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Microbial Cyclic Di-Nucleotide Signaling pp 519–543Cite as

Cyclic di-GMP in Burkholderia spp.

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Abstract

Burkholderia spp. survive in diverse ecological niches in association with soil, plants, and animals. In these environments, some members of the Burkholderia spp. participate in beneficial interactions that promote plant growth, nutrient cycling, and bioremediation; however, some Burkholderia spp. are also pathogens of plants, fungi, amoebae, insects, animals, and humans. In order to transition between niches and compete with other microbes, Burkholderia spp. have evolved sophisticated sensory systems to detect and respond to a variety of cues and signals from external stimuli that allow rapid response to changing environmental conditions. Cyclic di-GMP is a nearly universal bacterial second messenger and a key signaling molecule in Burkholderia spp. that regulates a variety of bacterial behaviors including virulence, motility, and biofilm formation. This chapter will review the progress toward understanding the sensory components and associated regulatory components that respond to environmental cues and correspondingly alter the intracellular levels of cyclic di-GMP. Recent reports indicate that various members of the Burkholderia spp. respond to alterations in temperature, nutrient availability, and population density (via Burkholderia diffusible signal factor) to control bacterial behaviors associated with pathogenesis, dissemination, and survival in the niches that Burkholderia spp. inhabit.

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References

  1. 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 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. Parte AC (2018) LPSN – list of prokaryotic names with standing in nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 68:1825–1829

    Article  PubMed  Google Scholar 

  4. Estrada-de los Santos P, Uriel Rojas-Rojas F, Yanet Tapia-Garcia E, Soledad Vasquez-Murrieta M, Hirsch A (2016) To split or not to split: an opinion on dividing the genus Burkholderia. Ann Microbiol 66:1303–1314

    Article  CAS  Google Scholar 

  5. 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 

  6. Shinjo R, Uesaka K, Ihara K, Sakazaki S, Yano K, Kondo M, Tanaka A (2018) Draft genome sequence of Burkholderia vietnamiensis strain RS1, a nitrogen-fixing endophyte isolated from sweet potato. Microbiol Resour Announc 7(3):e00820–e00818

    Article  PubMed  PubMed Central  Google Scholar 

  7. 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 (2007) 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 

  8. Reis VM, Estrada-de los Santos P, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Mavingui P, Baldani VL, Schmid M, Baldani JI, Balandreau J, Hartmann 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 

  9. Drigo B, Kowalchuk GA, Knapp BA, Pijl AS, Boschker HT, van Veen JA (2013) Impacts of 3 years of elevated atmospheric CO2 on rhizosphere carbon flow and microbial community dynamics. Glob Chang Biol 19:621–636

    Article  PubMed  Google Scholar 

  10. Draghi WO, Degrossi J, Bialer M, Brelles-Marino G, Abdian P, Soler-Bistue A, Wall L, Zorreguieta A (2018) Biodiversity of cultivable Burkholderia species in Argentinean soils under no-till agricultural practices. PLoS One 13:e0200651

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Eberl L, Vandamme P (2016) Members of the genus Burkholderia: good and bad guys. F1000Res 5:F1000

    Article  PubMed  PubMed Central  Google Scholar 

  12. Singh RK, Malik N, Singh S (2013) Improved nutrient use efficiency increases plant growth of rice with the use of IAA-overproducing strains of endophytic Burkholderia cepacia strain RRE25. Microb Ecol 66:375–384

    Article  CAS  PubMed  Google Scholar 

  13. Castanheira N, Dourado AC, Kruz S, Alves PI, Delgado-Rodriguez AI, Pais I, Semedo J, Scotti-Campos P, Sanchez C, Borges N, Carvalho G, Barreto Crespo MT, Fareleira P (2016) Plant growth-promoting Burkholderia species isolated from annual ryegrass in Portuguese soils. J Appl Microbiol 120:724–739

    Article  CAS  PubMed  Google Scholar 

  14. Mitter B, Petric A, Shin MW, Chain PS, Hauberg-Lotte L, Reinhold-Hurek B, Nowak J, Sessitsch A (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 4:120

    Article  PubMed  PubMed Central  Google Scholar 

  15. Jiang CY, Sheng XF, Qian M, Wang QY (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164

    Article  CAS  PubMed  Google Scholar 

  16. Compant S, Reiter B, Sessitsch A, Nowak J, Clement C, Ait Barka E (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Sheibani-Tezerji R, Rattei T, Sessitsch A, Trognitz F, Mitter B (2015) Transcriptome profiling of the endophyte Burkholderia phytofirmans PsJN indicates sensing of the plant environment and drought stress. MBio 6:e00621–e00615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Su F, Jacquard C, Villaume S, Michel J, Rabenoelina F, Clement C, Barka EA, Dhondt-Cordelier S, Vaillant-Gaveau N (2015) Burkholderia phytofirmans PsJN reduces impact of freezing temperatures on photosynthesis in Arabidopsis thaliana. Front Plant Sci 6:810

    PubMed  PubMed Central  Google Scholar 

  19. Kim M, Kim WS, Tripathi BM, Adams J (2014) Distinct bacterial communities dominate tropical and temperate zone leaf litter. Microb Ecol 67:837–848

    Article  CAS  PubMed  Google Scholar 

  20. Vu HP, Mu A, Moreau JW (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 

  21. Chain PS, Denef VJ, Konstantinidis KT, Vergez LM, Agullo L, Reyes VL, Hauser L, Cordova M, Gomez L, Gonzalez M, Land M, Lao V, Larimer F, LiPuma JJ, Mahenthiralingam E, Malfatti SA, Marx CJ, Parnell JJ, Ramette A, Richardson P, Seeger M, Smith D, Spilker T, Sul WJ, Tsoi TV, Ulrich LE, Zhulin IB, Tiedje JM (2006) Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci U S A 103:15280–15287

    Article  PubMed  PubMed Central  Google Scholar 

  22. Denet E, Coupat-Goutaland B, Nazaret S, Pelandakis M, Favre-Bonte S (2017) Diversity of free-living amoebae in soils and their associated human opportunistic bacteria. Parasitol Res 116:3151–3162

    Article  PubMed  Google Scholar 

  23. Noinarin P, Chareonsudjai P, Wangsomnuk P, Wongratanacheewin S, Chareonsudjai S (2016) Environmental free-living amoebae isolated from soil in Khon Kaen, Thailand, antagonize Burkholderia pseudomallei. PLoS One 11:e0167355

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y (2005) Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 71:20–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. De Smet B, Mayo M, Peeters C, Zlosnik JE, Spilker T, Hird TJ, LiPuma JJ, Kidd TJ, Kaestli M, Ginther JL, Wagner DM, Keim P, Bell SC, Jacobs JA, Currie BJ, Vandamme P (2015) Burkholderia stagnalis sp. nov. and Burkholderia territorii sp. nov., two novel Burkholderia cepacia complex species from environmental and human sources. Int J Syst Evol Microbiol 65:2265–2271

    Article  CAS  PubMed  Google Scholar 

  26. Sfeir MM (2018) Burkholderia cepacia complex infections: more complex than the bacterium name suggest. J Infect 77:166–170

    Article  PubMed  Google Scholar 

  27. Kenna DTD, Lilley D, Coward A, Martin K, Perry C, Pike R, Hill R, Turton JF (2017) Prevalence of Burkholderia species, including members of Burkholderia cepacia complex, among UK cystic and non-cystic fibrosis patients. J Med Microbiol 66:490–501

    Article  PubMed  Google Scholar 

  28. Medina-Pascual MJ, Valdezate S, Villalon P, Garrido N, Rubio V, Saez-Nieto JA (2012) Identification, molecular characterisation and antimicrobial susceptibility of genomovars of the Burkholderia cepacia complex in Spain. Eur J Clin Microbiol Infect Dis 31:3385–3396

    Article  CAS  PubMed  Google Scholar 

  29. Zlosnik JE, Zhou G, Brant R, Henry DA, Hird TJ, Mahenthiralingam E, Chilvers MA, Wilcox P, Speert DP (2015) Burkholderia species infections in patients with cystic fibrosis in British Columbia, Canada. 30 years’ experience. Ann Am Thorac Soc 12:70–78

    Article  PubMed  Google Scholar 

  30. Abdelfattah R, Al-Jumaah S, Al-Qahtani A, Al-Thawadi S, Barron I, Al-Mofada S (2018) Outbreak of Burkholderia cepacia bacteraemia in a tertiary care centre due to contaminated ultrasound probe gel. J Hosp Infect 98:289–294

    Article  CAS  PubMed  Google Scholar 

  31. Ahn Y, Kim JM, Lee YJ, LiPuma J, Hussong D, Marasa B, Cerniglia C (2017) Effects of extended storage of chlorhexidine gluconate and benzalkonium chloride solutions on the viability of Burkholderia cenocepacia. J Microbiol Biotechnol 27:2211–2220

    Article  CAS  PubMed  Google Scholar 

  32. Becker SL, Berger FK, Feldner SK, Karliova I, Haber M, Mellmann A, Schafers HJ, Gartner B (2018) Outbreak of Burkholderia cepacia complex infections associated with contaminated octenidine mouthwash solution, Germany, August to September 2018. Euro Surveill 23:1800540

    Article  PubMed Central  Google Scholar 

  33. Glowicz J, Crist M, Gould C, Moulton-Meissner H, Noble-Wang J, de Man TJB, Perry KA, Miller Z, Yang WC, Langille S, Ross J, Garcia B, Kim J, Epson E, Black S, Pacilli M, LiPuma JJ, Fagan R, Workgroup BcI (2018) A multistate investigation of health care-associated Burkholderia cepacia complex infections related to liquid docusate sodium contamination, January-October 2016. Am J Infect Control 46:649–655

    Article  PubMed  PubMed Central  Google Scholar 

  34. Song JE, Kwak YG, Um TH, Cho CR, Kim S, Park IS, Hwang JH, Kim N, Oh GB (2018) Outbreak of Burkholderia cepacia pseudobacteraemia caused by intrinsically contaminated commercial 0.5% chlorhexidine solution in neonatal intensive care units. J Hosp Infect 98:295–299

    Article  CAS  PubMed  Google Scholar 

  35. Brooks RB, Mitchell PK, Miller JR, Vasquez AM, Havlicek J, Lee H, Quinn M, Adams E, Baker D, Greeley R, Ross K, Daskalaki I, Walrath J, Moulton-Meissner H, Crist MB, Burkholderia cepacia Workgroup (2018) Multistate outbreak of Burkholderia cepacia complex bloodstream infections after exposure to contaminated saline flush syringes – United States, 2016–2017. Clin Infect Dis 69(3):445–449. https://doi.org/10.1093/cid/ciy910

    Article  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. Elshafie HS, Camele I, Racioppi R, Scrano L, Iacobellis NS, Bufo SA (2012) In vitro antifungal activity of Burkholderia gladioli pv. agaricicola against some phytopathogenic fungi. Int J Mol Sci 13:16291–16302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Simonetti E, Roberts IN, Montecchia MS, Gutierrez-Boem FH, Gomez FM, Ruiz JA (2018) A novel Burkholderia ambifaria strain able to degrade the mycotoxin fusaric acid and to inhibit Fusarium spp. growth. Microbiol Res 206:50–59

    Article  CAS  PubMed  Google Scholar 

  39. Swain DM, Yadav SK, Tyagi I, Kumar R, Kumar R, Ghosh S, Das J, Jha G (2017) A prophage tail-like protein is deployed by Burkholderia bacteria to feed on fungi. Nat Commun 8:404

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Zilinskas RA (2017) A brief history of biological weapons programmes and the use of animal pathogens as biological warfare agents. Rev Sci Tech 36:415–422

    Article  CAS  PubMed  Google Scholar 

  41. Program FSA (2017) 2017 Annual report of the Federal Select Agent Program. https://www.selectagents.gov/resources/FSAP_Annual_Report_2017.pdf

  42. Chou SH, Galperin MY (2016) Diversity of cyclic Di-GMP-binding proteins and mechanisms. J Bacteriol 198:32–46

    Article  CAS  PubMed  Google Scholar 

  43. Roelofs KG, Jones CJ, Helman SR, Shang X, Orr MW, Goodson JR, Galperin MY, Yildiz FH, Lee VT (2015) Systematic identification of cyclic-di-GMP binding proteins in Vibrio cholerae reveals a novel class of cyclic-di-GMP-binding ATPases associated with type II secretion systems. PLoS Pathog 11:e1005232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Romling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Wang YC, Chin KH, Tu ZL, He J, Jones CJ, Sanchez DZ, Yildiz FH, Galperin MY, Chou SH (2016) Nucleotide binding by the widespread high-affinity cyclic di-GMP receptor MshEN domain. Nat Commun 7:12481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Tal R, Wong HC, Calhoon R, Gelfand D, Fear AL, Volman G, Mayer R, Ross P, Amikam D, Weinhouse H, Cohen A, Sapir S, Ohana P, Benziman M (1998) Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180:4416–4425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Galperin MY (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188:4169–4182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Galperin MY (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol 5:35

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Johnson SL, Bishop-Lilly KA, Ladner JT, Daligault HE, Davenport KW, Jaissle J, Frey KG, Koroleva GI, Bruce DC, Coyne SR, Broomall SM, Li PE, Teshima H, Gibbons HS, Palacios GF, Rosenzweig CN, Redden CL, Xu Y, Minogue TD, Chain PS (2015) Complete genome sequences for 59 Burkholderia isolates, both pathogenic and near neighbor. Genome Announc 3:e00159-15

    Article  PubMed  PubMed Central  Google Scholar 

  50. NCBI. Burkholderia cenocepacia AU 1054 genome sequence. https://www.ncbi.nlm.nih.gov/genome/?term=Burkholderia%20cenocepacia%20AU%201054. Last accessed 20 Feb 2019

  51. Seo YS, Lim J, Choi BS, Kim H, Goo E, Lee B, Lim JS, Choi IY, Moon JS, Kim J, Hwang I (2011) Complete genome sequence of Burkholderia gladioli BSR3. J Bacteriol 193:3149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lim J, Lee TH, Nahm BH, Choi YD, Kim M, Hwang I (2009) Complete genome sequence of Burkholderia glumae BGR1. J Bacteriol 191:3758–3759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Nierman WC, DeShazer D, Kim HS, Tettelin H, Nelson KE, Feldblyum T, Ulrich RL, Ronning CM, Brinkac LM, Daugherty SC, Davidsen TD, Deboy RT, Dimitrov G, Dodson RJ, Durkin AS, Gwinn ML, Haft DH, Khouri H, Kolonay JF, Madupu R, Mohammoud Y, Nelson WC, Radune D, Romero CM, Sarria S, Selengut J, Shamblin C, Sullivan SA, White O, Yu Y, Zafar N, Zhou L, Fraser CM (2004) Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad Sci U S A 101:14246–14251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. NCBI. Burkholderia multivorans ATCC 17616 genome sequence. https://www.ncbi.nlm.nih.gov/genome/?term=Burkholderia%20multivorans%20ATCC%2017616. Last accessed 20 Feb 2019

  55. Moulin L, Klonowska A, Caroline B, Booth K, Vriezen JA, Melkonian R, James EK, Young JP, Bena G, Hauser L, Land M, Kyrpides N, Bruce D, Chain P, Copeland A, Pitluck S, Woyke T, Lizotte-Waniewski M, Bristow J, Riley M (2014) Complete genome sequence of Burkholderia phymatum STM815(T), a broad host range and efficient nitrogen-fixing symbiont of Mimosa species. Stand Genomic Sci 9:763–774

    Article  PubMed  PubMed Central  Google Scholar 

  56. Weilharter A, Mitter B, Shin MV, Chain PS, Nowak J, Sessitsch A (2011) Complete genome sequence of the plant growth-promoting endophyte Burkholderia phytofirmans strain PsJN. J Bacteriol 193:3383–3384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Holden MT, Titball RW, Peacock SJ, Cerdeno-Tarraga AM, Atkins T, Crossman LC, Pitt T, Churcher C, Mungall K, Bentley SD, Sebaihia M, Thomson NR, Bason N, Beacham IR, Brooks K, Brown KA, Brown NF, Challis GL, Cherevach I, Chillingworth T, Cronin A, Crossett B, Davis P, DeShazer D, Feltwell T, Fraser A, Hance Z, Hauser H, Holroyd S, Jagels K, Keith KE, Maddison M, Moule S, Price C, Quail MA, Rabbinowitsch E, Rutherford K, Sanders M, Simmonds M, Songsivilai S, Stevens K, Tumapa S, Vesaratchavest M, Whitehead S, Yeats C, Barrell BG, Oyston PC, Parkhill J (2004) Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A 101:14240–14245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Hayden HS, Lim R, Brittnacher MJ, Sims EH, Ramage ER, Fong C, Wu Z, Crist E, Chang J, Zhou Y, Radey M, Rohmer L, Haugen E, Gillett W, Wuthiekanun V, Peacock SJ, Kaul R, Miller SI, Manoil C, Jacobs MA (2012) Evolution of Burkholderia pseudomallei in recurrent melioidosis. PLoS One 7:e36507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. NCBI. Burkholderia rhizoxinica HKI 454 genome sequence. https://www.ncbi.nlm.nih.gov/genome/?term=Burkholderia+rhizoxinica+HKI+454. Last accessed 20 Feb 2019

  60. NCBI. Burkholderia sp. 383 genome sequence. https://www.ncbi.nlm.nih.gov/genome/?term=Burkholderia%20sp.%20383. Last accessed 20 Feb 2019

  61. NCBI. Burkholderia sp. CCGE1001 genome sequence. https://www.ncbi.nlm.nih.gov/genome/?term=Burkholderia%20sp.%20CCGE1001. Last accessed 20 Feb 2019

  62. Ormeno-Orrillo E, Rogel MA, Chueire LM, Tiedje JM, Martinez-Romero E, Hungria M (2012) Genome sequences of Burkholderia sp. strains CCGE1002 and H160, isolated from legume nodules in Mexico and Brazil. J Bacteriol 194:6927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. NCBI. Burkholderia sp. CCGE1003 genome sequence. https://www.ncbi.nlm.nih.gov/genome/?term=Burkholderia%20sp.%20CCGE1003. Last accessed 20 Feb 2019

  64. Kim HS, Schell MA, Yu Y, Ulrich RL, Sarria SH, Nierman WC, DeShazer D (2005) Bacterial genome adaptation to niches: divergence of the potential virulence genes in three Burkholderia species of different survival strategies. BMC Genomics 6:174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. NCBI. Burkholderia vietnamiensis G4 genome sequence. https://www.ncbi.nlm.nih.gov/genome/?term=Burkholderia+vietnamiensis+G4. Last accessed 20 Feb 2019

  66. Plumley BA, Martin KH, Borlee GI, Marlenee NL, Burtnick MN, Brett PJ, AuCoin DP, Bowen RA, Schweizer HP, Borlee BR (2017) Thermoregulation of biofilm formation in Burkholderia pseudomallei is disrupted by mutation of a putative diguanylate cyclase. J Bacteriol 199:5

    Article  Google Scholar 

  67. Lardi M, Aguilar C, Pedrioli A, Omasits U, Suppiger A, Carcamo-Oyarce G, Schmid N, Ahrens CH, Eberl L, Pessi G (2015) sigma54-dependent response to nitrogen limitation and virulence in Burkholderia cenocepacia strain H111. Appl Environ Microbiol 81:4077–4089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Tuanyok A, Mayo M, Scholz H, Hall CM, Allender CJ, Kaestli M, Ginther J, Spring-Pearson S, Bollig MC, Stone JK, Settles EW, Busch JD, Sidak-Loftis L, Sahl JW, Thomas A, Kreutzer L, Georgi E, Gee JE, Bowen RA, Ladner JT, Lovett S, Koroleva G, Palacios G, Wagner DM, Currie BJ, Keim P (2017) Burkholderia humptydooensis sp. nov., a new species related to Burkholderia thailandensis and the fifth member of the Burkholderia pseudomallei complex. Appl Environ Microbiol 83:e02802–e02816

    Article  PubMed  PubMed Central  Google Scholar 

  69. Dance DA (1991) Melioidosis: the tip of the iceberg? Clin Microbiol Rev 4:52–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Chirakul S, Norris MH, Pagdepanichkit S, Somprasong N, Randall LB, Shirley JF, Borlee BR, Lomovskaya O, Tuanyok A, Schweizer HP (2018) Transcriptional and post-transcriptional regulation of PenA beta-lactamase in acquired Burkholderia pseudomallei beta-lactam resistance. Sci Rep 8:10652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Limmathurotsakul D, Golding N, Dance DA, Messina JP, Pigott DM, Moyes CL, Rolim DB, Bertherat E, Day NP, Peacock SJ, Hay SI (2016) Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis. Nat Microbiol 1:15008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Kaestli M, Harrington G, Mayo M, Chatfield MD, Harrington I, Hill A, Munksgaard N, Gibb K, Currie BJ (2015) What drives the occurrence of the melioidosis bacterium Burkholderia pseudomallei in domestic gardens? PLoS Negl Trop Dis 9:e0003635

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Limmathurotsakul D, Kanoksil M, Wuthiekanun V, Kitphati R, deStavola B, Day NP, Peacock SJ (2013) Activities of daily living associated with acquisition of melioidosis in Northeast Thailand: a matched case-control study. PLoS Negl Trop Dis 7:e2072

    Article  PubMed  PubMed Central  Google Scholar 

  75. Hemarajata P, Baghdadi JD, Hoffman R, Humphries RM (2016) Burkholderia pseudomallei: challenges for the clinical microbiology laboratory. J Clin Microbiol 54:2866–2873

    Article  PubMed  PubMed Central  Google Scholar 

  76. Lee HS, Gu F, Ching SM, Lam Y, Chua KL (2010) CdpA is a Burkholderia pseudomallei cyclic di-GMP phosphodiesterase involved in autoaggregation, flagellum synthesis, motility, biofilm formation, cell invasion, and cytotoxicity. Infect Immun 78:1832–1840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Amikam D, Galperin MY (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3–6

    Article  CAS  PubMed  Google Scholar 

  78. Mangalea MR, Plumley BA, Borlee BR (2017) Nitrate sensing and metabolism inhibit biofilm formation in the opportunistic pathogen Burkholderia pseudomallei by reducing the intracellular concentration of c-di-GMP. Front Microbiol 8:1353

    Article  PubMed  PubMed Central  Google Scholar 

  79. Majerczyk CD, Brittnacher MJ, Jacobs MA, Armour CD, Radey MC, Bunt R, Hayden HS, Bydalek R, Greenberg EP (2014) Cross-species comparison of the Burkholderia pseudomallei, Burkholderia thailandensis, and Burkholderia mallei quorum-sensing regulons. J Bacteriol 196:3862–3871

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Price EP, Viberg LT, Kidd TJ, Bell SC, Currie BJ, Sarovich DS (2018) Transcriptomic analysis of longitudinal Burkholderia pseudomallei infecting the cystic fibrosis lung. Microb Genom 4:e000194

    PubMed Central  Google Scholar 

  81. Traverse CC, Mayo-Smith LM, Poltak SR, Cooper VS (2013) Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proc Natl Acad Sci U S A 110:E250–E259

    Article  CAS  PubMed  Google Scholar 

  82. Lazar Adler NR, Allwood EM, Deveson Lucas D, Harrison P, Watts S, Dimitropoulos A, Treerat P, Alwis P, Devenish RJ, Prescott M, Govan B, Adler B, Harper M, Boyce JD (2016) Perturbation of the two-component signal transduction system, BprRS, results in attenuated virulence and motility defects in Burkholderia pseudomallei. BMC Genomics 17:331

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Saikh KU, Mott TM (2017) Innate immune response to Burkholderia mallei. Curr Opin Infect Dis 30:297–302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Memisevic V, Zavaljevski N, Pieper R, Rajagopala SV, Kwon K, Townsend K, Yu C, Yu X, DeShazer D, Reifman J, Wallqvist A (2013) Novel Burkholderia mallei virulence factors linked to specific host-pathogen protein interactions. Mol Cell Proteomics 12:3036–3051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Bochkareva OO, Moroz EV, Davydov II, Gelfand MS (2018) Genome rearrangements and selection in multi-chromosome bacteria Burkholderia spp. BMC Genomics 19:965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Galyov EE, Brett PJ, DeShazer D (2010) Molecular insights into Burkholderia pseudomallei and Burkholderia mallei pathogenesis. Annu Rev Microbiol 64:495–517

    Article  CAS  PubMed  Google Scholar 

  87. Cloutier M, Muru K, Ravicoularamin G, Gauthier C (2018) Polysaccharides from Burkholderia species as targets for vaccine development, immunomodulation and chemical synthesis. Nat Prod Rep 35(12):1251–1293. https://doi.org/10.1039/c8np00046h

    Article  CAS  PubMed  Google Scholar 

  88. Borlee GI, Plumley BA, Martin KH, Somprasong N, Mangalea MR, Islam MN, Burtnick MN, Brett PJ, Steinmetz I, AuCoin DP, Belisle JT, Crick DC, Schweizer HP, Borlee BR (2017) Genome-scale analysis of the genes that contribute to Burkholderia pseudomallei biofilm formation identifies a crucial exopolysaccharide biosynthesis gene cluster. PLoS Negl Trop Dis 11:e0005689

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Rosenstein BJ, Hall DE (1980) Pneumonia and septicemia due to Pseudomonas cepacia in a patient with cystic fibrosis. Johns Hopkins Med J 147:188–189

    CAS  PubMed  Google Scholar 

  90. Hauser AR, Jain M, Bar-Meir M, McColley SA (2011) Clinical significance of microbial infection and adaptation in cystic fibrosis. Clin Microbiol Rev 24:29–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Ferreira AS, Leitao JH, Sousa SA, Cosme AM, Sa-Correia I, Moreira LM (2007) Functional analysis of Burkholderia cepacia genes bceD and bceF, encoding a phosphotyrosine phosphatase and a tyrosine autokinase, respectively: role in exopolysaccharide biosynthesis and biofilm formation. Appl Environ Microbiol 73:524–534

    Article  CAS  PubMed  Google Scholar 

  92. Ferreira AS, Silva IN, Oliveira VH, Cunha R, Moreira LM (2011) Insights into the role of extracellular polysaccharides in Burkholderia adaptation to different environments. Front Cell Infect Microbiol 1:16

    Article  PubMed  PubMed Central  Google Scholar 

  93. Romling U, Galperin MY (2015) Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions. Trends Microbiol 23:545–557

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Moreira LM, Videira PA, Sousa SA, Leitao JH, Cunha MV, Sa-Correia I (2003) Identification and physical organization of the gene cluster involved in the biosynthesis of Burkholderia cepacia complex exopolysaccharide. Biochem Biophys Res Commun 312:323–333

    Article  CAS  PubMed  Google Scholar 

  95. Fazli M, McCarthy Y, Givskov M, Ryan RP, Tolker-Nielsen T (2013) The exopolysaccharide gene cluster Bcam1330-Bcam1341 is involved in Burkholderia cenocepacia biofilm formation, and its expression is regulated by c-di-GMP and Bcam1349. Microbiology 2:105–122

    CAS  Google Scholar 

  96. Kumar B, Sorensen JL, Cardona ST (2018) A c-di-GMP-modulating protein regulates swimming motility of Burkholderia cenocepacia in response to arginine and glutamate. Front Cell Infect Microbiol 8:56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Richter AM, Fazli M, Schmid N, Shilling R, Suppiger A, Givskov M, Eberl L, Tolker-Nielsen T (2018) Key players and individualists of cyclic-di-GMP Signaling in Burkholderia cenocepacia. Front Microbiol 9:3286

    Article  PubMed  Google Scholar 

  98. Boon C, Deng Y, Wang LH, He Y, Xu JL, Fan Y, Pan SQ, Zhang LH (2008) A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J 2:27–36

    Article  CAS  PubMed  Google Scholar 

  99. Subramoni S, Sokol PA (2012) Quorum sensing systems influence Burkholderia cenocepacia virulence. Future Microbiol 7:1373–1387

    Article  CAS  PubMed  Google Scholar 

  100. McCarthy Y, Yang L, Twomey KB, Sass A, Tolker-Nielsen T, Mahenthiralingam E, Dow JM, Ryan RP (2010) A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia. Mol Microbiol 77:1220–1236

    Article  CAS  PubMed  Google Scholar 

  101. Deng Y, Schmid N, Wang C, Wang J, Pessi G, Wu D, Lee J, Aguilar C, Ahrens CH, Chang C, Song H, Eberl L, Zhang LH (2012) Cis-2-dodecenoic acid receptor RpfR links quorum-sensing signal perception with regulation of virulence through cyclic dimeric guanosine monophosphate turnover. Proc Natl Acad Sci U S A 109:15479–15484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Silva IN, Santos PM, Santos MR, Zlosnik JE, Speert DP, Buskirk SW, Bruger EL, Waters CM, Cooper VS, Moreira LM (2016) Long-term evolution of Burkholderia multivorans during a chronic cystic fibrosis infection reveals shifting forces of selection. mSystems 1:e00029–e00016

    Article  PubMed  PubMed Central  Google Scholar 

  103. Schmid N, Suppiger A, Steiner E, Pessi G, Kaever V, Fazli M, Tolker-Nielsen T, Jenal U, Eberl L (2017) High intracellular c-di-GMP levels antagonize quorum sensing and virulence gene expression in Burkholderia cenocepacia H111. Microbiology 163:754–764

    Article  CAS  PubMed  Google Scholar 

  104. Yang C, Cui C, Ye Q, Kan J, Fu S, Song S, Huang Y, He F, Zhang LH, Jia Y, Gao YG, Harwood CS, Deng Y (2017) Burkholderia cenocepacia integrates cis-2-dodecenoic acid and cyclic dimeric guanosine monophosphate signals to control virulence. Proc Natl Acad Sci U S A 114:13006–13011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Mangalea MR, Borlee GI, Borlee BR (2017) The current status of extracellular polymeric substances produced by Burkholderia pseudomallei. Curr Trop Med Rep 4:117–126

    Article  Google Scholar 

  106. Ferreira AS, Silva IN, Oliveira VH, Becker JD, Givskov M, Ryan RP, Fernandes F, Moreira LM (2013) Comparative transcriptomic analysis of the Burkholderia cepacia tyrosine kinase bceF mutant reveals a role in tolerance to stress, biofilm formation, and virulence. Appl Environ Microbiol 79:3009–3020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Fazli M, O’Connell A, Nilsson M, Niehaus K, Dow JM, Givskov M, Ryan RP, Tolker-Nielsen T (2011) The CRP/FNR family protein Bcam1349 is a c-di-GMP effector that regulates biofilm formation in the respiratory pathogen Burkholderia cenocepacia. Mol Microbiol 82:327–341

    Article  CAS  PubMed  Google Scholar 

  108. Fazli M, Rybtke M, Steiner E, Weidel E, Berthelsen J, Groizeleau J, Bin W, Zhi BZ, Yaming Z, Kaever V, Givskov M, Hartmann RW, Eberl L, Tolker-Nielsen T (2017) Regulation of Burkholderia cenocepacia biofilm formation by RpoN and the c-di-GMP effector BerB. Microbiology 6:e00480

    Article  CAS  PubMed Central  Google Scholar 

  109. Stanier RY, Palleroni NJ, Doudoroff M (1966) The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43:159–271

    Article  CAS  PubMed  Google Scholar 

  110. Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, LiPuma JJ, Mahenthiralingam E, Speert DP, Dowson C, Vandamme P (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59:102–111

    Article  CAS  PubMed  Google Scholar 

  111. Jung HI, Kim YJ, Lee YJ, Lee HS, Lee JK, Kim SK (2017) Mutation of the cyclic di-GMP phosphodiesterase gene in Burkholderia lata SK875 attenuates virulence and enhances biofilm formation. J Microbiol 55:800–808

    Article  CAS  PubMed  Google Scholar 

  112. Kikuchi Y, Yumoto I (2013) Efficient colonization of the bean bug Riptortus pedestris by an environmentally transmitted Burkholderia symbiont. Appl Environ Microbiol 79:2088–2091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Kim JK, Kwon JY, Kim SK, Han SH, Won YJ, Lee JH, Kim CH, Fukatsu T, Lee BL (2014) Purine biosynthesis, biofilm formation, and persistence of an insect-microbe gut symbiosis. Appl Environ Microbiol 80:4374–4382

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Ham JH, Melanson RA, Rush MC (2011) Burkholderia glumae: next major pathogen of rice? Mol Plant Pathol 12:329–339

    Article  CAS  PubMed  Google Scholar 

  115. Chen R, Barphagha IK, Ham JH (2015) Identification of potential genetic components involved in the deviant quorum-sensing signaling pathways of Burkholderia glumae through a functional genomics approach. Front Cell Infect Microbiol 5:22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Melanson RA, Barphagha I, Osti S, Lelis TP, Karki HS, Chen R, Shrestha BK, Ham JH (2017) Identification of new regulatory genes involved in the pathogenic functions of the rice-pathogenic bacterium Burkholderia glumae. Microbiology 163:266–279

    Article  CAS  PubMed  Google Scholar 

  117. Kumar R, Kumar Yadav S, Swain DM, Jha G (2017) Burkholderia gladioli strain NGJ1 deploys a prophage tail-like protein for mycophagy. Microb Cell 5:116–118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Nandakumar R, Shahjahan AKM, Yuan XL, Dickstein ER, Groth DE, Clark CA, Cartwright RD, Rush MC (2009) Burkholderia glumae and B. gladioli cause bacterial panicle blight in rice in the Southern United States. Plant Dis 93:896–905

    Article  CAS  PubMed  Google Scholar 

  119. Vigliani MB, Cunha CB (2018) Multiple recurrent abscesses in a patient with undiagnosed IL-12 deficiency and infection by Burkholderia gladioli. IDCases 12:80–83

    Article  PubMed  PubMed Central  Google Scholar 

  120. Zanotti C, Munari S, Brescia G, Barion U (2018) Burkholderia gladioli sinonasal infection. Eur Ann Otorhinolaryngol Head Neck Dis 136(1):55–56. https://doi.org/10.1016/j.anorl.2018.01.011

    Article  PubMed  Google Scholar 

  121. Shehata HR, Lyons EM, Jordan KS, Raizada MN (2016) Bacterial endophytes from wild and ancient maize are able to suppress the fungal pathogen Sclerotinia homoeocarpa. J Appl Microbiol 120:756–769

    Article  CAS  PubMed  Google Scholar 

  122. Shehata HR, Ettinger CL, Eisen JA, Raizada MN (2016) Genes required for the anti-fungal activity of a bacterial endophyte isolated from a corn landrace grown continuously by subsistence farmers since 1000 BC. Front Microbiol 7:1548

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO, USA

    Grace I. Borlee, Mihnea R. Mangalea & Bradley R. Borlee

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  1. Grace I. Borlee
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  2. Mihnea R. Mangalea
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  3. Bradley R. Borlee
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Correspondence to Bradley R. Borlee .

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Editors and Affiliations

  1. Institute of Biochemistry and Agricultural Biotechnology Center, National Chung Hsing University, Taichung, Taiwan

    Shan-Ho Chou

  2. Department of Biology, Faculty of Sciences, Universidad de Chile, Santiago, Chile

    Nicolas Guiliani

  3. Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD, USA

    Vincent T. Lee

  4. Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden

    Ute Römling

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Borlee, G.I., Mangalea, M.R., Borlee, B.R. (2020). Cyclic di-GMP in Burkholderia spp.. In: Chou, SH., Guiliani, N., Lee, V., Römling, U. (eds) Microbial Cyclic Di-Nucleotide Signaling. Springer, Cham. https://doi.org/10.1007/978-3-030-33308-9_30

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