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PLOS ONE  2014 

Plant-Associated Symbiotic Burkholderia Species Lack Hallmark Strategies Required in Mammalian Pathogenesis

DOI: 10.1371/journal.pone.0083779

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Abstract:

Burkholderia is a diverse and dynamic genus, containing pathogenic species as well as species that form complex interactions with plants. Pathogenic strains, such as B. pseudomallei and B. mallei, can cause serious disease in mammals, while other Burkholderia strains are opportunistic pathogens, infecting humans or animals with a compromised immune system. Although some of the opportunistic Burkholderia pathogens are known to promote plant growth and even fix nitrogen, the risk of infection to infants, the elderly, and people who are immunocompromised has not only resulted in a restriction on their use, but has also limited the application of non-pathogenic, symbiotic species, several of which nodulate legume roots or have positive effects on plant growth. However, recent phylogenetic analyses have demonstrated that Burkholderia species separate into distinct lineages, suggesting the possibility for safe use of certain symbiotic species in agricultural contexts. A number of environmental strains that promote plant growth or degrade xenobiotics are also included in the symbiotic lineage. Many of these species have the potential to enhance agriculture in areas where fertilizers are not readily available and may serve in the future as inocula for crops growing in soils impacted by climate change. Here we address the pathogenic potential of several of the symbiotic Burkholderia strains using bioinformatics and functional tests. A series of infection experiments using Caenorhabditis elegans and HeLa cells, as well as genomic characterization of pathogenic loci, show that the risk of opportunistic infection by symbiotic strains such as B. tuberum is extremely low.

References

[1]  Berg G, Eberl L, Hartmann A (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7: 1673–1685.
[2]  Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendo?a-Previato L, James EK, et al. (2012) Common features of environmentally and potentially beneficial plant-associated Burkholderia. Microb Ecol 63: 249–266.
[3]  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.
[4]  Yabuuchi E, Kosako Y, Oyaizu H, Yano I, Hotta H, et al. (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.
[5]  Yabuuchi E, Kosako Y, Yano I, Hotta H, Nishiuchi Y (1995) Transfer of two Burkholderia and an Alcaligenes species to Ralstonia gen. Nov.: Proposal of Ralstonia pickettii (Ralston, Palleroni and Doudoroff 1973) comb. Nov., Ralstonia solanacearum (Smith 1896) comb. Nov. and Ralstonia eutropha (Davis 1969) comb. Nov. Microbiol Immunol 39: 897–904.
[6]  Onofre-Lemus J, Hernández-Lucas I, Girard L, Caballero-Mellado J (2009) ACC (1-aminocyclopropane-1-carboxylate) deaminase activity, a widespread trait in Burkholderia species, and its growth-promoting effect on tomato plants. Appl Environ Microbiol 75: 6581–6590.
[7]  Payne GW, Vandamme P, Morgan SH, LiPuma JJ, Coenye T, et al. (2005) Development of a recA gene-based identification approach for the entire Burkholderia genus. Appl Environ Microbiol 71: 3917–3927.
[8]  Perin L, Martinez-Aguilar L, Castro-Gonzalez R, Estrada-de Los Santos P, Cabellos-Avelar T, et al. (2006) Diazotrophic Burkholderia species associated with field-grown maize and sugarcane. Appl Environ Microbiol 72: 3103–3110.
[9]  Baldwin A, Sokol PA, Parkhill J, Mahenthiralingam E (2004) The Burkholderia cepacia epidemic strain marker is part of a novel genomic island encoding both virulence and metabolism-associated genes in Burkholderia cenocepacia. Infect Immun 72: 1537–1547.
[10]  Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, et al. (2011) Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant Microbe Interact 24: 1276–1288.
[11]  O'sullivan LA, Weightman AJ, Jones TH, Marchbank AM, Tiedje JM, et al. (2007) Identifying the genetic basis of ecologically and biotechnologically useful functions of the bacterium Burkholderia vietnamiensis. Environ Microbiol 9: 1017–1034.
[12]  de Los Santos-Villalobos S, Barrera-Galicia GC, Miranda-Salcedo MA, Pe?a-Cabriales JJ (2012) Burkholderia cepacia XXVI siderophore with biocontrol capacity against Colletotrichum gloeosporioides. World J Microbiol Biotechnol 28: 2615–2623.
[13]  Holmes A, Govan J, Goldstein R (1998) Agricultural use of Burkholderia (Pseudomonas) cepacia: a threat to human health? Emerg Infect Diseases 4: 221–227.
[14]  Torbeck L, Raccasi D, Guilfoyle DE, Friedman RL, Hussong D (2011) Burkholderia cepacia: this decision is overdue. PDA J Pharm Sci Technol 65: 535–543.
[15]  Magalh?es M, de Britto MCA, Vandamme P (2002) Burkholderia cepacia genomovar III and Burkholderia vietnamiensis double infection in a cystic fibrosis child. J Cyst Fibros 1: 292–294.
[16]  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.
[17]  U.S. Environmental Protection Agency (2003) Burkholderia cepacia Complex; Significant New Use Rule. Federal Register 68: 35315–35320 Available: http://www.epa.gov/fedrgstr/EPA-TOX/2003?/June/Day-13/t15010.htm.
[18]  Sanchez PA (2010) Tripling crop yields in tropical africa. Nature Geosci 3: 299–300.
[19]  Galyov EE, Brett PJ, DeShazer D (2010) Molecular insights into Burkholderia pseudomallei and Burkholderia mallei pathogenesis. Annu Rev Microbiol 64: 495–517.
[20]  Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
[21]  Haraga A, West TE, Brittnacher MJ, Skerrett SJ, Miller SI (2008) Burkholderia thailandensis as a model system for the study of the virulence-associated Type III secretion system of Burkholderia pseudomallei. Infect Immun 76: 5402–5411.
[22]  Reinke SN, Hu X, Sykes BD, Lemire BD (2010) Caenorhabditis elegans diet significantly affects metabolic profile, mitochondrial DNA levels, lifespan and brood size. Mol Gen Metab 100: 274–282.
[23]  Kaplan D, Maymon M, Agapakis CM, Lee A, Wang A, et al.. (2013) A survey of the microbial community in the rhizosphere of two dominant shrubs of the Negev Desert highlands, Zygophyllum dumosum (Zygophyllaceae) and Atriplex halimus (Amaranthaceae) using cultivation-dependent and -independent methods. Amer J Bot, doi:10.3732/ajb.1200615.
[24]  Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45: 493–496.
[25]  Stiernagle T (2006) Maintenance of C. elegans. WormBook: 1–11.
[26]  Wiersinga WJ, van der Poll T, White NJ, Day NP, Peacock SJ (2006) Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Micro 4: 272–282.
[27]  Reckseidler-Zenteno SL, DeVinney R, Woods DE (2005) The capsular polysaccharide of Burkholderia pseudomallei contributes to survival in serum by reducing complement factor C3b deposition. Infect Immun 73: 1106–1115.
[28]  Essex-Lopresti AE, Boddey JA, Thomas R, Smith MP, Hartley MG, et al. (2005) A type IV pilin, PilA, contributes to adherence of Burkholderia pseudomallei and virulence in vivo. Infect Immun 73: 1260–1264.
[29]  Holden MTG, Titball RW, Peacock SJ, Cerde?o-Tárraga AM, Atkins T, et al. (2004) Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci USA 101: 14240–14245.
[30]  DeShazer D, Brett PJ, Carlyon R, Woods DE (1997) Mutagenesis of Burkholderia pseudomallei with Tn5-OT182: isolation of motility mutants and molecular characterization of the flagellin structural gene. J Bacteriol 179: 2116–2125.
[31]  Chua KL, Chan YY, Gan YH (2003) Flagella are virulence determinants of Burkholderia pseudomallei. Infect Immun 71: 1622–1629.
[32]  French CT, Toesca IJ, Wu T-H, Teslaa T, Beaty SM, et al. (2011) Dissection of the Burkholderia intracellular life cycle using a photothermal nanoblade. Proc Natl Acad Sci USA 108: 12095–12100.
[33]  Urban TA, Griffith A, Torok AM, Smolkin ME, Burns JL, et al. (2004) Contribution of Burkholderia cenocepacia flagella to infectivity and inflammation. Infect Immun 72: 5126–5134.
[34]  Whitlock GC, Mark Estes D, Torres AG (2007) Glanders: off to the races with Burkholderia mallei. FEMS Microbiol Lett 277: 115–122.
[35]  de Oliveira Cunha C, Goda Zuleta LF, Paula de Almeida LG, Prioli Ciapina L, Lustrino Borges W, et al. (2012) Complete genome sequence of Burkholderia phenoliruptrix BR3459a (CLA1), a heat-tolerant, nitrogen-fixing symbiont of Mimosa flocculosa. J Bacteriol 194: 6675–6676.
[36]  Mitter B, Petric A, Shin MW, Chain PS, Hauberg-Lotte L, et al. (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants, Front Plant Sci. 4: 1–15 doi:10.3389/fpls.2013.00120/abstract.
[37]  Chain PS, Denef VJ, Konstantinidis KT, Vergez LM, Agulló L, et al. (2006) Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci USA 108: 15280–15287..
[38]  Schmidt MA, Balsanelli E, Faoro H, Cruz LM, Wassem R, et al.. (2012) The type III secretion system is necessary for the development of a pathogenic and endophytic interaction between Herbaspirillum rubrisubalbicans and Poaceae. BMC Microbiol 12: doi:10.1186/1471-2180-12-98.
[39]  Backert S, Meyer TF (2006) Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 9: 207–217.
[40]  Cascales E, Christie PJ (2003) The versatile bacterial type IV secretion systems. Nat Rev Micro 1: 137–149.
[41]  Zhang R, LiPuma JJ, Gonzalez CF (2009) Two type IV secretion systems with different functions in Burkholderia cenocepacia K56-2. Microbiology 155: 4005–4013.
[42]  Schwarz S, Hood RD, Mougous JD (2010) What is type VI secretion doing in all those bugs? Trends Microbiol 18: 531–537.
[43]  Bingle LE, Bailey CM, Pallen MJ (2008) Type VI secretion: a beginner's guide. Curr Opin Microbiol 11: 3–8.
[44]  Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I (2009) Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics 10: 104.
[45]  Schwarz S, West TE, Boyer F, Chiang W-C, Carl MA, et al. (2010) Burkholderia Type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 6: e1001068.
[46]  Riesenfeld CS, Goodman RM, Handelsman J (2004) Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ Microbiol 6: 981–989.
[47]  Tan MW, Mahajan-Miklos S, Ausubel FM (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci USA 96: 715–720.
[48]  Zachow C, Pirker H, Westendorf C, Tilcher R, Berg G (2009) The Caenorhabditis elegans assay: a tool to evaluate the pathogenic potential of bacterial biocontrol agents. Euro Plant Path 125: 367–376.
[49]  Niu Q, Huang X, Zhang L, Xu J, Yang D, et al. (2010) A Trojan horse mechanism of bacterial pathogenesis against nematodes. Proc Natl Acad Sci USA 107: 16631–16636.
[50]  Cooper VS, Carlson WA, LiPuma JJ (2009) Susceptibility of Caenorhabditis elegans to Burkholderia infection depends on prior diet and secreted bacterial attractants. PLoS ONE 4: e7961.
[51]  Gyaneshwar P, Kumar GN, Parekh L (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245: 83–93.
[52]  Ulrich RL, DeShazer D, Brueggemann EE, Hines HB, Oyston PC, et al. (2004) Role of quorum sensing in the pathogenicity of Burkholderia pseudomallei. J Med Microbiol 53: 1053–1064.
[53]  Valade E, Thibault FM, Gauthier YP, Palencia M, Popoff MY, et al. (2004) The PmlI-PmlR quorum-sensing system in Burkholderia pseudomallei plays a key role in virulence and modulates production of the MprA protease. J Bacteriol 186: 2288–2294.
[54]  Suarez-Moreno ZR, Caballero-Mellado J, Venturi V (2008) The new group of non-pathogenic plant-associated nitrogen-fixing Burkholderia spp. shares a conserved quorum-sensing system, which is tightly regulated by the RsaL repressor. Microbiology 154: 2048–2059.
[55]  Roest HP, Mulders IHM, Spaink HP, Wijffelman CA, Lugtenberg BJJ (1997) A Rhizobium leguminosarum biovar trifolii locus not localized on the sym plasmid hinders effective nodulation on plants of the pea cross-inoculation group. Mol Plant Microbe Interact 10: 938–941.
[56]  Bladergroen MR, Badelt K, Spaink HP (2003) Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant Microbe Interact 16: 53–64.
[57]  McCarter LL (2004) Dual flagellar systems enable motility under different circumstances. J Mol Microbiol Biotechnol 7: 18–29.
[58]  Angus AA, Lee A, Lum MR, Shehayeb M, Hessabi R, et al. (2013) Nodulation and effective nitrogen fixation of Macroptilium atropurpureum (siratro) by Burkholderia tuberum, a nodulating and plant growth promoting beta-proteobacterium, are influenced by environmental factors. Plant Soil 369: 543–562.
[59]  Araujo R, Rodrigues AG (2004) Variability of germinative potential among pathogenic species of Aspergillus. J Clin Microbiol 42: 4335–4337.
[60]  Coenye T, Goris J, Spilker T, Vandamme P, LiPuma JJ (2002) Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients and description of Inquilinus limosus gen. nov., sp. nov. J Clin Microbiol 40: 2062–2069.
[61]  Paphitou NI, Rolston KVI (2003) Catheter-related bacteremia caused by Agrobacterium radiobacter in a cancer patient: case report and literature review. Infection 31: 421–424.
[62]  Chen CY, Hansen KS, Hansen LK (2008) Rhizobium radiobacter as an opportunistic pathogen in central venous catheter-associated bloodstream infection: case report and review. J Hosp Infect 68: 203–207.
[63]  Kuykendall LD, Shao JY, Hartung JS (2012) Conservation of gene order and content in the circular Chromosomes of “Candidatus Liberibacter asiaticus” and other Rhizobiales. PLoS ONE 7: e34673.
[64]  La Scola B (2002) Description of Afipia birgiae sp. nov. and Afipia massiliensis sp. nov. and recognition of Afipia felis genospecies A. Int J Syst Evol Microbiol 52: 1773–1782.
[65]  Bhatt AS, Freeman SS, Herrera AF, Pedamallu CS, Gevers D, et al. (2013) Sequence-based discovery of Bradyrhizobium enterica in cord colitis syndrome. N Engl J Med 369: 517–528.
[66]  Caballero-Mellado J, Martinez-Aguilar L, Paredes-Valdez G, Estrada-de los Santos P (2004) Burkholderia unamae sp. nov., a N2-fixing rhizospheric and endophytic species. Int J Syst Evol Microbiol 54: 1165–1172.
[67]  Seo Y-S, Lim J, Choi BS, Kim H, Goo E, et al. (2011) Complete genome sequence of Burkholderia gladiolii BSR3. J Bact 193: 3149 doi: 10.1128/JB.00420-11.

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