Biofilm formation by strains of Burkholderia cenocepacia lineages IIIA and IIIB and B. gladioli pv. alliicola associated with onion bacterial scale rot.

Bacterial ecology Burkholderia cepacia complex Onion slippery skin Onion sour skin Plant pathogenic bacteria Swarming motility

Journal

Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology]
ISSN: 1678-4405
Titre abrégé: Braz J Microbiol
Pays: Brazil
ID NLM: 101095924

Informations de publication

Date de publication:
Dec 2021
Historique:
received: 25 02 2021
accepted: 27 06 2021
pubmed: 6 8 2021
medline: 15 12 2021
entrez: 5 8 2021
Statut: ppublish

Résumé

The Burkholderia genus has high ecological and nutritional versatility, having species capable of causing diseases in animals, humans, and plants. During chronic infections in humans, biofilm formation is a characteristic often associated with strains from different species of this genus. However, there is still no information on the formation of biofilms by plant pathogenic strains of B. cenocepacia (Bce) lineages IIIA and IIIB and B. gladioli pv. alliicola (Bga), which are associated with onion bacterial scale rot in the semi-arid region of northeast Brazil. In this study, we performed an in vitro characterization of biofilm formation ability in different culture media by the phytopathogenic strains of Bce and Bga and investigated its relationship with swarming motility. Our results indicated the existence of an intraspecific variation in biofilm formation capacity in vitro by these bacteria and the existence of a negative correlation between swarming motility and biofilm formation for strains of Bce lineage IIIB. In addition, histopathological analyses performed using optical microscopy and scanning electron microscopy revealed the formation of biofilm in vivo by Bce strains in onion tissues.

Identifiants

pubmed: 34351603
doi: 10.1007/s42770-021-00564-6
pii: 10.1007/s42770-021-00564-6
pmc: PMC8578472
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1665-1675

Subventions

Organisme : Brazilian National Research Council (CNPq)
ID : Process number 132864/2019-3

Informations de copyright

© 2021. Sociedade Brasileira de Microbiologia.

Références

Wordell Filho JA, Boff P (2006) “Doenças de origem parasitária.” In: WordellFilho JA, Rowe E, Gonçalves PAS, Debarba JF, Boff P, Thomazelli LF (eds) Manejo fitossanitário da cebola. EPAGRI, Florianopolis, pp 19–126
Silva AMF, Baia ADB, Velez LS, Oliveira WJ, Gama MAS (2018) Diversidade taxonômica e patológica de espécies de Burkholderia causadoras de podridão das escamas da cebola. Revisão Anual de Patologia de Plantas 26:81–95
Oliveira WJ, Silva WA, Silva AMF, Candeia JA, Souza EB, Mariano RLR, Gama MAS (2017) First report of Burkholderia cenocepacia causing sour skin of onion (Allium cepa) in Brazil. Plant Dis 101:1950. https://doi.org/10.1094/PDIS-05-17-0759-PDN
doi: 10.1094/PDIS-05-17-0759-PDN
Oliveira WJ, Souza EB, Silva AMF, Lima NB, Leal CM, Candeia JA, Gama MAS (2019) Elucidating the etiology of onion bacterial scale rot in the semiarid region of Northeastern Brazil. Trop Pant Pathol 44:494–502. https://doi.org/10.1007/s40858-019-00310-2
doi: 10.1007/s40858-019-00310-2
Baia ADB, Silva AMF, Ribeiro BG, Souza CC, Silva Júnior WJ, Balbino VQ, Leal CM, Farias ARG, Souza EB, Gama MAS (2020) Predominance of Burkholderia cenocepacia lineages causing onion sour skin in the semi-arid region of north-east Brazil. Plant Pathol 00:1–13. https://doi.org/10.1111/ppa.13311
doi: 10.1111/ppa.13311
Burkholder WH (1950) Sour skin, a bacterial rot of onion bulbs. Phytopathology 40:15–117
Burkholder WH (1942) Three bacterial plant pathogens: Phytomonas earyophylli sp.n., Phytomonas alliicola sp.n., and Phytomonas manihotis (Arthaud-Berthet et Sondar) Viégas. Phytopathology 32(2):141–149
Compant S, Nowak J, Coenye T, Clément C, AitBarka E (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32(4):607–626. https://doi.org/10.1111/j.1574-6976.2008.00113.x
doi: 10.1111/j.1574-6976.2008.00113.x pubmed: 18422616
Wallner A, King E, Ngonkeu ELM, Moulin L, Béna G (2019) Genomic analyses of Burkholderia cenocepacia reveal multiple species with differential host-adaptation to plants and humans. BMC Genomics 20:803. https://doi.org/10.1186/s12864-019-6186-z
doi: 10.1186/s12864-019-6186-z pubmed: 31684866 pmcid: 6829993
Segonds C, Heulin T, Marty N, Chabanon G (1999) Differentiation of Burkholderia species by PCR-restriction fragment length polymorphism analysis of the 16S rRNA gene and application to cystic fibrosis isolates. J Clin Microbiol 37(7):2201–2208. https://doi.org/10.1128/JCM.37.7.2201-2208.1999
doi: 10.1128/JCM.37.7.2201-2208.1999 pubmed: 10364586 pmcid: 85118
Sousa SA, Feliciano AR, Pita T, Guerreiro SI, Leitão JH (2017) Burkholderia cepacia complex regulation of virulence gene expression: a review. Genes 8(1):43. https://doi.org/10.3390/genes8010043
doi: 10.3390/genes8010043 pmcid: 5295037
Caraher E, Reynolds G, Murphy P, McClean S, Callaghan M (2007) Comparison of antibiotic susceptibility of Burkholderia cepacia complex organisms when grown planktonically or as biofilm in vitro. Eur J Clin Microbiol Infect Dis 26:213–216. https://doi.org/10.1007/s10096-007-0256-x
doi: 10.1007/s10096-007-0256-x pubmed: 17265071
Cunha MV, Sousa SA, Leitão JH, Moreira LM, Videira PA, Sa-Correia I (2004) Studies on the involvement of the exopolysaccharide produced by cystic fibrosis-associated isolates of the Burkholderia cepacia complex in biofilm formation and in persistence of respiratory infections. J Clin Microbiol 42(7):3052–3058. https://doi.org/10.1128/jcm.42.7.3052-3058.2004
doi: 10.1128/jcm.42.7.3052-3058.2004 pubmed: 15243059 pmcid: 446245
Leitão JH, Sousa SA, Ferreira AS, Ramos CG, Silva IN, Moreira LM (2010) Pathogenicity, virulence factors, and strategies to fight against Burkholderia cepacia complex pathogens and related species. Appl Microbiol Biotechnol 87(1):31–40. https://doi.org/10.1007/s00253-010-2528-0
doi: 10.1007/s00253-010-2528-0 pubmed: 20390415
Fazli M, Almblad H, Rybtke ML, Givskov M, Eberl L, Tolker-Nielsen T (2014) Regulation of biofilm formation in Pseudomonas and Burkholderia species. Environ Microbiol 16(7):1961–1981. https://doi.org/10.1111/1462-2920.12448
doi: 10.1111/1462-2920.12448 pubmed: 24592823
Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Ann Rev Microbiol 56(1):187–209. https://doi.org/10.1146/annurev.micro.56.012302.160705
doi: 10.1146/annurev.micro.56.012302.160705
Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14(9):563–575. https://doi.org/10.1038/nrmicro.2016.94
doi: 10.1038/nrmicro.2016.94 pubmed: 27510863
Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61(1):401–422. https://doi.org/10.1146/annurev.micro.61.080706.093316
doi: 10.1146/annurev.micro.61.080706.093316 pubmed: 17506679
Velez LS, Silva AMF, Santos CAF, Assunção EF, Silva MS, Souza EB, Gama MAS (2020) Evaluation of onion genotypes to slippery skin caused by Burkholderia gladioli pv. alliicola. Hortic Bras 38:000–000. https://doi.org/10.1590/s0102-053620200402
doi: 10.1590/s0102-053620200402
Antunes AL, Trentin DS, Bonfanti JW, Pinto CC, Perez LR, Macedo AJ, Barth AL (2010) Application of a feasible method for determination of biofilm antimicrobial susceptibility in staphylococci. Acta Pathol Microbiol Immunol Scand 118:873–877. https://doi.org/10.1111/j.1600-0463.2010.02681.x
doi: 10.1111/j.1600-0463.2010.02681.x
Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M (2000) A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 40(2):175–179. https://doi.org/10.1016/s0167-7012(00)00122-6
doi: 10.1016/s0167-7012(00)00122-6 pubmed: 10699673
Makizumi Y, Igarashi M, Gotoh K, Murao K, Yamamoto M, Udonsri N, Ochiai H, Thummabenjapone P, Kaku H (2011) Genetic diversity and pathogenicity of cucurbit associated Acidovorax. J Gen Plant Pathol 77:24–32. https://doi.org/10.1007/s10327-010-0273-y
doi: 10.1007/s10327-010-0273-y
Caputo LFG, Gitirana LB, Manso PPA (2010) Técnicas histológicas. In: Molinaro EM, Caputo LFG, Amendoeiro MR (eds) Conceitos e métodos para a formação de profissionais em laboratórios de saúde, 2nd edn. EPSJV, IOC, Rio de Janeiro, pp 89–174
Fonseca SC, Silva CL, Xavier MF (2005) Microstructural analysis of fresh-cut red bell pepper (Capsicum annuum L.) for postharvest quality optimization. Electron J Environ Agric Food Chem 3:1081–1085
Rashid MH, Kornberg A (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 97:4885–4890. https://doi.org/10.1073/pnas.060030097
doi: 10.1073/pnas.060030097 pubmed: 10758151 pmcid: 18327
Barbosa JC, Maldonado JRW (2014) AgroEstat - system for statistical analysis of agronomic trials - Version 1.1.0.711. Faculty of Agrarian and Veterinary Sciences, Sao Paulo State University, Jaboticabal
Conway BA, Venu V, Speert DP (2002) Biofilm Formation and Acyl Homoserine Lactone Production in the Burkholderia cepacia Complex. J Bacteriol 184(2):5678–5685. https://doi.org/10.1128/jb.184.20.5678-5685.2002
doi: 10.1128/jb.184.20.5678-5685.2002 pubmed: 12270826 pmcid: 139610
Sena-Vélez M, Redondo C, Gell I, Ferragud E, Johnson E, Graham JH, Cubero J (2015) Biofilm formation and motility of Xanthomonas strains with different citrus host range. Plant Pathol 64:767–775. https://doi.org/10.1111/ppa.12311
doi: 10.1111/ppa.12311
Guerra ML, Malafaia CB, Macedo AJ, Silva MV, Mariano RLR, Souza EB (2017) Biofilm formation by Xanthomonas campestris pv. viticola affected by abiotic surfaces and culture media. Trop Plant Pathol 43(2):146–151. https://doi.org/10.1007/s40858-017-0190-0
Malafaia CB, Barros MP, Macedo AJ, Guerra ML, Souza EB, Correia MTS, Silva MV (2018) Biofilm formation by phytopathogenic bacteria Acidovorax citrulli and Ralstonia solanacearum. J Environ Anal Prog 3(4):347–355.  https://doi.org/10.24221/jeap.3.4.2018.2018.347-355
Martinez LC, Vadyvaloo V (2014) Mechanisms of post-transcriptional gene regulation in bacterial biofilms. Front Cell Infect Microbiol 4:38. https://doi.org/10.3389/fcimb.2014.00038
doi: 10.3389/fcimb.2014.00038 pubmed: 24724055 pmcid: 3971182
Tang J, Chen J, Liu J, Zhang R, Yang R, Chen L (2012) Effects of different cultivation conditions on Staphylococcus aureus biofilm formation and diversity of adhesin genes. J Food Saf 32(2):210–218. https://doi.org/10.1111/j.1745-4565.2012.00370.x
doi: 10.1111/j.1745-4565.2012.00370.x
Petrova OE, Sauer K (2012) Sticky situations: key components that control bacterial surface attachment. J Bacteriol 194(10):2413–2425. https://doi.org/10.1128/JB.00003-12
doi: 10.1128/JB.00003-12 pubmed: 22389478 pmcid: 3347170
Ghosh R, Barman S, Mandal NC (2019) Phosphate deficiency induced biofilm formation of Burkholderia on insoluble phosphate granules plays a pivotal role for maximum release of soluble phosphate. Sci Rep 9(1):5477. https://doi.org/10.1038/s41598-019-41726-9
doi: 10.1038/s41598-019-41726-9 pubmed: 30940828 pmcid: 6445130
Pellizzoni E, Ravalico F, Scaini D, Delneri A, Rizzo R, Cescutti P (2016) Biofilms produced by Burkholderia cenocepacia: influence of media and solid supports on composition of matrix exopolysaccharides. Microbiology 162(2):283–294. https://doi.org/10.1099/mic.0.000214
doi: 10.1099/mic.0.000214 pubmed: 26586192
Rigano LA, Siciliano F, Enrique R, Sendín L, Filippone P, Torres PS, Qüesta J, Dow JM, Castagnaro AP, Vojnov AA, Marano MR (2007) Biofilm formation, epiphytic fitness, and canker development in Xanthomonas axonopodis pv.citri. Mol Plant Microbe Interact 20(10):1222–1230. https://doi.org/10.1094/MPMI-20-10-1222
Mohan R, Benton M, Dangelmaier E, Fu Z, Chandra Sekhar A (2018) Quorum sensing and biofilm formation in pathogenic and mutualistic plant-bacterial interactions. In: Bramhachari PV (ed) Implication of quorum sensing system in biofilm formation and virulence. Springer, Singapore. https://doi.org/10.1007/978-981-13-2429-1_9
Kado CI (2010) Plant bacteriology. APS Press, St Paul
Whitaker JR (1990) Microbial pectinolytic enzymes. In: Fogarty WM, Kelly CT (eds) Microbial enzymes and biotechnology, 2nd edn. Elsevier Science Ltd, England, pp 133–176
Jayani RS, Saxena S, Gupta R (2005) Microbial pectinolytic enzymes: a review. Process Biochem 40:2931–2944. https://doi.org/10.1016/j.procbio.2005.03.026
doi: 10.1016/j.procbio.2005.03.026
Morris CE, Monier JM (2003) The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol 41(1):429–453. https://doi.org/10.1146/annurev.phyto.41.022103.134521
doi: 10.1146/annurev.phyto.41.022103.134521 pubmed: 12730399
Toyofuku M, Inaba T, Kiyokawa T, Obana N, Yawata Y, Nomura N (2015) Environmental factors that shape biofilm formation. Biosci Biotechnol Biochem 80(1):7–12. https://doi.org/10.1080/09168451.2015.1058701
doi: 10.1080/09168451.2015.1058701 pubmed: 26103134
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8(9):623–633. https://doi.org/10.1038/nrmicro2415
doi: 10.1038/nrmicro2415 pubmed: 20676145
Verstraeten N, Braeken K, Debkumari B, Fauvart M, Fransaer J, Vermant J, Michiels J (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol 16(10):496–506. https://doi.org/10.1016/j.tim.2008.07.004
doi: 10.1016/j.tim.2008.07.004 pubmed: 18775660
Kearns DB (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8(9):634–644. https://doi.org/10.1038/nrmicro2405
doi: 10.1038/nrmicro2405 pubmed: 20694026 pmcid: 3135019
Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S, Eberl L (2001) The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147(9):2517–2528. https://doi.org/10.1099/00221287-147-9-2517
doi: 10.1099/00221287-147-9-2517 pubmed: 11535791
Guttenplan SB, Kearns DB (2013) Regulation of flagellar motility during biofilm formation. FEMS Microbiol Rev 37(6):849–871. https://doi.org/10.1111/1574-6976.12018
doi: 10.1111/1574-6976.12018 pubmed: 23480406

Auteurs

Pedro Henrique Rodrigues da Silva (PHR)

Departamento de Agronomia, Universidade Federal Rural de Pernambuco, Recife, Pernambuco, Brazil.

Emanuel Feitosa de Assunção (EF)

Departamento de Agronomia, Universidade Federal Rural de Pernambuco, Recife, Pernambuco, Brazil.

Leandro da Silva Velez (L)

Departamento de Agronomia, Universidade Federal Rural de Pernambuco, Recife, Pernambuco, Brazil.

Lucas Nascimento Dos Santos (LN)

Departamento de Agronomia, Universidade Federal Rural de Pernambuco, Recife, Pernambuco, Brazil.

Elineide Barbosa de Souza (EB)

Departamento de Biologia, Universidade Federal Rural de Pernambuco, Recife, Pernambuco, Brazil.

Marco Aurélio Siqueira da Gama (MAS)

Departamento de Agronomia, Universidade Federal Rural de Pernambuco, Recife, Pernambuco, Brazil. mas.gama@yahoo.com.br.

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Classifications MeSH