62 validly recognized as members of the non-fluorescent pseudomo- described species, and their 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 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 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 characteristics References

B. acidipaludis Endophyte, rhizosphere Eleocharis dulcis nif+aluminum tolerant [2] B. bannensis Rhizosphere Panicum repens nif+ [2] B. bryophila Associated with mosses A. palustre, S. palustre, S. rubellum Growth promotion in lettuce, antifungal activity [149] B. caledonica Rhizosphere, sandy soil Vitis vinifera acdS, braI/R [37] B. caribensis Nodules, vertisol Mimosa diplotricha nif+, nod, acdS, braI/R, high EPS production [1] B. ferrariae Soil Iron ore nif+, phosphate solubilizer [146] B. fungorum Fungal P. chrysosporium braI/R, acdS, aromatic compound degrader [37] B. graminis Rhizosphere Zea mays, L. deliciosus, P. pinea, acdS, braI/R, may induce systemic resistance and [16, 155] S. lycopersicum tolerance to salt and drought B. ginsengisoli Rhizosphere Panax ginseng β-Galactosidase activity [76] B. heleia Rhizosphere Eleocharis dulcis nif+, grow in acidic environments [2] B. hospita Soil A/B horizon agricultural soil braI/R, acceptor of plasmids pJP4. pEMT1 [59] B. kururiensis Endophyte, rhizosphere, Oryza sativa, Manihot esculenta, nif+, acdS, braI/R, plant-growth promotion, [5, 10] TCE3 soil Mussa acuminata, Nicotiana aromatic compound degradation tabacum B. megapolitana Associated with mosses A. palustre Plant growth promotion, antifungal activity [149] B. mimosarum Nodules Mimosa pigra, Mimosa pudica, nod+, nif+, braI/R, main endosymbiont [29] Mimosa scrabrella Mimosa spp. B. nodosa Nodules M. bimucronata, M. scrabrella nif+, nod+, nodulates Mimosa roots [28] B. oxyphila Acidic soil Acidic forest soil Catabolizes (+)-catechin into taxifolin [106] B. phenazinium Soil, associated with mosses Unknown, S. rubellum braI/R, produces ionidin, acidophilic [70, 155] B. phenoliruptrix Isolated from a chemostat Unknown acdS, braI/R, degrades halogen–phenol [36, 74, 75] with 2,4,5 T Trichlorophenoxyacetic acid substituted compounds B. phymatum Nodules Mimosa spp., Phaseolus vulgaris nif+, nod+, acdS, braI/R, N-fixation in vivo [139, 147] and ex planta B. phytofirmans Endophyte, rhizosphere Allium cepa, Solanum spp., Oryza acdS, braI/R, plant growth promotion, antifungal [52, 127] sativa activity B. sabiae Nodules Mimosa caesalpiniifolia nif+, nod+, PHA production [27] B. saccharii Soil Saccharum officinarum braI/R, PHA production [21] B. sartisoli Rhizosphere, PAH–soil, Zea mays Aromatic compound degradation [153] compost

B. sediminicola Water sediments PHA production [81] al. et Suárez-Moreno Z.R. B. silvatlantica Rhizosphere, endosphere Zea mays, S. officinarum, A. comosus nif+, acdS, braI/R, plant growth promotion [114] B. terrae Soil, rhizosphere Broad-leaved soil forest, Lycopersicum nif+, braI/R [76, 160] esculentum B. terricola Soil acdS, braI/R, acceptor of plasmids pJP4. pEMT1 [59] B. tropica Rhizosphere, endophyte S. officinarum, L. esculentum, Zea mays, nif+, acdS, braI/R, production of PHAs and EPS, [119] A. comosus plant-growth promotion B. tuberum Nodules Cyclopia spp., Macroptilium atropurpureum nif+, nod+, acdS, braI/R, nodulates several plants [98, 147] Beneficial Burkholderia 253

Biogeography and Distribution ] PCB 58 ], of the Beneficial-Plant-Environmental (PBE) ] , 137 37 20 Burkholderia Cluster [ [

PBE Burkholderia have been isolated from all of the continents. In fact, strains from the same species have been recovered from distant locations and from very different niches. For instance, Burkholderia caribensis strains were first isolated from a vertisol in Martinique and were later isolated from nodules of Mimosa spp. in Taiwan and China [1, 82]; Burkholderia graminis strains were isolated from rhizosphere soils in both France and Australia [155], and

are specified in the text strains of Burkholderia tropica have been identified in the rhizosphere of species of Poaceae (sugarcane, maize, and , phenol and benzene degradation, , PCB degradation, associated teosinte) in Mexico, Brazil, and South Africa [119]. verified presence of the BraI/R QS system [ braI/R

braI/R Although many of them have been identified in , , association with plants, with which they may have braI/R acdS acdS epiphytic, endophytic, or endosymbiotic interactions, spe- , ], +, plant-growth promotion with plants cies from this PBE cluster may be also found free-living in 105 the soil or even associated with fungi and insects. So far, species of this group have not been reported to cause a polyaromatic hydrocarbons detrimental effect on plant (or animal) hosts, and some are

PAH currently under evaluation to assess their potential as biofertilizers and biocontrol agents owing to their plant growth-promoting effects, whereas some are considered as

Coffea arabica nif+ potential candidates for rhizoremediation. ,

trichloroethylene, Burkholderia in the Rhizosphere and in Association Coffea arabica nif ,

TCE with Fungi S. officinarum , The rhizosphere is a biologically active zone of the soil

verified presence of ACC deaminase gene [ around plant roots that contains soil-borne microbes, Zea mays S. lycopersicum including bacteria and fungi. The rhizosphere is the most acdS frequent habitat for PBE Burkholderia (Table 1). It has been speculated that such preference may be associated with their catabolic versatility which enables them to degrade root exudates and other root-derived compounds, and thus

exopolysaccharide production, to persist on the root surface [26]. A considerable number

EPS of Burkholderia unamae, B. xenovorans, B. tropica, and Burkholderia silvatlantica strains have been recovered from

verified plant nodulation, the rhizosphere, which suggests that this could be their

nod main niche [24, 25, 50, 113]. Burkholderia heleia, Burkholderia bannensis, Burkholderia acidipaludis, Bur-

genes, kholderia oxyphila, and Burkholderia ginsengisoli have also been recovered from the rhizosphere, but their species nifH polyhydroxyalcanoates, descriptions are based only on a few isolates, and hence Endophyte, roots, rhizosphere Rhizosphere, PCB-polluted soil conclusions about their occurrence and diversity requires PHA further research [2, 3, 81]. It is possible that plants have preferences for particular rhizospheric Burkholderia species, and that geographical (continued) location may also be a factor in this preference. For

+ verified presence of instance, B. unamae, which occurs in the rhizosphere of Table 1 SpeciesB. unamae Isolated from Host Relevant characteristics References B. xenovorans The references correspond to thenif description and isolation reports for each species, while the identification of the genes and other relevant traits polychlorobiphenyl, maize, coffee, sugarcane, and tomato, has been found to be 254 Z.R. Suárez-Moreno et al. prevalent in the rhizosphere of sugarcane in Mexico, but plants (Table 1) and therefore are considered to be putative not in Brazil, even though other Burkholderia species were endophytes awaiting confirmation of their endophytic isolated under the same conditions [24, 25, 113]. Similarly, nature via detailed microscopical studies [71]. A primary B. tropica was found to be prevalent in the rhizosphere of focus of the study of these endophytic and putatively sorghum and maize in Mexico, whereas B. silvatlantica was endophytic Burkholderia species is their potential for plant- recovered from the rhizosphere of maize and sugarcane in growth promotion [38]. B. phytofirmans PsJN is one of the Brazil [113, 160]. most studied endophytes and it has greatly contributed to Some species may not only occur in the rhizosphere but our understanding of plant–endophyte interactions. This also in other niches, such as the bulk soil. For example, B. strain was isolated in 1991 as a contaminant from onion xenovorans LB400T was recovered from a polychlorobi- roots infected with the mycorrhizal fungus Glomus vesicu- phenyl (PCB)-polluted soil, but several other B. xenovorans liferum [52]. Colonization experiments in tomato, grape- strains have also been isolated from the rhizosphere of vine, and several potato varieties with strain PsJN have coffee and tomato [20, 25, 58]. Similarly, Burkholderia shown that it is able to colonize the rhizosphere and the sartisoli, originally isolated from polycyclic aromatic plant interior, resulting in a pronounced enhancement of the hydrocarbon (PAH)-polluted soils, was recently recovered root system, including more adventitious secondary roots from the rhizosphere of maize and from compost heaps with higher lignin deposition, as well as increased leaf area [153]. Burkholderia caledonica, which exists in sandy and improved water use efficiency [12, 52, 102, 103, 115]. soils, was also recovered from the rhizosphere of Vitis B. phytofirmans PsJNcanalsoinduceresistanceingrapevine vinifera in Scotland [37]. Other species, such as the to Botrytis cinerea, the causal agent of gray mold, and can legume-nodulating Burkholderia phymatum or the soil increase the growth of grapevine at low temperatures [12, inhabitant Burkholderia terrae, may also live in the 13]. Other B. phytofirmans strains have been recovered from rhizosphere of tomato [160]. agricultural soils in the Netherlands, the interior of rice in Interestingly, one species from the PBE Burkholderia Korea, and from sugarcane in Brazil [84, 99, 124]. cluster was described as being associated with a mycorrhi- Another recognized and studied putative endophyte is B. zal fungus [156–158]. B. terrae was isolated from the kururiensis M130, formerly named “Burkholderia brasi- mycosphere of Laccaria proxima, probably because 15 of lensis”, which was originally isolated from surface- 18 compounds that have been found in fungal exudates are sterilized rice roots in Brazil, although strains from the utilized by this bacterium. This species is also able to same species have also been recovered from cassava, migrate and grow with growing fungal hyphae through the banana, pineapple, and sugarcane [10]. Subsequent taxo- soil [157, 158], a feature that presumably allows the bacteria nomical analysis, including 16S rRNA, nifH, glnB, as well to respond to a growing mycosphere, and to find its preferred as other markers, determined that “B. brasilensis” M130 ecological niche within it. Later studies showed that B. terrae was actually a strain of B. kururiensis [25, 89]. The BS001 is also able to help the migration of migration- infection of rice by B. kururiensis has been examined using negative bacteria, which could be useful for biocontrol and scanning electron microscopy (SEM) and transmission even bioremediation [156]. For instance, non-migrating plant electron microscopy (TEM) [93]. This study has shown growth-promoting rhizobacteria or pollutant-degrading that although most of the bacteria are surface dwelling, bacteria could be translocated via fungal hyphae with the some appear to enter the roots and spread up to the aerial help of B. terrae BS001. It is likely that other Burkholderia– parts, possibly through the xylem [93]; this process may be fungus interactions may be discovered in the future. mediated by cell wall-degrading enzymes, similar to what has been previously observed during plant colonization by Endophytic Burkholderia B. phytofirmans PsJN [39, 40]. Indeed, the aggressive entry of other confirmed endophytic bacteria in rice, such as Endophytes are defined as those bacteria able to colonize Azoarcus [68], [63], and Herbaspir- the internal tissue of the plant without causing external illum seropedicae [64, 72], has been demonstrated. How- signs of infection or negative effects on their host. Although ever, it should be noted that unlike the latter studies which the presence of bacterial endophytes in plants is variable, used reporter gene-tagged strains and specific antibodies to they are often capable of enhancing plant development via examine samples embedded in resin for light microscopy various mechanisms, including BNF, plant hormone pro- and TEM, the study by Mattos et al. [93] used unmarked duction, phosphate solubilization, siderophore production, wild-type strains, and their microscopical observations and antagonistic effects against phytopathogens [7, 8, 38, mainly relied upon SEM, which is a technique subject to 66, 121]. B. tropica, B. kururiensis, B. unamae, B. artifacts, particularly the potential to move surface bacteria silvatlantica, Burkholderia phytofirmans, and Burkholderia into the internal tissues during sample processing [71]. This acidipaludis have all been isolated from surface-sterilized means that we cannot be sure as yet that the bacteria Beneficial Burkholderia 255 observed by Mattos et al. [93] are genuinely endophytic, Machaerium lunatum [98], B. phymatum was also found and further microscopy studies with reporter gene-tagged B. to be a Mimosa nodulator by Elliott et al. [48], who had kururiensis strains and/or with antibodies specific to B. noted that its nodA gene sequence was very close to that of kururiensis are required. Mimosa-nodulating β-rhizobia, such as B. mimosarum and BCC species are also often recovered as putative C. taiwanensis. A later study by dos Reis Junior et al. [42] endophytes of agriculturally important plants, such as rice extended the number of Mimosa spp. that can be nodulated and maize [60, 96], but their potential pathogenicity has by B. phymatum to more than 40 (Fig. 2a). It has also been impaired further biotechnological applications [50, 109]. shown to be highly promiscuous outside the genus Mimosa, For example, B. vietnamiensis strains have been isolated nodulating several legumes in the sub-family Mimosoideae, from rice, and they have shown significant yield increases such as species of Piptadenia (Fig. 2c). when used as inoculants on this crop in Vietnam [142], but The relationship between β-rhizobia and Mimosa was because B. vietnamiensis is within the BCC group, these investigated in a large-scale study by Bontemps et al. [19] rice growth-promoting strains cannot be used in agriculture. who isolated rhizobia from 50 Mimosa spp. in the Cerrado and Caatinga biomes of central Brazil, where the large genus Legume-Nodulating Burkholderia Mimosa has evolved and diversified into more than 200 native and endemic species (Fig. 2a, b). All of the species Legume-nodulating bacteria, collectively called rhizobia, were found to be nodulated by Burkholderia, and the live as saprophytes in the soil and in facultative phylogenies obtained from the concatenated 16S rDNA and with plants. They induce the formation of root nodules, recA sequences of the isolates showed that they were closely where they fix atmospheric nitrogen and provide it to the related to the known legume-nodulating Burkholderia plant in exchange for carbon compounds [91]. Although the species, but were in seven deep and distinct clades that variety of legume-nodulating bacteria has been expanding probably represented seven new species [62]. Bontemps et greatly since the original description of Rhizobium, with al. [19]alsodemonstratedthatthenifH and nodC gene many new genera being shown to nodulate [61], until 2001 phylogenies were highly congruent with the 16S rRNA/recA it was originally assumed that these bacteria were still phylogenies, suggesting that horizontal gene transfer (HGT) restricted only to the class. In this year, was uncommon, and that these symbiosis-related genes had however, the possibility that legumes were also nodulated not been recently acquired from other legume-nodulating by was raised by the report of isolation bacteria, e.g., Rhizobium. Indeed, a major conclusion of the of Ralstonia taiwanensis (now renamed Cupriavidus study by Bontemps et al. [19] was that Burkholderia was an taiwanensis) from two invasive Mimosa species in Taiwan ancient symbiont of legumes, at least 50 million years old, [33]. In the same year [98], Moulin and colleagues showed which would mean that it was possibly extant at the time that evidence of potential nodulation by two strains of Burkhol- nodulation was first evolving in legumes[134], and definitely deria. However, although light and electron microscopy extant at the time that Mimosa evolved 28 million years ago with GFP-tagged strains and measurements of nitrogenase [62]. activity were soon reported for C. taiwanensis [32], Although Burkholderia (and C. taiwanensis) are the confirmation of effective symbiotic nodulation of legumes most common symbionts to be isolated from Mimosa spp., by Burkholderia had to wait until 2005 when similar GFP/ some species of this legume can also be nodulated by microscopy-based studies using strains of Burkholderia Rhizobium [14, 49], but it should be noted that the nod mimosarum and Burkholderia nodosa were published by genes of the Rhizobium strains so far shown to nodulate Chen et al. [30]. Mimosa are very different from those of the Mimosa- Interestingly, however, both Chen et al. [30, 31] and nodulating β-rhizobia [19, 49], as would be expected if Barrett and Parker [14, 15] showed that Burkholderia (and they had evolved separately [62]. Elliott et al. [49] C. taiwanensis) appeared only to be symbiotic with compared the ability of Rhizobium and C. taiwanensis to legumes from the sub-family Mimosoideae, particularly compete with Burkholderia spp. for nodulation of three with Mimosa spp. (Fig. 2a, b). The close affinity between invasive Mimosa spp. (Mimosa diplotricha, Mimosa pigra, β-rhizobia and Mimosa was further demonstrated by the Mimosa pudica). They found that B. mimosarum and B. isolation and identification of a number of new Burkholde- phymatum always outcompeted Rhizobium and C. taiwa- ria species from a variety of Mimosa spp., particularly in nensis to the point of total exclusion, but most particularly South and Central America. The new Mimosa-nodulating if the concentration of mineral N (ammonium or nitrate) in Burkholderia spp. so far includes B. mimosarum, B. the growth medium was very low; the competitive ability of nodosa, and Burkholderia sabiae [27–29], but at least three the Burkholderia strains was reduced in favor of the other others are currently being described (see review by [62]). rhizobial types (e.g., C. taiwanensis) only when N was Surprisingly, given that it was allegedly isolated from increased. The preferential nodulation of Mimosa by 256 Z.R. Suárez-Moreno et al.

Figure 2 a The Brazilian native legume, Mimosa ursina, nodulated Mimosa spp. examined so far (approximately 100) are Burkholderia by either Burkholderia phymatum STM815 (left)orCupriavidus strains, many of them belonging to new and so far undescribed species taiwanensis LMG19424 (right). In comparison to the plant inoculated in the plant-beneficial group. c Section through a nodule on the roots with C. taiwanensis, the one inoculated with B. phymatum is green of Piptadenia stipulacea (Mimosoideae), a tree endemic to the and healthy, and its roots have large N2-fixing nodules (arrow). b Caatinga biome in Brazil, which is closely related to Mimosa, and is Section through a nodule on the roots of Mimosa pseudosepiaria,a also nodulated by Burkholderia. d Section through a nodule on the species endemic to the Chapada Diamantina in Brazil. Central Brazil South African endemic legume Podalyria canescens (Papilionoideae) is the major center of Mimosa radiation, with more than 200 native infected with a green fluorescent protein (GFP) variant strain of species, most of them endemics, and the symbionts of all Brazilian Burkholderia tuberum STM678

Burkholderia in low fertility soils shown by Elliott et al. [49] Recent studies have extended the nodulation of legumes in laboratory studies would help to explain why Burkholde- by Burkholderia to the other sub-families, such as the ria are so predominant in Mimosa spp. in natural ecosystems Papilionoideae, but there are distinct preferences in terms of such as the Brazilian Cerrado and Caatinga where soils are the host range of Papilionoideae-nodulating Burkholderia, very low in N (and acidic, which would also favor and these are based upon the nodulation genes. For Burkholderia;[42]). On the other hand, two of the pan- example, B. tuberum STM678 has a very different nodA tropical Mimosa spp. used in the study of Elliott et al. [42], gene sequence from all the other (all Mimosa-) nodulating M. diplotricha and M. pudica, are commonly found as Burkholderia spp. so far described [31]; it can nodulate invasive weeds on roadsides and wasteground, where soils members of the genus Cyclopia, which is a Papilionoid can be highly fertile, and it is thus possible that this fertility genus native to South Africa [47], but as would be selects against their nodulation by Burkholderia and favors predicted from the phylogenies of its nod genes, it cannot other rhizobial types. This appears not be the case, however, nodulate Mimosa or other members of the Mimosoideae for the other invasive species in the study, M. pigra.This [47]. Interestingly, it can also nodulate other South African species has a strong preference for nodulating with Burkhol- genera related to Cyclopia in the same tribe, the Podalyr- deria regardless of soil fertility [30, 31, 49], thus suggesting ieae, such as Podalyria (Fig. 2d;[62]), but it has not so far that the competitive ability of Burkholderia to nodulate not been demonstrated to nodulate species in the genus particular Mimosa spp. results from an interaction between Aspalathus (tribe Crotalarieae), which, although not close- plant phylogeny and soil environment, with the former being ly related to the Podalyrieae, grow in the same acidic soils more important than the latter in the case of M. pigra [48]. of the South African Cape Fynbos biome, and thus will be Beneficial Burkholderia 257 exposed to the same nodulating microflora, including Features of the PBE Burkholderia Cluster Burkholderias. Burkholderia tuberum can also effectively nodulate Siratro (Macroptilium atropurpureum)[47], which As described above, this group of PBE Burkholderia is in the tribe Phaseoleae. Garau et al. [53] in their study of species have common niches resulting in a beneficial Rhynchosia ferufolia, another legume in the tribe Phaseo- interaction with many different plants. Although they are leae that is native to the acidic soils of the South African now beginning to receive considerable attention from the Cape, have shown that it is also nodulated by Burkholderia scientific community, the physiological and molecular strains with nodA genes similar to that of B. tuberum mechanisms underlying these plant–Burkholderia interac- STM678. tions are far from clear. In the next section, we have briefly It would thus appear that there are at least two groups of described some of the general properties of PBE cluster and legume-nodulating Burkholderias defined and separated not have then focused in more detail upon properties that may by their core genomes nor by their nif genes (which are be considered as important for their existence in close closely related; [19]), but geographically, and by their association with plants. nodulation genes. These are the Mimosoid-nodulating Burkholderias centred on South America (e.g., B. mimosa- General features rum, B. nodosa, B. phymatum, B. sabiae)andthe Papilionoid-nodulating Burkholderias centered on South Members of the PBE group of Burkholderia have a strictly Africa (e.g., B. tuberum). Interestingly, however, although respiratory type of metabolism with oxygen as the terminal the Papilionoid-nodulating B. tuberum-type symbionts electron acceptor. Moreover, with the exception of B. appear not to be capable of nodulating Mimosoids [47, sartisoli, most species are also able to reduce nitrate to 53], the opposite is not the case with some of the Mimosa nitrite, but they do not denitrify [153]. Similarly, with the nodulators. For example, strains of the highly promiscuous exception of a recently proposed strain of B. kururiensis species, B. phymatum, have recently been isolated from subsp. thiooxydans, none of the species from this group nodules on common bean (Phaseolus vulgaris) in Morocco have exhibited chemolithoautotrophic growth with thiosul- by Talbi et al. [139]. These strains have nodA genes similar fate, tetrathionate, or sulfur [5]. The cellular fatty acids to B. phymatum STM815 and can nodulate Mimosa spp., typically found in plant-beneficial Burkholderia contain 14, but are also capable of nodulating common bean and fixing 16, 17, and 18 carbon atoms (C16:0,C17:0 cyclo, and C18:0 N2 in this highly important agricultural plant. ω7c), with C16:0 3OH as the most characteristic. Two Further isolation of bacteria from the huge numbers of different ornithine lipids may be present in some species, (mainly tropical) legumes that remain to be described in and ubiquinone Q-8 has been found to be the predominant terms of their bacterial symbionts will no doubt reveal new quinone system [55, 107, 161]. Catalase is produced, groups of nodulating Burkholderias, not to mention although oxidase activity may vary between species. completely new types of “rhizobia” to add to the current The GC content in plant-beneficial Burkholderia alpha and beta subdivisions. However, at present it would species ranges from 61.2% to 64%. Five genome projects appear that all of the known β-rhizobia are taxonomically have been completed, namely B. xenovorans LB400T [26], located in the group of beneficial Burkholderia [19], as B. tuberum STM678T, B. phytofirmans PsJNT [159], B. although BCC strains are frequently isolated from legume phymatum STM815T,andB. graminis C4D1MT (http:// nodules [117, 147], none have been confirmed as nodulat- genome.jgi-psf.org/programs/bacteria-archaea/index.jsf), ing symbionts [62]. For example, approximately 100 whereas the genomes of B. unamae MTI-641T, B. beneficial Burkholderia and 20 BCC isolates were isolated silvatlantica SRMrh-20T,andB. seminalis 0901 are during the study of Bontemps et al. [19], but only the currently being sequenced (http://www.ncbi.nlm.nih.gov/ beneficial Burkholderia isolates tested positively for the genomes/lproks.cgi). A comparison of the available presence of nodC and for their ability to nodulate Mimosa genomes has revealed high levels of synteny [26, 159], pudica. Given the lack of confirmed positive reports of and, furthermore, an analysis of the chromosomes from their ability to nodulate, and the large number of negative several species has suggested that genome sizes in the reports, it is safe to say that, although it cannot be PBE Burkholderia group range from 6.5 to 9.7 Mbp. completely excluded, current evidence is largely against These genomes are divided among several chromosomes the likelihood that members of the BCC are symbiotic with and megaplasmids, which are conserved within strains of legumes. It is likely, however, that BCC bacteria use the the same species [90]. An important exception is B. epidermal and cortical tissues of nodules as a niche, and xenovorans, in which the type strain (LB400T)hostsa possibly some are also genuinely endophytic and actually 1.47 megaplasmid that is absent in most strains, although live within nodules, as has been described for some 0.8-Mbp plasmids have also been detected in strains enterobacteria [100]. LMG16224 and LMG22943. 258 Z.R. Suárez-Moreno et al.

Exopolysaccharide (EPS) production has long been which thus enhance the host plants pollutant-degrading shown to be essential for the colonization of plants and ability [128]. for attachment by plant-associated bacteria (reviewed by Leigh and Coplin [78]). Some members of the PBE Nitrogen Fixation Burkholderia group, such as B. caribensis, B. kururiensis, and B. tropica, have shown a remarkable synthesis of EPS. Importantly, the ability to fix nitrogen is a major feature of These polysaccharides have distinct repeating units and species in the PBE Burkholderia group, although it should different monosaccharide proportions, but they show be noted that it is not exclusive to this group, as it has also particular structural similarities, such as the presence of been described in the BCC species B. vietnamiensis [55, carboxylated groups and high levels of O-acetylation [1, 65, 95]. B. unamae, B. xenovorans, B. kururiensis, B. silvat- 92, 126]. The molecular structure of EPS has been lantica, B. tropica, B. bannensis, B. heleia, B. terrae, and B. determined for B. caribensis, B. tropica, B. phytofirmans, gisengisoli are the most common diazotrophs found and B. kururiensis [94, 116, 129, 150], and the three- associated with (non-legume) plants [24, 25, 32, 50, 98, dimensional structure was recently elucidated by molecular 113, 119], while Burkholderia ferrariae has been isolated dynamic studies in the cases of B. caribensis and B. tropica from the bulk soil (i.e., it is a free-living nitrogen fixer), and as well as the pathogenic species B. cepacia [116, 150]. B. sabiae, B. tuberum, B. phymatum, B. mimosarum, and B. Recent studies have also revealed similarities between nodosa can fix nitrogen in symbiosis with legumes [62]. 15 cepacian (EPS produced by members of the BCC complex) N2 isotope dilution assays have revealed unambiguous and the EPS synthesized by B. graminis, B. phytofirmans, diazotrophy in B. unamae, B. tropica, B. silvatlantica, B. B. phymatum,andB. xenovorans [51]. So far, both xenovorans, and B. kururiensis, and analyses of nifH gene structural and microbiological studies have suggested that sequences have shown a tight clustering among these and EPS may have a role in the tolerance of these species to other species from the group, such as B. mimosarum, B. iron stress, desiccation [51], and also in the aggregation of ferrariae, and B. phymatum [90]. It is worth noting that the soils, as has been shown for B. caribensis strains [150]. nif genes in B. tropica are located on a 450–600-kb However, it is believed that the main function of the EPS in plasmid, while in the other Burkholderia species the genes PBE Burkholderia could be in their attachment to root are located on the chromosome [90]. However, although surfaces, as this role for EPS has been shown to be essential nifH PCR assays have been positive for the B. bannensis for the colonization of plants by both symbiotic bacteria, and B. acidipaludis type strains, acetylene reduction assays such as Ensifer (Sinorhizobium) meliloti [112], and patho- and growth in N-limiting media have not been positive for genic bacteria, such as B. cepacia [41, 112]. these strains, and thus further studies are necessary to Species from the PBE Burkholderia cluster are also able determine their diazotrophy [4]. to utilize a large number of aromatic compounds as energy Remarkably, the observed congruence between phyloge- and carbon sources, and some have a considerable netic trees of 16S rRNA and nifH genes has indicated that biotechnological potential to reduce the concentration and the most likely common ancestor of all Burkholderia was a toxicity of chemical pollutants from the environment. diazotroph, and that this function has been inherited in most Strains of B. xenovorans, B. kururiensis, B. unamae, B. species and lost in others [19]. In fact, genome comparison sartisoli,andBurkholderia phenoliruptrix have been analyses have recently shown synteny between the nifHDK- recovered from polluted soils, and they are able to tolerate nifENX from B. vietnamiensis and B. xenovorans LB400T, and metabolize recalcitrant compounds [20, 24, 25, 36, 152, with a single indel related to the presence of a putative iscS 162]. B. xenovorans LB400T is probably one of the most gene in the B. xenovorans nif cluster [95]. studied xenobiotic-biodegrading bacteria. It was isolated The possible use of these Burkholderia spp. as biofertil- from a PCB-containing landfill in New York and is able to izers for the provision of biologically fixed nitrogen has degrade the widest range of polychlorinated biphenyl still to be properly evaluated. The use of B. tropica together (PCB) congeners, although it may also degrade isoflavo- with a bacterial consortium has been recommended in noids, abietan diterpenoids, and sulfonates [122, 125, 130– Brazil in order to increase sugarcane yield [120]. Impor- 132]. In recent years, microbial degradation of hazardous tantly, the positive effects exerted by diazotrophic Burkhol- compounds in the rhizosphere (rhizoremediation) and the deria are not only confined to the fixation of atmospheric use of plants to extract and degrade harmful substances N2 but to a combination of other mechanisms that increase (phytoremediation) have been considered as alternative the nutrient availability and promote the solubilization of strategies for decontamination of soils. Furthermore, it has phosphates and the iron uptake via siderophores [25]. been demonstrated that plants grown in polluted soils Owing to these properties, several species from this group naturally recruit endophytes and other plant-associated may thus be considered as plant growth-promoting bacteria bacteria with the necessary contaminant-degrading genes, (PGPB). Beneficial Burkholderia 259

ACC Deaminase and IAA Production rophores has also been verified in B. phytofirmans, B. unamae, B. kururiensis, B. xenovorans, B. tropica, and B. The lowering of plant ethylene levels through the action of silvatlantica, which suggests that these species may also the enzyme 1-aminocyclopropane-1-carboxylate (ACC) have biocontrol properties [25, 127]. Indeed, B. tropica is deaminase is one of the main mechanisms by which able to inhibit the growth in culture media of phytopatho- Burkholderia can promote plant growth. ACC is one of genic fungi, such as Fusarium culmorum, F. oxysporum, the precursors of ethylene synthesis in plants, and ACC and Colletotrichum spp. (unpublished results). Recently, it deaminase degrades it to ammonia and α-ketobutyrate [56]. was hypothesized that B. tropica might also have a role in A role for ACC deaminase in the promotion of plant growth controlling nematodes in sugarcane. Statistical analysis of has been shown in the endophytic species B. phytofirmans the occurrence of this species and Xhipinema elongatum and in the rhizospheric species B. unamae,asacdS indicated a negative correlation between the presence of the defective mutants of both species were impaired in their nematode and the bacteria, whereas a positive correlation promotion of growth of rapeseed and tomato, respectively was found between B. tropica and less pathogenic [105, 138]. Moreover, the ACC encoding gene, acdS, was nematodes. If these mathematical relationships can be found to be widely distributed in 20 species of the confirmed, then B. tropica could be inoculated on to Burkholderia genus, 14 of them belonging to the PBE sugarcane in order to attract the less pathogenic nematode cluster (Table 1). community, and thereby reduce damage to this crop [104]. Beneficial Burkholderia that inhabit the rhizosphere may also influence plant growth by contributing to their Quorum Sensing endogenous pool of phytohormones, such as auxins, as many potentially beneficial bacteria synthesize indole acetic The cell density-dependent regulation system known as acid (IAA). However, in the case of Burkholderia, although quorum sensing (QS) has been shown to play a determinant IAA production has been shown for B. kururiensis, B. role among the global regulatory mechanisms in members phytofirmans, and B. unamae, the biosynthesis pathway and of the BCC [45]. The most common QS signals in Gram- the mechanisms involved in the plant growth enhancement negative bacteria are N-acyl homoserine lactones (AHLs) remain to be elucidated [25, 138]. (reviewed by [6, 101]). In an AHL–QS circuit, AHLs synthesized by a LuxI-family protein bind a LuxR-family Plant-Protective Effects against Biotic and Abiotic Factors protein, which then becomes activated by exposing a DNA- binding that recognizes a palindromic lux box cis- Plant-beneficial Burkholderia species may also trigger element in the promoter region of the target genes [46]. disease resistance in the host plant by induced systemic Importantly, species of the BCC complex all share a resistance (ISR), e.g., B. phytofirmans strains can increase conserved AHL QS system called CepI/R, which produces resistance against potato, tomato, and grapevine pathogens and responds to N-octanoyl homoserine lactone (C8-HSL). [12, 102]. Several studies have correlated the expression of This system regulates virulence as well as several other some genes involved in the defensive response with genes important activities such as biofilm formation and side- expressed under conditions of salt and drought stress [18, rophore production [45, 67, 154]. In addition, B. cenoce- 83]. For example, recent in vivo experiments with isolates pacia, B. vietnamiensis, B. mallei, B. pseudomallei, and B. of B. graminis, a species which has been isolated from the thailandensis have been shown to harbor more than one rhizosphere of corn, pasture, and wheat, resulted in an AHL QS system, and thus produce numerous AHL signal enhancement in shoot height and neck diameter of tomato molecules [43, 44, 77, 87, 88, 144]. plants, as well as inducing a protective response to salt and Recent studies have shown that AHL–QS is also drought stress in this plant [16, 17]. widespread among the PBE Burkholderia group. The Production of siderophores by PGPB is considered to be production of AHLs was initially reported in the description important in the suppression of deleterious microorganisms of the species B. phytofirmans, B. megapolitana, and B. and soil-borne plant pathogens by monopolizing the bryophila [127, 149]. Further AHL screening of 27 strains available iron in the soil [83]. The presence of siderophores from 21 species of this group not only revealed that AHLs was reported in B. bryophila and B. megapolitana were produced by all the species tested but also showed the associated with the mosses Aulacomnium palustre, Sphag- overall similarity in their AHL production profiles, which num rubellum, and Sphagnum pallustre in Germany [149]. are comprised of several 3-oxo-AHL derivatives [137]. Importantly, strains of both species also exhibited antifungal Genetic characterization of the AHL–QS loci in B. and antibacterial activity, as well as plant growth promotion kururiensis M130T, B. unamae MTI-641T, and B. xenovor- in lettuce, thus making them promising candidates for ans LB400T has indicated that these three strains possess a biological control purposes [149]. The production of side- highly conserved AHL QS luxIR family pair designated as 260 Z.R. Suárez-Moreno et al. the BraI/R system (>75% similar at protein level). LB400 respond preferentially to 3-oxo-C14-HSL and are Interestingly, ortholog BraI/R-like systems were also found negatively regulated by the repressor RsaL, but positively in the sequenced genomes of the cluster mates B. phytofir- regulated by BraR proteins [137]. It was also revealed that mans, B. graminis, and B. phymatum, and in the type BraI/R-like systems are present in all members of the PBE strains of another 15 species [136, 137]. BraI/R-like cluster, but that they exhibit low overall similarity values systems from B. unamae, B. kururiensis, and B. xenovorans when compared with QS systems from the other Burkhol-

Figure 3 Phylogenetic analysis of the LuxIR pairs present in branch lengths in the same units as those of the evolutionary distances Burkholderia species. Thirty-four LuxI and LuxR sequences from used to infer the phylogenetic tree. Numbers at branch nodes are different Burkholderia and other species were retrieved from the bootstrap values. Phylogenetic analyses were conducted in MEGA4. NCBI database, concatenated, and aligned with ClustalW [141]. Red Concatenated LuxIR sequences from V. fisheri (LuxIR) were used as square shows the XenI2/R2-like systems and green square highlights outgroup. The acronyms XEN: B. xenovorans; UNA: B. unamae; the BraIR-like systems. The evolutionary history was inferred using KUR, B. kururiensis the neighbor-joining method [123]. The tree is drawn to scale, with Beneficial Burkholderia 261 deria species (<31%). Interestingly, however, they display was evaluated by transcriptomic analysis, and the results significant similarity to the LasI/R and PpuI/R AHL QS suggested that although the inoculation effects may depend systems from P. aeruginosa and P. putida, respectively on the strain, AHLs play a determinant role in the plant– [136], as is evidenced from a phylogenetic analysis of the endophyte interaction [143]. Further studies focused both on sequenced BraIR systems and other LuxIR pairs (Fig. 3). the detection of AHLs, their genetic mechanisms, and their The BraIR-like systems constitute a major commonality regulons, as well as on the production and perception of among the species in the PBE Burkholderia group since it other signals, need to be conducted in order to more fully has been found in all species so far tested, suggesting that understand the role of QS in the adaptability and versatility this QS system belongs to their core genomes, and most of the plant-beneficial group of Burkholderia. likely was originally present in their common ancestor. The BraI/R-like systems were found to positively regulate the production of EPS in B. kururiensis, B. unamae, and B. Concluding Remarks xenovorans, which also indicates the possible existence of a common core of targets. Other important traits such as the Burkholderia species are characterized by their versatility, and degradation of aromatic compounds, plant colonization, and by their ubiquity and diversity in both niches and environ- biofilm formation were found, however, to be regulated ments. Most of the species belonging to the emerging PBE in a species-specific manner, suggesting that they are Burkholderia group share important features which provide responsive to the environment [136]. It is possible that a them with advantages in their association with plants and conserved QS system among these species could facilitate with their immediate environments. These include multi- inter-species communication within the PBE Burkholderia replicon genomes nitrogen fixation, the ability to nodulate cluster, possibly providing advantages in multispecies legumes, and the ability to degrade aromatic compounds niche adaptation. (Table 1). Importantly, all of these species share a common Interestingly, B. xenovorans possesses an additional QS system, which therefore appears to be part of the core AHL–QS system designated XenI2/R2, producing and genome of this group of species. Several Burkholderia responding to 3-hydroxy-C8-HSL. In contrast to the BraI/ species belonging to this group also exhibit a considerable R system, XenI2/R2 is more similar to the LuxI/R pairs potential for bioinoculation and biocontrol. However, details present in other Burkholderia species (e.g., CciI/R, BpsI3/ of their relationships, genome contents, and adaptations to R3 among others) (Fig. 3) and is present in only six species specific niches (including plants) will become clearer as of the PBE cluster, with most of them in the graminis- more genomes from Burkholderia strains and species with xenovorans subclade. It is, however, surprisingly absent in diverse life styles are sequenced and made available for B. xenovorans strains other than LB400 [136]. These facts comparative genomic analyses. The diversity and versatility indicate that XenI2/R2 could have been acquired by lateral of this group of species is largely unexplored, and this gene transfer events at the strain level, although the reasons includes their production of secondary metabolites, which that could have triggered this event remain to be studied might have important practical applications. Finally, under- [80]. XenI2/R2 and BraI/R are not hierarchically organized standing the regulatory mechanisms underlying the striking and no phenotypes regulated by XenI2/R2 have so far been features of this group of Burkholderia species will help in identified. The advantages of harboring a second system, interpreting how they live in close non-pathogenic associa- and if the XenI2/R2 regulon overlaps with the BraI/RXEN tion with so many different kinds of plants. regulon, are not currently known, but the generation of double mutants and global transcriptome analysis could help answer these questions. Acknowledgments ZRSM was financially supported by an ICGEB fellowship. BGC PhD programme is funded by CAPES (Brazil). We Several insights have provided evidence for the important thank Paulina Estrada de Los Santos for reading the manuscript and role of AHL–QS in the interaction of PBE Burkholderia with useful suggestions. During the preparation of this review, our dear friend plants. For instance, a study of two B. graminis isolates and colleague Jesús Caballero-Mellado unexpectedly passed away; his reported that both strains were able to produce AHLs during warm friendship, availability, and important contributions in this research field are very sadly missed. EKJ thanks NERC (UK) for funds, and the colonization of the rhizosphere of tomato. Moreover, numerous colleagues and collaborators for participating in the NERC- effects on plant growth promotion and protection from funded Beta-rhizobia project. salinity and stress were altered by the presence of AHLs produced by transgenic tomato plants, although this effect was strain dependent [17]. In a similar study, a lactonase- References expressing vector was mobilized into B. phytofirmans PsJN to reduce the production of AHLs, and experiments on two 1. Achouak W, Christen R, Barakat M, Martel MH, Heulin T potato cultivars were performed [143]. The potato response (1999) Burkholderia caribensis sp. nov., an exopolysaccharide- 262 Z.R. Suárez-Moreno et al.

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