Journal of Nematology 35(2):208–211. 2003. © The Society of Nematologists 2003. Strains from the Burkholderia cepacia Complex: Relationship to Opportunistic Pathogens1 Peter Vandamme2 and Eshwar Mahenthiralingam3 Abstract: Burkholderia cepacia-like organisms attract much interest from the agricultural industry as natural promoters of plant growth and biological control agents, and for bioremediation. Some of these organisms, however, cause life-threatening infections, particularly in cystic fibrosis patients for whom this multi-resistant bacterium is a major pathogen. The biodiversity of this group of bacteria is severely underestimated, and current identification procedures are inadequate. Presumed B. cepacia isolates belong to at least nine distinct genomic species (genomovars), referred to collectively as the B. cepacia complex. All these B. cepacia complex genomovars have been isolated from clinical and environmental sources. There are no phenotypic, genomic, or taxonomic grounds to differentiate environmental and clinical strains of the B. cepacia complex or to use the source of isolation to assess the safety of biopesticides containing members of the B. cepacia complex. Key words: Burkholderia cepacia complex, cystic fibrosis, epidemiology, genomovar, strain typing. Burkholderia cepacia is an extremely versatile organism tions caused numerous deaths in cystic fibrosis popula- that is truly considered both a friend and foe to humans tions worldwide and new guidelines were issued to re- (Govan et al., 2000). It is a genuinely ubiquitous organ- duce the risk of B. cepacia acquisition (Govan and ism with soil, water (including antiseptic and pharma- Deretic, 1996). More recently, serious outbreaks with ceutical solutions, and seawater), animals, plants, and fatalities have occurred in non-cystic fibrosis patients humans as niches. Although originally known as a plant treated in intensive care units in Europe and North pathogen, it is now also recognized as a most useful America (Holmes et al., 1999; Ledson et al., 1998). organism with a range of biotechnological applications There have been few reports of B. cepacia infection in that include biocontrol, bioremediation, and plant- veterinary medicine. Burkholderia cepacia has been re- growth promotion. However, it simultaneously has be- ported in mixed culture in clinical specimens from come notorious as a naturally multi-resistant and life- horses with pneumonia and in specific-pathogen-free threatening pathogen in immune-suppressed hosts piglets, as the sole organism involved in a case of veg- such as cystic fibrosis patients and patients with chronic etative endocarditis in a horse, and as the causative granulomatous disease (LiPuma, 1998; Speert, 2001). agent of an epidemic outbreak of subclinical mastitis Infections in humans and animals: The genus Burkhol- associated with infection in a large flock of milking deria comprises several established human pathogens. sheep (Berriatua et al., 2001). Before the early 1980s, reports of human infections Biotechnological applications: Care and concern for the caused by B. cepacia were sporadic and generally re- environment urge scientists, private firms, and legal au- stricted to hospitalized patients exposed to contami- thorities to develop biological alternatives to the nated disinfectant and anesthetic solutions in which present chemical controls in the agro-industry, thereby this highly adaptable saprophyte survives for long peri- reducing environmental chemical pollution (Parke and ods (LiPuma, 1998). A rising incidence, particularly in Gurian-Sherman, 2001). The major reasons for the in- patients with cystic fibrosis, was noted during the early terest in bacterial biopesticides or bioremediation are 1980s. Cystic fibrosis is the most common lethal inher- to provide environmentally benign means of control- ited disease of Caucasian populations, with pulmonary ling pests, remove toxic and other dangerous chemicals infections as the major cause of morbidity and mortal- from the environment, or use environment-friendly fer- ity. Infection or colonization by B. cepacia leads to dif- tilizers. Control of plant diseases, insects, and nema- ferent outcomes in different patients (Mahenthiralin- todes by bacteria and fungi has been proposed as an gam et al., 2001). However, a prime cause for concern alternative or supplement to chemical pesticides such is that pulmonary colonization reduces survival by 50% as captan, thiram, and thiobendazole. Roots and rhizo- and that about one-third to one-half of the patients spheres of various economically important crops in- succumb to “cepacia syndrome,” a rapidly fatal necro- cluding corn, maize, rice, pea, sunflower, and radish tizing pneumonia, sometimes accompanied by bacte- can be colonized by B. cepacia-like organisms, some of remia (Govan and Deretic, 1996). During the 1980s which produce a variety of antimicrobial compounds and 1990s, several major outbreaks of B. cepacia infec- that are active against soil pathogens (Govan and Van- damme, 1998; Parke and Gurian-Sherman, 2001). Us- ing these B. cepacia-like organisms as seed inoculants or 1 Symposium paper presented at the 40th Annual Meeting of the Society of root dips for biological control of pathogens that cause Nematologists, 25–29 August 2001, Salt Lake City, UT. 2 Laboratorium voor Microbiologie, Faculteit Wetenschappen, Universiteit rot of seeds or seedlings can increase crop yields sig- Gent, Ghent, Belgium. nificantly. In addition, in absence of soil pathogens, a 3 School of Biosciences, Cardiff University, Cardiff, United Kingdom. E-mail: [email protected] significant growth-promoting effect has been reported. This paper was edited by B. C. Hyman. The exceptional nutritional potential of some B. ce- 208 B. cepacia Complex Taxonomy: Vandamme, Mahenthiralingam 209 pacia strains is also used in the bioremediation of haz- TABLE 1. Current Burkholderia species and their sources. ardous waste sites and effluents. Carcinogenic or toxic products such as ethers present in gasoline, polycyclic Species Sources aromatic compounds, and other constituents of crude B. ambifaria (B. cepacia genomo- Soil, humans oils and coal cause serious concerns whenever acciden- var VII) tal spillage, improper disposal, transportation, or im- B. anthina (B. cepacia genomovar Soil, rhizosphere, humans, VIII) animals proper commercial usage occurs. Herbicides such as B. andropogonisa Plants 2,4-dichlorophenoxyacetic acid or 2,4,5-trichlorophe- B. caledonica Rhizosphere noxyacetic acid (the principal component of Agent B. caribensis Soil Orange) can efficiently be degraded by certain B. cepa- B. caryophylli Plants B. cepacia (genomovar I) Plants, soil, water, humans cia strains (Govan and Vandamme, 1998; Holmes et al., B. cepacia (genomovar III) Plants, soil, humans, animals 1998). B. cepacia (genomovar VI) Humans, soil Taxonomic history: Burkholderia cepacia was first de- B. fungorum Fungi, root nodules, animals, scribed as Pseudomonas cepacia by Walter Burkholder in humans B. gladiolib Plants, soil, humans 1950 as the phytopathogen responsible for bacterial rot B. glathei Soil of onions (Burkholder, 1950). In their seminal taxo- B. glumae Plants nomic study published in the 1960s, Stanier and col- B. graminis Soil, rhizosphere B. kururiensis Water leagues (Stanier et al., 1966) noted the extraordinary B. mallei Animals metabolic versatility of another novel pseudomonad, P. B. multivorans (B. cepacia ge- Plants, soil, humans multivorans. This novel species was mainly isolated from nomovar II) soil and water samples. A few years later Ballard et al. B. phenazinium Soil B. plantariic Plants (1970) reported on the synonymy between P. cepacia B. pseudomallei Soil, humans and P. multivorans. Nomenclatural priority was given to B. pyrrocinia (B. cepacia genomo- Soil, humans the former, as this was the oldest validly described spe- var IX) cies. The same year, Jonsson (1970) proposed the name B. sacchari Soil B. stabilis (B. cepacia genomovar Soil, humans Pseudomonas kingii for CDC group EO-1 (eugonic oxi- IV) dizer group 1), an opportunistic human pathogen. Sub- B. thailandensis Soil, humans sequent taxonomic analysis by Snell et al. (1972) and B. ubonensis Soil, humans Samuels et al. (1973) again revealed that the novel or- B. vietnamiensis (B. cepacia ge- Plants, soil, humans nomovar V) ganism was the same as P. cepacia. The taxonomic heterogeneity of the genus Pseudomo- a Including Pseudomonas woodsii. b Including B. cocovenenans and Pseudomonas antimicrobica. nas was revealed by the work of Palleroni et al. (1973) c Including B. vandii. and led to the gradual dissection of the genus over the following decades (Kersterts et al., 1996). In 1992, P. oli, another well-known plant pathogen (Simpson et al., cepacia and several other species of rRNA group II sensu 1994). These data, together with the striking differ- Palleroni et al. were transferred to the new genus Burk- ences in clinical outcome, transmissibility, plant patho- holderia (Yabuuchi et al., 1992). During the past 10 genic or biocontrol properties, might all have con- years, the clinical and biotechnological interest in B. cerned strain-specific differences but could also have cepacia-like organisms led to the discovery and descrip- pointed to an underlying taxonomic problem. A poly- tion of a multitude of novel species. The genus now phasic taxonomic study was initiated in 1992 and in- contains 26 species: Burkholderia andropogonis, B. ambi- cluded comparative 16S rDNA and recA sequence analy- faria,