Investigation of factors related to biofilm formation in <i>Providencia stuartii</i>

SILVA, SIVONEIDE M. DA; RAMOS, BÁRBARA A.; SÁ, RAFAEL A.Q.C. DE; SILVA, MÁRCIA V. DA; CORREIA, MARIA T.S.; OLIVEIRA, MARIA B.M. DE

doi:10.1590/0001-3765202220210765

SIVONEIDE M. DA SILVA

Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Bioquímica, Av. Prof. Moraes Rego, 1235, Cidade Universitária, 50670-901 Recife, PE, Brazil

https://orcid.org/0000-0002-6507-2609

BÁRBARA A. RAMOS

Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Bioquímica, Av. Prof. Moraes Rego, 1235, Cidade Universitária, 50670-901 Recife, PE, Brazil

https://orcid.org/0000-0002-1166-8183

RAFAEL A.Q.C. DE SÁ

Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Bioquímica, Av. Prof. Moraes Rego, 1235, Cidade Universitária, 50670-901 Recife, PE, Brazil

https://orcid.org/0000-0002-0313-1482

MÁRCIA V. DA SILVA

Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Bioquímica, Av. Prof. Moraes Rego, 1235, Cidade Universitária, 50670-901 Recife, PE, Brazil

https://orcid.org/0000-0002-2221-5059

MARIA T.S. CORREIA

Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Bioquímica, Av. Prof. Moraes Rego, 1235, Cidade Universitária, 50670-901 Recife, PE, Brazil

https://orcid.org/0000-0003-4920-9975

MARIA B.M. DE OLIVEIRA

Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Bioquímica, Av. Prof. Moraes Rego, 1235, Cidade Universitária, 50670-901 Recife, PE, Brazil

https://orcid.org/0000-0001-5188-3243

Correspondence to: Sivoneide Maria da Silva E-mail: sivoneidems@gmail.com

AUTHOR CONTRIBUTIONS

SIVONEIDE M. DA SILVA, BÁRBARA A. RAMOS and RAFAEL A.Q.C DE SÁ contributed with laboratory experiments, writing and study design. In addition, MÁRCIA V. DA SILVA, MARIA T.S. CORREIA and MARIA B.M. DE OLIVEIRA read and approved the final manuscript.

Isolates	Biofilm			Hidrophobicity	Genes
Isolates	BHI	LB	TSB	Hidrophobicity	fimH	mrkD
8234	+++	++	+++	Hydrophilic	–	–
8686	+++	++	+++	Hydrophilic	–	–
8763	+++	++	+++	Hydrophilic	–	–
8944	++	++	++	Hydrophilic	–	–
8945	+++	+++	+++	Hydrophilic	–	–
8953	+++	++	+++	Hydrophilic	–	–
8972	+++	++	+++	Hydrophilic	–	–
10702	+++	++	+++	Hydrophilic	–	–
11255	+++	++	+++	Hydrophilic	–	–
11933	+++	++	+++	Hydrophilic	–	–
12353	+++	++	+++	MO Hydrophobic	–	–
12536	++	+++	++	Hydrophilic	–	–
12692	++	++	++	Hydrophilic	–	–
12953	+++	++	+++	Hydrophilic	–	–
13638	+++	++	+++	Hydrophilic	–	–
13646	+++	++	+++	Hydrophilic	–	–
13648	+++	++	+++	Hydrophilic	–	–
13684	+++	++	+++	Hydrophilic	–	–
13762	+++	++	+++	Hydrophilic	–	–
14051	+++	+++	+++	Hydrophilic	–	–
14569	+++	++	+++	Hydrophilic	–	–
15060	+++	++	+++	Hydrophilic	–	–
16995	++	++	++	Hydrophilic	–	–
17852	+++	++	+++	Hydrophilic	–	–
18809	++	++	++	Hydrophilic	–	–
01011	+++	+++	+++	Hydrophilic	–	–
01474	+++	++	+++	Hydrophilic	–	–
04446	+	+	+	Hydrophilic	–	–

Gene	Enterobacteriaceae	References
fimH	Edwardsiella piscicida	Zhang et al. (2019)ZHANG Q, HE TT, LI DY, LIU LY, NIE P & XIE HX. 2019. The Edwardsiella piscicida Type III Effector EseJ Suppresses Expression of Type 1 Fimbriae, Leading to Decreased Bacterial Adherence to Host Cells. Infect Immun 87: 00187-19.
	Enterobacter aerogenes	Azevedo et al. (2018)AZEVEDO PAA, FURLAN JPR, SILVA MO, SILVA RN, GOMES CN, COSTA KRC, STEHLING EG & SILVA AP. 2018. Detection of virulence and β-lactamase encoding genes in Enterobacter aerogenes and Enterobacter cloacae clinical isolates from Brazil. Braz J Microbiol 49: 224-228.
	Escherichia coli	Feenstra et al. (2017)FEENSTRA T ET AL. 2017. Adhesion of Escherichia coli under flow conditions reveals potential novel effects of FimH mutations. Eur J Clin Microbiol Infect Dis 36: 467-478., Chen et al. (2018)CHEN Z, PHAN MD, BATES LJ, PETERS KM, MUKERJEE C, MOORE KH & SCHEMBRI MA. 2018. The urinary microbiome in patients with refractory urge incontinence and recurrent urinary tract infection. Int Urogynecol J 29: 1775-1782., Rabbani et al. (2018)RABBANI S, FIEGE B, ERIS D, SILBERMANN M, JAKOB RP, NAVARRA G, MAIER T & ERNST B. 2018. Conformational switch of the bacterial adhesin FimH in the absence of the regulatory domain: Engineering a minimalistic allosteric system. J Biol Chem 293: 1835-1849., Zhang et al. (2020)ZHANG W, XU L, PARK HB, HWANG J, KWAK M, LEE PCW, LIANG G, ZHANG X, XU J & JIN JO. 2020. Escherichia coli adhesion portion FimH functions as an adjuvant for cancer immunotherapy. Nat Commun 11: 1187.
	Klebsiella pneumoniae	Ferreira et al. (2019)FERREIRA RL ET AL. 2019. High Prevalence of Multidrug-Resistant Klebsiella pneumoniae Harboring Several Virulence and β-Lactamase Encoding Genes in a Brazilian Intensive Care Unit. Front Microbiol 9: 3198.
	Klebsiella oxytoca	Ghasemian et al. (2018)GHASEMIAN A, MOBAREZ AM, PEERAYEH SN & ABADI ATB. 2018. The association of surface adhesin genes and the biofilm formation among Klebsiella oxytoca clinical isolates. New Microbes New Infect 27: 36-39.
	Salmonella enterica Enterica	Rakov et al. (2019)RAKOV AV, MASTRIANI E, LIU SL & SCHIFFERLI DM. 2019. Association of Salmonella virulence factor alleles with intestinal and invasive serovars. BMC Genomics 20: 429.
	Salmonella enterica serovar Enteritidis	Kuźmińska-Bajor et al. (2012KUŹMIŃSKA-BAJOR M, KUCZKOWSKI M, GRZYMAJLO K, WOJCIECH Ł, SABAT M, KISIELA D, WIELICZKO A & UGORSKI M. 2012. Decreased colonization of chicks by Salmonella enterica serovar Gallinarum expressing mannose-sensitive FimH adhesin from Salmonella enterica serovar Enteritidis. Vet Microbiol 158: 205-210., 2015KUŹMIŃSKA-BAJOR M, GRZYMAJLO K & UGORSKI M. 2015. Type 1 fimbriae are important factors limiting the dissemination and colonization of mice by Salmonella Enteritidis and contribute to the induction of intestinal inflammation during Salmonella invasion. Front Microbiol 6: 276.)
	Salmonella enterica serovar Choleraesuis	Grzymajlo et al. (2013)GRZYMAJLO K, UGORSKI M, KOLENDA R, KĘDZIERSKA A, KUZMINSKA-BAJOR M & WIELICZKO A. 2013. FimH adhesin from host unrestricted Salmonella Enteritidis binds to different glycoprotein ligands expressed by enterocytes from sheep, pig and cattle than FimH adhesins from host restricted Salmonella Abortus-ovis, Salmonella Choleraesuis and Salmonella Dublin. Vet Microbiol 166: 550-557., Lee & Yeh (2016)LEE CA & YEH KS. 2016. The Non-Fimbriate Phenotype Is Predominant among Salmonella enterica Serovar Choleraesuis from Swine and Those Non-Fimbriate Strains Possess Distinct Amino Acid Variations in FimH. PLoS ONE 11: 0151126.
	Salmonella enterica serovar Typhimurium	Zeiner et al. (2012)ZEINER SA, DWYER BE & CLEGG S. 2012. FimA, FimF, and FimH are necessary for assembly of type 1 fimbriae on Salmonella enterica serovar Typhimurium. Infect Immun 80: 3289-3296., Uchiya et al. (2019)UCHIYA KI, KAMIMURA Y, JUSAKON A & NIKAI T. 2019. Salmonella Fimbrial Protein FimH Is Involved in Expression of Proinflammatory Cytokines in a Toll-Like Receptor 4-Dependent Manner. Infect Immun 87: 00881-18.
mrkD	Citrobacter freundii	Ong et al. (2010)ONG CL, BEATSON SA, TOTSIKA M, FORESTIER C, MCEWAN AG & SCHEMBRI MA. 2010. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol 10: 183.
	Citrob acter koseri	Ong et al. (2010)ONG CL, BEATSON SA, TOTSIKA M, FORESTIER C, MCEWAN AG & SCHEMBRI MA. 2010. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol 10: 183.
	Enterobacter aerogenes	Azevedo et al. (2018)AZEVEDO PAA, FURLAN JPR, SILVA MO, SILVA RN, GOMES CN, COSTA KRC, STEHLING EG & SILVA AP. 2018. Detection of virulence and β-lactamase encoding genes in Enterobacter aerogenes and Enterobacter cloacae clinical isolates from Brazil. Braz J Microbiol 49: 224-228.
	Enterobacter cloacae	Amaretti et al. (2020)AMARETTI A, RIGHINI L, CANDELIERE F, MUSMECI E, BONVICINI F, GENTILOMI GA, ROSSI M & RAIMONDI S. 2020. Antibiotic Resistance, Virulence Factors, Phenotyping, and Genotyping of Non-Escherichia coli Enterobacterales from the Gut Microbiota of Healthy Subjects. Int J Mol Sci 21: 1847.
	Escherichia coli	Ong et al. (2010)ONG CL, BEATSON SA, TOTSIKA M, FORESTIER C, MCEWAN AG & SCHEMBRI MA. 2010. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol 10: 183., Stahlhut et al. (2013)STAHLHUT SG, CHATTOPADHYAY S, KISIELA DI, HVIDTFELDT K, CLEGG S, STRUVE C, SOKURENKO EV & KROGFELT KA. 2013. Structural and population characterization of MrkD, the adhesive subunit of type 3 fimbriae. J Bacteriol 195: 5602-5613.
	Klebsiella oxytoca	Ong et al. (2010)ONG CL, BEATSON SA, TOTSIKA M, FORESTIER C, MCEWAN AG & SCHEMBRI MA. 2010. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol 10: 183., Ghasemian et al. (2018)GHASEMIAN A, MOBAREZ AM, PEERAYEH SN & ABADI ATB. 2018. The association of surface adhesin genes and the biofilm formation among Klebsiella oxytoca clinical isolates. New Microbes New Infect 27: 36-39.
	Klebsiella pneumoniae	Ong et al. (2010)ONG CL, BEATSON SA, TOTSIKA M, FORESTIER C, MCEWAN AG & SCHEMBRI MA. 2010. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol 10: 183., Stahlhut et al. (2013)STAHLHUT SG, CHATTOPADHYAY S, KISIELA DI, HVIDTFELDT K, CLEGG S, STRUVE C, SOKURENKO EV & KROGFELT KA. 2013. Structural and population characterization of MrkD, the adhesive subunit of type 3 fimbriae. J Bacteriol 195: 5602-5613., Ferreira et al. (2019)FERREIRA RL ET AL. 2019. High Prevalence of Multidrug-Resistant Klebsiella pneumoniae Harboring Several Virulence and β-Lactamase Encoding Genes in a Brazilian Intensive Care Unit. Front Microbiol 9: 3198., Imai et al. (2019)IMAI K ET AL. 2019. Clinical characteristics in blood stream infections caused by Klebsiella pneumoniae, Klebsiella variicola, and Klebsiella quasipneumoniae: a comparative study, Japan, 2014-2017. BMC Infect Dis 19: 946., Amaretti et al. (2020)AMARETTI A, RIGHINI L, CANDELIERE F, MUSMECI E, BONVICINI F, GENTILOMI GA, ROSSI M & RAIMONDI S. 2020. Antibiotic Resistance, Virulence Factors, Phenotyping, and Genotyping of Non-Escherichia coli Enterobacterales from the Gut Microbiota of Healthy Subjects. Int J Mol Sci 21: 1847.
	Klebsiella quasipneumoniae	Imai et al. (2019)IMAI K ET AL. 2019. Clinical characteristics in blood stream infections caused by Klebsiella pneumoniae, Klebsiella variicola, and Klebsiella quasipneumoniae: a comparative study, Japan, 2014-2017. BMC Infect Dis 19: 946.
	Klebsiella variicola	Imai et al. (2019)IMAI K ET AL. 2019. Clinical characteristics in blood stream infections caused by Klebsiella pneumoniae, Klebsiella variicola, and Klebsiella quasipneumoniae: a comparative study, Japan, 2014-2017. BMC Infect Dis 19: 946.

[1] Correspondence to: Sivoneide Maria da Silva E-mail: sivoneidems@gmail.com

Brasil

Brasil

Investigation of factors related to biofilm formation in Providencia stuartii

Abstract