Skip to main content

Advertisement

SpringerLink
Log in

To split or not to split: an opinion on dividing the genus Burkholderia

  • Review Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

The genus Burkholderia is a large group of species of bacteria that inhabit a wide range of environments. We previously recommended, based on multilocus sequence analysis, that the genus be separated into two distinct groups—one that consists predominantly of human, plant, and animal pathogens, including several opportunistic pathogens, and a second, much larger group of species comprising plant-associated beneficial and environmental species that are primarily known not to be pathogenic. This second group of species is found mainly in soils, frequently in association with plants as plant growth-promoting bacteria. They also possess genetic traits that bestow them with an added potential for agriculture and soil restoration, such as nitrogen fixation, phosphate solubilization, iron sequestration, and xenobiotic degradation, and they are not pathogenic. In this review, we present an update of current information on this second group of Burkholderia species, with the goal of focusing attention on their use in agriculture and environmental remediation. We describe their distribution in the environment, their taxonomy and genetic features, and their relationship with plants as either associative nitrogen-fixers or legume-nodulating/nitrogen-fixing bacteria. We also propose that a concerted and coordinated effort be made by researchers on Burkholderia to determine if a definitive taxonomic split of this very large genus is justified, especially now as we describe here for the first time intermediate groups based upon their 16S rRNA sequences. We need to learn more about the plant-associated Burkholderia strains regarding their potential for pathogenicity, especially in those strains intermediate between the two groups, and to discover whether gene exchange occurs between the symbiotic and pathogenic Burkholderia species. The latter studies will require both field and laboratory analyses of gene loss and gain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ackermann M (2015) A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol 13:497–508

    Article  CAS  PubMed  Google Scholar 

  • Anandham R, Gandhi PI, Kwon SW, Sa TM, Kim YK, Jee HJ (2009) Mixotrophic metabolism in Burkholderia kururiensis subsp. thiooxydans subsp. nov., a facultative chemolithoautotrophic thiosulfate oxidizing bacterium isolated from rhizosphere soil and proposal for classification of the type strain of Burkholderia kururiensis as Burkholderia kururiensis subsp. kururiensis subsp. nov. Arch Microbiol 191:885–894

    Article  CAS  PubMed  Google Scholar 

  • Angus AA, Lee AS, Lum MR, Shehayeb M, Hessabi R, Fujishige NA, Yerrapragada S, Kano S, Song N, Yang P, Estrada-de los Santos P, de Faria SM, Dakora FD, Weinstock G, Hirsch AM (2013) Nodulation and effective nitrogen fixation of Macroptilium atropurpureum (siratro) by Burkholderia tuberum, a beta-proteobacterium, are influenced by environmental factors. Plant Soil 362:543–562

    Article  Google Scholar 

  • Angus AA, Agapakis CM, Fong S, Yerrapragada S, Estrada-de los Santos P, Yang P, Song N, Kano S, Caballero-Mellado J, de Faria SM, Dakora FD, Weinstock G, Hirsch AM (2014) Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. PLoS ONE 9:e83779

    Article  PubMed  PubMed Central  Google Scholar 

  • Beukes CW, Venter SN, Law IJ, Phalane FL, Steenkamp ET (2013) South African papilionoid legumes are nodulated by diverse Burkholderia with unique nodulation and nitrogen-fixation loci. PLoS ONE 8:e68406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blaha D, Pringent-Combaret C, Mirza MS, Moënne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminse-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470

    Article  CAS  PubMed  Google Scholar 

  • Bontemps C, Elliott GN, Simon MF, Dos Reis Junior FB, Gross E, Lawton R, Neto NE, Loureiro MF, de Faria SM, Sprent JI, James EK, Young JPW (2010) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19:44–52

    Article  CAS  PubMed  Google Scholar 

  • Bontemps C, Rogel MA, Wiechmann A, Mussebekova A, Moody S, Simon MF, Moulin L, Elliott GN, Lacercat-Didier L, Dasilva C, Grether R, Camargo-Ricalde SL, Chen W, Sprent JI, Martinez-Romero E, Young JPW, James EK (2016) Endemic Mimosa species from Mexico prefer alphaprotebacterial rhizobial symbionts. New Phytol 209(1):319–333. doi:10.1111/nph.13573

  • Bournaud C, de Faria SM, Ferreira dos Santos JM, Tisseyre P, Silva M, Chaintreuil C, Gross E, James EK, Prin Y, Moulin L (2013) Burkholderia species are the most common and preferred nodulating symbionts of the Piptadenia group (Tribe Mimoseae). PLoS ONE 8:e63478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown NF, Beacham IR (2000) Cloning and analysis of genomic differences unique to Burkholderia pseudomallei by comparison with Burkholderia thailandensis. J Med Microbiol 49:993–1001

    Article  CAS  PubMed  Google Scholar 

  • Caballero-Mellado J, Martínez-Aguilar L, Paredes-Valdez G, Estrada-de los Santos P (2004) Burkholderia unamae sp. nov., an N2-fixing rhizospheric and endophytic species. Int J Syst Evol Microbiol 54:1165–1172

    Article  CAS  PubMed  Google Scholar 

  • Caballero-Mellado J, Onofre-Lemus J, Estrada-de los Santos P, Martínez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro-González R, Martínez-Aguilar L, Ramírez-Trujillo A, Estrada-de los Santos P, Caballero-Mellado J (2011) High diversity of culturable Burkholderia speices associated with sugarcane. Plant Soil 345:155–169

    Article  Google Scholar 

  • Chen W-M, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by β-Proteobacteria is widespread in nature. J Bacteriol 185:7266–7272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WM, de Faria SM, Straliotto R, Pitard RM, Simoes-Araujo JL, Chou JH, Barrios E, Prescott AR, Elliott GN, Sprent JI, Young JPW, James EK (2005a) Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Appl Environ Microbiol 71:7461–7471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WM, James EU, Chou JH, Sheu SY, Yang SZ, Sprent JI (2005b) β-Rhizobia from Mimosa pigra, a newly discovered invasive palnt in Taiwan. New Phytol 168:661–675

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Schröder I, French CT, Jaroszewicz A, Yee XJ, Teh BE, Toesca IJ, Miller JF, Gan YH (2014) Characterization and analysis of the Burkholderia pseudomallei BsaN virulence regulon. BMC Microbiol 14:206

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng AC, Currie BJ (2005) Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18:383–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiarini L, Bevivino A, Dalmastri C, Tabacchioni S, Visca P (2006) Burkholderia cepacia complex species: health hazards and biotechnological potential. Trends Microbiol 14:277–286

    Article  CAS  PubMed  Google Scholar 

  • Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729

    Article  CAS  PubMed  Google Scholar 

  • Coenye T, Vandamme P (2007) Burkholderia: molecular microbiology and genomics. Horizon Scientific Press, Norfolk

  • Coenye T, Laevens S, Gillis M, Vandamme P (2001) Genotypic and chemotaxonomic evidence for the reclassification of Pseudomonas woodsii (Smith 1911) Stevens 1925 as Burkholderia andropogonis (Smith 1911) Gillis et al. 1995. Int J Syst Evol Microbiol 51:183–185

    Article  CAS  PubMed  Google Scholar 

  • Coenye T, Henry D, Speert DP, Vandamme P (2004) Burkholderia phenoliruptrix sp. nov., to accommodate the 2, 4, 5-trichlorophenoxyacetic acid and halophenol-degrading strain AC1100. Syst Appl Microbiol 27:623–627

    Article  CAS  PubMed  Google Scholar 

  • Cunha CO, Zuleta LFG, De Almeida LGP, Ciapina LP, Borges WL, Pitard RM, Baldani JI, Straliotto R, De Faria SM, Hungria M, Cavada BS, Mercante FM, De Vasconcelos ATR (2012) Complete genome sequence of Burkholderia phenoliruptrix BR3459a (CLA1), a heat-tolerant, nitrogen-fixing symbiont of Mimosa flucculosa. J Bacteriol 194:6675–6676

    Article  CAS  Google Scholar 

  • Dalmastri C, Chiarini L, Cantale C, Bevivino A, Tabacchioni S (1999) Soil type and maize cultivar affect the genetic diversity of maize root–associated Burkholderia cepacia populations. Microb Ecol 38:273–284

    Article  PubMed  Google Scholar 

  • De Los Cobos-Vasconcelos D, Santoyo-Tepole F, Juarez-Ramirez C, Ruiz-Ordaz N, Galindez-Mayer C (2006) Cometabolic degradation of chlorophenols by a strain of Burkholderia in fed-batch culture. Enzymol Microb Technol 40:57–60

    Article  CAS  Google Scholar 

  • de Oliveira-Langatti SM, Marra LM, Soares BL, Bomfeti CA, da Silva K, Ferreira PAA, de Souza Moreira FM (2014) Bacteria isolated from soils of the western Amazon and from rehavilitated bauxite-mining areas have potential as plant growth promoters. World J Microbiol Biotechnol 30:1239–1250

    Article  Google Scholar 

  • Elliott GN, Chen W-M, Bontemps C, Chou J-H, Young JPW, Sprent JI, James EK (2007a) Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Ann Bot 100:1403–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elliott GN, Chen WM, Chou JH, Wang HC, Sheu SY, Perin L, Reis VM, Moulin L, Simon MF, Bontemps C, Sutherland JM, Bessi R, de Faria SM, Trinick MJ, Prescott AR, Sprent JI, James EK (2007b) Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol 173:168–180

    Article  CAS  PubMed  Google Scholar 

  • Estrada-de los Santos P, Bustillos-Cristales RO, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67:2790–2798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estrada-de los Santos P, Vinuesa P, Martínez-Aguilar L, Hirsch AM, Caballero-Mellado J (2013) Phylogenetic analysis of Burkholderia species by multilocus sequence analysis. Curr Microbiol 67:51–60

    Article  CAS  PubMed  Google Scholar 

  • Ferreira PAA, Bomfeti CA, Soares BL, de Souza Moreira FM (2012) Efficient nitrogen-fixing Rhizobium strains isolated from Amazonian soils are highly tolerant to acidity and aluminium. World J Microbiol Biotechnol 28:1947–1959

    Article  Google Scholar 

  • Gangadhara K, Kunhi A (2000) Protection of tomato seed germination from the inhibitory effect of 2,4,5-trichlorophenoxyacetic acid by inoculation of soil with Burkholderia cepacia AC1100. J Agric Food Chem 48:4314–4319

    Article  CAS  PubMed  Google Scholar 

  • Gehlot HS, Tak N, Kaushik M, Mitra S, Chen WM, Poseleit N, Panwar D, Poonar N, Parihar R, Tak A, Sankhla IS, Ojha A, Rao SR, Simon MF, dos Reis Junior FB, Perigolo N, Tripathi AK, Sprent JI, Yound JPW, Gyaneshwar P (2013) An invasive Mimosa in India does not adopt the symbionts of its native relatives. Ann Bot 112:1–18

    Article  Google Scholar 

  • Gillis M, Tran VV, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fenandez MP (1995) Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Bacteriol 45:274–289

    Article  CAS  Google Scholar 

  • Glagoleva O, Kovalskaya N, Umarov M (1996) Endosymbiosis formation between nitrogen-fixing bacteria Pseudomonas caryophylli and rape root cells. Edocyt Cell Res 11:147–158

    Google Scholar 

  • Gómez-De Jesús A, Romano-Baez F, Leyva-Amezcua L, Juárez-Ramírez C, Ruiz-Ordaz N, Galíndez-Mayer J (2009) Biodegradation of 2,4,6-trichlorophenol in a packed-bed biofilm reactor equipped with an internal net draft tube riser for aeration and liquid circulation. J Hazard Mater 161:1140–1149

    Article  PubMed  Google Scholar 

  • Gonzalez CF, Venturi V, Engledow AS (2007) The phytopathogenic Burkholderia. In: Coenye T, Mahenthiralingam E (eds) Molecular microbiology and genomics. Caister Academic Press, Norfolk, pp 153–176

    Google Scholar 

  • Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, Estrada-de los Santos P, Gross E, dos Reis FB, Sprent JI, Young JPW, James EK (2011) Legume-nodulating betaproeteobacteria: diversity, host range, and future prospects. Mol Plant Microb Int 24:1276–1288

    Article  CAS  Google Scholar 

  • Haahtela K, Helander I, Nurmiaho-Lassila EL, Sundman V (1983) Morphological and physiological characteristics and lipopolysaccharide composition of N2-fixing (C2H2-reducing) root-associated Pseudomonas sp. Can J Microbiol 29:874–880

    Article  CAS  PubMed  Google Scholar 

  • Howieson JG, De Meyer SE, Vivas-Marfisi A, Ratnayake S, Ardley JK, Yates RJ (2013) Novel Burkholderia bacteria isolated from Lebeckia ambigua—a perennial suffrutescent legume of the fynbos. Soil Biol Biochem 60:55–64

    Article  CAS  Google Scholar 

  • Hussain S, Arshad M, Saleem M, Khalid A (2007) Biodegradation of α-and β-endosulfan by soil bacteria. Biodegradation 18:731–740

    Article  CAS  PubMed  Google Scholar 

  • Jaeger K, Dijkstra B, Reetz M (1999) Bacterial biocatalysts: molecular biology, three-dimensional structures, and biotechnological applications of lipases. Annu Rev Microbiol 53:315–351

    Article  CAS  PubMed  Google Scholar 

  • Karns J, Kilbane J, Duttagupta S, Chakrabarty A (1983) Metabolism of halophenols by 2,4,5-trichlorophenoxyacetic acid-degrading Pseudomonas cepacia. Appl Environ Microbiol 46:1176–1181

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kellogg S, Chatterjee DK, Chakrabarty AM (1981) Plasmid-assisted molecular breeding: new technique for enhanced biodegradation of persistent toxic chemicals. Science 214:1133–1135

    Article  CAS  PubMed  Google Scholar 

  • Kilbane J, Chatterjee D, Chakrabarty A (1983) Detoxification of 2,4,5-trichlorophenoxyacetic acid from contaminated soil by Pseudomonas cepacia. Appl Environ Microbiol 45:1697–1700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laurie AD, Lloyd-Jones G (1999) The phn Genes of Burkholderia sp. strain RP007 constitute a divergent gene cluster for polycyclic aromatic hydrocarbon catabolism. J Bacteriol 181:531–540

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lemaire B, Dlodlo O, Chimphango S, Stirton C, Schrire B, Boatwright JS, Honnay O, Smets E, Sprent J, James EK, Muasya AM (2015) Symbiotic diversity, specificity and distribution of rhizobia in native legumes of the Core Cape Subregion (South Africa). FEMS Microbiol Ecol 9:1–17

    Article  Google Scholar 

  • Lessie TG, Hendrickson W, Manning BD, Devereux R (1996) Genomic complexity and plasticity of Burkholderia cepacia. FEMS Microbiol Lett 144:117–128

    Article  CAS  PubMed  Google Scholar 

  • Li G-X, Wu X-Q, Ye J-R (2013) Biosafety and colonization of Burkholderia multivorans WS-FJ9 and its growth-promoting effects on poplars. Appl Microbiol Biotechnol 97:10489–10498

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Meggo R, Hu D, Schnoor JL, Mattes TE (2014) Enhanced polychlorinated biphenyl removal in a switchgrass rhizosphere by bioaugmentation with Burkholderia xenovorans LB400. Ecol Eng 71:215–222

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu WYY, Ridgway HJ, James TK, James EK, Chen WM, Sprent JI, Young JPW, Andrews M (2014) Burkholderia sp. induces functional nodules on the South African invasive legume Dipogon lignosus (Phaseoleae) in New Zealand soils. Microb Ecol 68:542–555

    Article  CAS  PubMed  Google Scholar 

  • Liu XY, Wei S, Wang F, James EK, Guo XY, Zagar C, Xia LG, Dong X, Wang YP (2012) Burkholderia and Cupriavidus spp. are the preferred symbionts of Mimosa spp. in Southern China. FEMS Microb Ecol 80:417–426

    Article  CAS  Google Scholar 

  • Mahenthiralingam E, Baldwin A, Dowson CG (2008) Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104:1539–1551

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Aguilar L, Díaz R, Peña-Cabriales JJ, Estrada-de los Santos P, Dunn MF, Caballero-Mellado J (2008) Multichromosomal genome structure and confirmation of diazotrophy in novel plant-associated Burkholderia species. Appl Environ Microbiol 74:4574–4579

    Article  PubMed  PubMed Central  Google Scholar 

  • Martínez-Aguilar L, Salazar-Salazar C, Díaz-Mendez R, Caballero-Mellado J, Hirsch AM, Vasquez-Murrieta MS, Estrada-de los Santos P (2013) Burkholderia caballeronis sp. nov., a nitrogen fixing species isolated from tomato (Lycopersicon esculentum) with the ability to effectively nodulate Phaseolus vulgaris. Antonie van Leeuwenhoek 104:1063–1071

    Article  PubMed  Google Scholar 

  • Miché L, Faure D, Blot M, Cabanne-Giuli E, Balandreau J (2001) Detection and activity of insertion sequences in environmental strains of Burkholderia. Environ Microbiol 3:766–773

    Article  PubMed  Google Scholar 

  • Mishra RP, Tisseyre P, Melkonian R, Chaintreuil C, Miche L, Klonowska A, Gonzalez S, Bena G, Laguerre G, Moulin L (2012) Genetic diversity of Mimosa pudica rhizobial symbionts in soils of French Guiana: investigating the origin and diversity of Burkholderia phymatum and other beta-rhizobia. FEMS Microbiol Ecol 79:487–503

    Article  CAS  PubMed  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the β-subclass of Proteobacteria. Nature 411:948–950

    Article  CAS  PubMed  Google Scholar 

  • Mueller J, Devereux R, Santavy D, Lantz S, Willis S, Pritchard P (1997) Phylogenetic and physiological comparisons of PAH-degrading bacteria from geographically diverse soils. Antonie van Leeuwenhoek 71:329–343

    Article  CAS  PubMed  Google Scholar 

  • Naveed M, Qureshi M, Zahir ZA, Hassan MB, Sessitch A, Mitter B (2014) L-Tryptophan-dependent biosynthesis of indole-3-acetic acid (IAA) improves plant growth and colonization of maize by Burkholderia phytofirmans PsJN. Ann Microbiol 65:1381–1389

    Article  Google Scholar 

  • Nierman WC, DeShazer D, Kim HS, Tettelin H, Nelson KE, Feldblyum T, Ulrich RL, Ronning CM, Brinkac LM, Daugherty SC (2004) Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad Sci USA 101:14246–14251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Pantoja D, Donoso R, Agulló L, Córdova M, Seeger M, Pieper DH, González B (2012) Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderiales. Environ Microbiol 14:1091–1117

    Article  PubMed  Google Scholar 

  • Perin L, Martinez-Aguilar L, Paredes-Valdez G, Baldani J, Estrada-de Los Santos P, Reis V, Caballero-Mellado J (2006) Burkholderia silvatlantica sp. nov., a diazotrophic bacterium associated with sugar cane and maize. Int J Syst Evol Microbiol 56:1931–1937

    Article  CAS  PubMed  Google Scholar 

  • Postgate JR (1982) The fundamentals of nitrogen fixation. Phil Trans R Soc Lond B 296(1082) 375–385

  • Reis V, Estrada-de los Santos P, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Manvingui P, Baldani VLD, Schmid M, Baldani JI, Balandreau J, Harmann A, Caballero-Mellado J (2004) Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int J Syst Evol Microbiol 54:2155–2162

    Article  CAS  PubMed  Google Scholar 

  • Roselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67

    Article  Google Scholar 

  • Sawana A, Adeolu M, Gupta RS (2014) Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Gen 5:429. doi:10.3389/fgene.2014.00429

  • Seeger M, Zielinski M, Timmis KN, Hofer B (1999) Regiospecificity of dioxygenation of di-to pentachlorobiphenyls and their degradation to chlorobenzoates by the bph-encoded catabolic pathway of Burkholderia sp. strain LB400. Appl Environ Microbiol 65:3614–3621

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sessitsch A, Coenye T, Sturz A, Vandamme P, Barka EA, Salles J, Van Elsas J, Faure D, Reiter B, Glick B (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192

    Article  CAS  PubMed  Google Scholar 

  • Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, James EK, Sprent JI, Young JPW, Chen WM (2012) Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil. Int J Syst Evol Microbiol 62:2272–2278

  • Sheu SY, Chen MH, Liu WYY, Andrews M, James EK, Ardley JK, De Meyer SE, James TK, Howieson JG, Coutinho BG, Chen WM (2015) Burkholderia dipogonis sp. nov., isolated from root nodules of Dipogon lignosus in New Zealand and Western Australia. Int J Syst Evol Microbiol. doi:10.1099/ijsem.0.000639

    Google Scholar 

  • Singh RK, Nalik N, Singh S (2013) Improved nutrient use efficiency increases plant grwoth with the use of IAA-overproducing strains of endophytic Burkholderia cepacia strain RR25. Microb Ecol 66:375–384

    Article  CAS  PubMed  Google Scholar 

  • Somtrakoon K, Suanjit S, Pokethitiyook P, Kruatrachue M, Lee H, Upatham S (2008a) Enhanced biodegradation of anthracene in acidic soil by inoculated Burkholderia sp. VUN10013. Curr Microbiol 57:102–106

    Article  CAS  PubMed  Google Scholar 

  • Somtrakoon K, Suanjit S, Pokethitiyook P, Kruatrachue M, Lee H, Upatham S (2008b) Phenanthrene stimulates the degradation of pyrene and fluoranthene by Burkholderia sp. VUN10013. World J Microbiol Biotechnol 24:523–531

    Article  CAS  Google Scholar 

  • Sprague L, Neubauer H (2004) Melioidosis in animals: a review on epizootiology, diagnosis and clinical presentation. J Vet Med 51:305–320

    Article  CAS  Google Scholar 

  • Srinivasan S, Kim J, Kang S-R, Jheong W-H, Lee S-S (2013) Burkholderia humi sp. nov., isolated from peat soil. Curr Microbiol 66:300–305

    Article  CAS  PubMed  Google Scholar 

  • Steenkamp ET, van Zyl E, Beukes CW, Avontuur JR, Chan WY, Palmer M, Mthombeni LS, Phalane FL, Sereme TK, Venter SN (2015) Burkholderia kirstenboschensis sp. nov. nodulated papilionoid legumes indigenous to South Africa. Syst Appl Microbiol 38(8):545–554

    Article  CAS  PubMed  Google Scholar 

  • Suarez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonca-Previato L, James EK, Venturi V (2012) Common features of environmental and ppotentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266

    Article  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tindall BJ, Rossello-Mora R, Busse HJ, Ludwig W, Kampfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266

    Article  CAS  PubMed  Google Scholar 

  • Urakami T, Ito-Yoshida C, Araki H, Kijima T, Suzuki K-I, Komagata K (1994) Transfer of Pseudomonas plantarii and Pseudomonas glumae to Burkholderia as Burkholderia spp. and description of Burkholderia vandii sp. nov. Int J Syst Evol Microbiol 44:235–245

    CAS  Google Scholar 

  • Van VT, Berge O, Ke SN, Balandreau J, Heulin T (2000) Repeated beneficial effects of rice inoculation with a strain of Burkholderia vietnamiensis on early and late yield components in low fertility sulphate acid soils of Vietnam. Plant Soil 218:273–284

    Article  CAS  Google Scholar 

  • Vandamme P, Dawyndt P (2011) Classification and identification of the Burkholderia cepacia complex: past, presen and future. Syst Appl Microbiol 34:87–95

    Article  CAS  PubMed  Google Scholar 

  • Vandamme P, Peeters C (2014) Time to revisit polyphasic taxonomy. Antonie van Leeuwenhoek 106:57–65

    Article  PubMed  Google Scholar 

  • Vandamme P, Goris J, Chen W-M, De Vos P, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 25:507–512

    Article  PubMed  Google Scholar 

  • Vandamme P, De Brandt E, Houf K, Salles JF, van Elsas JD, Spilker T, LiPuma JJ (2013) Burkholderia humi sp. nov., Burkholderia choica sp. nov., Burkholderia telluris sp. nov., Burkholderia terrestris sp. nov. and Burkholderia udeis sp. nov.: Burkholderia glathei-like bacteria from soil and rhizosphere soil. Int J Syst Evol Microbiol 63:4707–4718

    Article  CAS  PubMed  Google Scholar 

  • Vanlaere E, van der Meer JR, Falsen E, Salles JF, De Brandt E, Vandamme P (2008) Burkholderia sartisoli sp. nov., isolated from a polycyclic aromatic hydrocarbon-contaminated soil. Int J Syst Evol Microbiol 58:420–423

    Article  CAS  PubMed  Google Scholar 

  • Viallard V, Poirier I, Cournoyer B, Haurat J, Wiebkin S, Ophel-Keller K, Balandreau J (1998) Burkholderia graminis sp. nov., a rhizospheric Burkholderia species, and reassessment of [Pseudomonas] phenazinium,[Pseudomonas] pyrrocinia and [Pseudomonas] glathei as Burkholderia. Int J Syst Bacteriol 48:549–563

    Article  CAS  PubMed  Google Scholar 

  • Vinuesa P, Leon-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Perez-Galdona R, Werner D, Martinz-Romero E (2005) Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 55:569–575

    Article  CAS  PubMed  Google Scholar 

  • Vu H, Mu A, Moreau J (2013) Biodegradation of thiocyanate by a novel strain of Burkholderia phytofirmans from soil contaminated by gold mine tailings. Lett Appl Microbiol 57:368–372

    CAS  PubMed  Google Scholar 

  • Wang L, Zhang L, Liu Z, Zhao D, Liu X et al (2013) A minimal nitrogen fixation gene cluster from Paenibacillus sp. WLY78 enables expression of active nitrogenase in Escherichia coli. PLoS Genet 9:e1003865. doi:10.1371/journal.pgen.1003865

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu L, Ge C, Cui Z, Li J, Fan H (1995) Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 45:706–711

    Article  CAS  PubMed  Google Scholar 

  • Yabuuchi E, Kosako Y, Oyaizu H, Yano I, Hotta H, Hashimoto Y, Ezaki T, Arakawa M (1992) Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol 36:1251–1275

    Article  CAS  PubMed  Google Scholar 

  • Yao ZY, Kan FL, Wang ET, Wei GH, Chen WX (2002) Characterization of rhizobia that nodulate legume species of the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov. Int J Syst Evol Microbiol 52:2219–2230

    CAS  PubMed  Google Scholar 

  • Yarza P, YilmazP PE, Glockner FO, Ludwig W, Schleifer KH, Whitman WB, Euzeby J, Amann R, Rosello-Mora R (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Hanada S, Shigematsu T, Shibuya K, Kamagata Y, Kanagawa T, Kurane R (2000) Burkholderia kururiensis sp. nov., a trichloroethylene (TCE)-degrading bacterium isolated from an aquifer polluted with TCE. Int J Syst Evol Microbiol 50:743–749

    Article  CAS  PubMed  Google Scholar 

  • Zuleta LF, de Cunha C, De Carvalho FM, Ciapina LP, Souza RC, Mercante FM, De Faria SM, Baldani JI, Straliotto R, Hungria M (2014) The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes. BMC Genomics 15:535

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported in part by Multidisciplinary project SIP20141652 with modules SIP20140353 and SIP20150358. Project IOB-0537497 from the National Science Foundation (USA) to George Weinstock and AMH and a grant from the Shanbrom Family Foundation to AMH also funded this research. FURR and EYTG were supported by CONACYT.

We thank Drs. Stefan J. Kirchanski, Martha E. Trujillo, Euan K. James, and J.A. Ibarra for their helpful comments.

Author information

Authors and Affiliations

  1. Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas, Prolongación Carpio y Plan de Ayala s/n., Col. Santo Tomás, Delegación Cuauhtémoc, México, D.F., Mexico

    Paulina Estrada-de los Santos, Fernando Uriel Rojas-Rojas, Erika Yanet Tapia-García & María Soledad Vásquez-Murrieta

  2. Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, 621 Charles E. Young Drive South, Los Angeles, CA, 90095-1606, USA

    Ann M. Hirsch

  3. Molecular Biology Institute, University of California, Los Angeles, 621 Charles E. Young Drive South, Los Angeles, CA, 90095-1606, USA

    Ann M. Hirsch

Authors
  1. Paulina Estrada-de los Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fernando Uriel Rojas-Rojas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erika Yanet Tapia-García
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. María Soledad Vásquez-Murrieta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ann M. Hirsch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paulina Estrada-de los Santos.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

(DOCX 82 kb)

Supplementary Table 2

(DOCX 21 kb)

Supplementary Table 3

(DOCX 25 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Estrada-de los Santos, P., Rojas-Rojas, F.U., Tapia-García, E.Y. et al. To split or not to split: an opinion on dividing the genus Burkholderia . Ann Microbiol 66, 1303–1314 (2016). https://doi.org/10.1007/s13213-015-1183-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-015-1183-1

Keywords

Search

Navigation