Biofilm can be defined as a structured consortium attached to a living or inert surface, which is formed as a result of encircling microorganisms by the extracellular polymeric substance (EPS) produced by them . Biofilms usually contain 10–25% cells and 75–90% EPS depending on the species that make up them . As will be discussed later, EPS has much more function than a sticky substance that holds cells together. Enormous advances in omic technologies, molecular biology and computer technology have revolutionized biofilm research. The fact that no habitats are occupied by only one bacterial species emphasizes the importance of working with biofilms. The types of microorganisms found in different habitats are capable of establishing various forms of interaction and communication between them to create stable communities. All these determinations brought together the research of the structure, formation and regulation mechanisms of biofilms. Researchers have found that biofilms consisting of more than one species are more stable and exhibit a lower level of nutritional requirements than biofilms formed by single cell species [3, 4]. Also multi-species biofilms exhibited higher tolerance to disinfectants, antimicrobial agents and predation. With the light of these findings recent researches focus on autotrophic-heterotrophic interactions between various microbial species using chemical signals, other interactions, competition and cooperation .
EPS generally consists of polysaccharides, proteins, nucleic acids and lipids. These components form the three-dimensional polymer network structure that provides the mechanical stability of the biofilm, forming the adhesive form, adhering to a surface and communication between the cells forming the biofilm . The purpose of the biofilm is to protect microorganisms from external factors or to gather nutrients within it. Biofilms are of great importance in the food industry due to their negative effects on both industrial production processes and health. The damage caused by microbial biofilms on medical and industrial tools and production surfaces, energy and product losses they cause in production processes and persistent recurrent infections are among the most important microbial problems in the world .
The use or control of any process or activity of biofilms for scientific or technological purposes is possible by knowing the formation and regulation of biofilms significantly. Biofilm formation is generally a multistage process. The first stage is the process of bacterial attachment to biotic or abiotic surfaces. This process is examined in two phases as reversible adhesion and irreversible adhesion. Although the bacterial cell is very close to the biotic and abiotic surface in reversible adhesion, it is the stage where no physical contact is provided. In this process, besides electrostatic forces, surface pH, nutrient concentration, temperature and hydrophobicity are also active. In addition, especially extracellular proteins attached to the surface may play a role in achieving the first physical contact with bacteria. In the irreversible adsorption – the second phase of the adsorption-dipole-dipole interactions, ionic and covalent bonds, hydrophobic interactions and hydrogen bonds play a critical role. After irreversible attachment, bacteria attached to the surface divide and form microcolonies. Many microcolonies can be produced in a biofilm structure depending on the number of bacteria attached to the surface from different regions. The bound cells are then matured and taken into the extracellular polymeric substance (EPS) produced by the cells that form the microcolonies. This EPS is responsible for the formation of the three-dimensional architectural structure and the stabilization of biofilms. Among the microcolonies within the EPS, a three-dimensional form of water channels and a primitive discharge system network, which serves in the transmission of food and waste, are formed. It has a linear or branched molecular structure formed by a repeating sugar (homopolysaccharides) or a mixture of different sugars (heteropolisaccharides). Although the EPS matrix varies according to the cell type that forms the biofilm; in general it contains 94–97% water, 1–2% extracellular nucleic acid and different lipids and 1–2% proteins. Biofilms that have completed their maturation are in the process of disintegration at the last stage. At this stage, the disruption of the enzymatic processes and matrix integrity due to other physical and chemical factors and the separation of planktonic cells from the biofilm matrix are involved  (Figure 1). In the light of the information obtained to date, it is believed that bacteria generally use environmental signals, flagella, outer membrane proteins, pili or lipopolysaccharides (LPS) for the formation of microcolonies and quorum sensing (QS) molecules to form biofilm structure . However; many questions regarding genetic and biochemical mechanisms involved in the perception of the surface by bacteria and the production of different stages during biofilm formation have not yet been lightened yet .
Members of the food-borne Salmonella enterica species, belonging to the Enterobacteriaceae family, have the ability to form biofilms both on biotic and abiotic surfaces in their natural life cycle [10, 11]. It is imperative to target the biofilms created by these bacteria in minimizing the industrial problems they cause, in addition to the control and treatment of infections caused by Salmonella species in humans and animals, which have been identified with more than 2500 serotypes to date. Main components of extracellular polymeric matrix (EPS) in Salmonella biofilms are curli fimbria and cellulose. These components, together or individually; plays a key role in the attachment of the bacteria to a surface, cell clustering and the formation of the biofilm structure [12–16]. The expression of curli fimbria in Salmonella in most cases has common regulation systems with cellulose production in which cell to cell and cell to surface interactions work together .
One of the most important features that play a role in Samonella virulence is the biofilm forming properties of the serovarieties of this genus. Therefore, it is extremely important to define the genetic, physiological and biochemical properties and microbial community characteristics of the biofilm structures in question. In this review article, it is aimed to summarize the information available in the literature on Salmonella biofilms and to define future perspectives.
Regulation of Biofilm Formation in Salmonella
Salmonella members show a morphotype called “rdar” because of its red, dry and rough structure on agar containing Congo Red . This biofilm form is formed by the expression of the two main matrix compotents, cellulose and curli fimbria, of Salmonella [18–21]. The transcriptional regulator CsgD protein is the main regulator of the “rdar” morphotypes . CsgD regulates the transcription of the csgBAC operon encoding the structural subunits of the curli fimbria and indirectly contributes to cellulose production by activation of adrA transcription [13, 22]. AdrA protein is a diguanylate cyclase that binds to cellulose and synthesizes secondary messenger cyclic diguanosine monophosphate (cyclic diguanosine monophosphate, c-di-GMP) that activates cellulose. C-di-GMP regulates the bcsABZC operon encoding genes, transcribed during the cellulose biosynthesis, in the post-transcriptional phase by changing the concentration of c-di-GMP [13, 23].
csgD is an integral part of the curli fimbria biosynthesis system, which is created by different transcribing of csgBAC and csgDEFG operons. The CsgD transcriptional regulator contains an acceptor N-terminal region. There is a preserved aspartate (D59) in this region. The csgD mutant strains exhibit a “saw” (smooth and white; plain and white) phenotype in the Congo Red (CR) agar medium. Point mutations that may occur in the csgD promotor region (in the 521 bp region between the csgB and csgD genes) can convert the protected promoter region from a highly regulated form to a semi-conservative form . As a result of passivating this gene in csgD insertion mutants, strains cannot form a pellicle structure in Luria Bertani (LB) broth, while ATM (adhesion test medium) can . At the nucleotide and protein level, the high similarity of S. Typhimurium and E. coli curli fimbriae indicates that these genes evolved from a common ancestor. Comparative genetic analysis performed in the region between the csgD-csgB genes showed a high degree of similarity in all Salmonella members, with the exception of S. bongori strains. This is an indication that changes in the csgD-csgB intermediate region are caused by natural mutations caused by genetic drift. These mutations are observed more frequently in strains adapted to laboratory conditions and as a result of possible mutational effects, “rdar” morphotype is lost. This change can be seen as a result of passage of Salmonella strains in rich nutrient media and laboratory conditions for long generations and the “rdar” morphotype can be lost. In wild type strains, these mutational changes are seen less frequently .
There is a strong relationship between activation of csgD and STM2123 and STM3388 (proteins containing complex GGDEF / EAL domain, respectively) proteins. STM2123 is a component needed for activation of csgD at the first step of biofilm formation. STM3388 protein, on the other hand, was found to have contributed positively to the formation of the biofilm since the stage when the biofilm began to mature. Proteins containing four other important EAL domains found in S. Typhimurium (STM1703, STM1827, STM3611 and STM4264) show similar activity in the expression of csgD. In some studies with the mutants of these proteins, a significant increase was also detected in the expression of csgD due to the increase in c-di-GMP at the cellular level was determined. In this context, the view has arisen that cellular c-di-GMP levels can control different targets in regulation of these proteins and biofilm formation .
These data are emphasizes that c-di-GMP plays an important role in virulence and mobility in biofilm formation due to its role in curli fimbria and cellulose biosynthesis via csgD .
BarA / SirA and Csr system
The BarA / SirA system is a widely conserved system in gamma-proteobacteria . SirA is a response regulator that is a member of the FixJ family proteins. BarA, on the other hand, act as a sensor kinase specific to SirA. It is known that bile salts and short chain fatty acids in the environment affect the BarA / SirA system in Salmonella. The SirA protein has also been found to be responsible for the transcriptional activation of csrB and csrC sRNAs, which are regulators of Salmonella invasion. This indicates that sirA controls host cell invasion of Salmonella [26–28].
In the study carried out by Teplitski et al. ; it was determined that sirA, fimI, csrB and csrC binary mutants could not perform biofilm formation on plastic surfaces. On the other hand flhDC mutants could form much more biofilm. In this study, the regulatory roles of SirA at the transcriptional level and the posttranscriptional level of the Csr system on the expressions of flagellar or type I fimbrial components that positively or negatively contribute to biofilm formation were clarified. Phosphorylated SirA-P activates csrB and csrC, fim operon and hilA at the transcriptional level. Increased csrB / csrC level inhibits CsrA activity. Reduced CsrA activity promotes biofilm formation by causing a decrease in expressions of factors that can inhibit biofilm formation, such as FlhDC and HilA proteins. CsrA also reduces film expression. The decrease in the activity of CsrA allows for more type I fimbria biosynthesis to be realized in this context and to have more biofilm production.
PhoPQ and RstA
Salmonella PhoPQ system is a binary system consisting of the cytoplasmic response regulator PhoP and the sensor kinase PhoQ localized in the inner membrane . As a result of PhoP activation, LPS modification is controlled by direct or indirect expression of more than 120 genes associated with many functions such as magnesium transport, invasion of epithelium cells and survival within macrophages [29, 30]. It is known that the phoP mutant strains of S. Typhimurium produce better biofilm compared to wild type strains. This mutation is also capable of increasing biofilm production on glass slides. These data clearly show that the PhoPQ system suppresses biofilm formation in S. Typhimurium. It was also that prgH may be associated with PhoPQ dependent biofilm regulation and determined that mutant Salmonella strains in terms of prgH gene could not form mature biofilms on gallstones and glass surfaces .
Another factor contributing to PhoPQ dependent biofilm regulation is the indirect regulation of RpoS by the PhoPQ system. As mentioned before, besides biofilm formation RpoS also regulates the synthesis of CsgD and mobility-related elements at the transcriptional level. PhoP can stabilize RpoS by acting as a transcriptional activator of iraP. iraP provides stabilization of RpoS by encoding a product that interacts with RssB . PhoP also activates RstA’s expression . This protein indirectly induces the breakdown of RpoS by the ClpXP-SsrB proteolytic pathway. RstA is the response regulator of the RstA / RstB binary system. The opposite effects of IraP and RstA play an active role in regulating RpoS’s expression based on extracellular signals. Activation of RstA by PhoP may offer other alternatives to PhoPQ dependent biofilm regulation. Unlike its effects on RpoS, RstA also affects the expression of bapA. High expression of RstA in E. coli leads to negative regulation by connecting RstA to the csgD promoter . The presence of RstA’s binding motif in the csgD operon in Salmonella proves that RstA directly inhibits the expression of csgD .
The interaction of cells in the biofilm structures through signal molecules
Biofilm forming is not a random event where bacteria only get together, attach to significant surface then adhere there and maintain their lives together with the other species on that surface. Many organisms give signals to each other to coordinate their activities, use little signal molecules. With the process called quorum sensing (QS) which is an important mechanism in biofilm forming, bacteria can measure the signal molecule density they produce, sense the amount of other microorganisms around them and enable to transfer this data to other bacteria . In another words with QS, bacteria determine the bacterial population in their environment. As increasing the amount of bacteria attaching to the surface, this signal’s local concentration increase and with this increase, a number of processes direct begining of biofilm forming. So, bacteria in the structure of biofilm contact to each other through the low molecular weighted messengers. QS also has some important regulative roles at synthesizing antibiotic, virulence factor formation, reproducing, spore forming, cell separation and pathogen bacterial infections . This mechanism which provides cellular interaction is regulated by auto-inducer (AI) molecules .
The reason why QS molecules are expressed as auto-inducer since they show regulative effect on the cell metabolism where they are produced . Some microorganisms use more than one different QS molecule. QS takes place in two ways as between species and inner species. Gram negative bacteria use N-acyl homoserine lactone (AHL, AHLs, acyl-HSL or HSL), Gram positive bacteria mostly use oligo-peptides as an auto-inducer in QS mechanism . Beside this, the usage characteristics of auto-inducer signal molecules in QS system of Gram negative and positive bacteria are mutual. In the studies conducted on QS systems it was determined that S. enterica has actualized the cellular interaction through auto-inducer signals .
Besides the formation of single and multi-species biofilm structures; symbiosis also plays an important role in the control of other social / physiological behaviors such as the formation of spore, bacteriocin production, genetic competence, programmed cell death, and virulence . This intracellular communication process was first described in the marine bacteria Vibrio fischeri, which produces bioluminescence. In this system, bacteria communicate by producing, detecting, and responding to small diffusable signal molecules called autoinducers. The bacterial QS system is generally divided into three types: 1) The LuxI / LuxR system in which Gram-negative bacteria use acyl homoserine lactones (AHL) as signal molecules 2) Two-component-oligopeptide system at which Gram-positive bacteria use small peptides as oligopeptide signaling molecules and 3) Autoinducer-2 (AI-2) system, encoded by luxS, common in both Gram-negative and Gram-positive bacteria. Each signal system type is detected and responded by the correct sensing element and regulatory control [41, 42].
Small RNAs (sRNA) are non-coding RNA molecules produced by bacteria that can be 50 to 250 nucleotides in length. Different studies have found that biofilm formation is influenced by the production of sRNA molecules in various S. enterica serovar Typhimurium mutants . The sRNA is encoded in the same region as the QS syntase (LuxS). MicA is a family of highly preserved small RNA molecules in some Enterobacteriaceae members. It has been determined that members of this small RNA family are a regulatory mechanism for biofilm formation in many bacterial species and play a critical role in the development of mature Salmonella biofilms by adjusting the level of balanced expression . To date, at least six sRNAs (arcZ, sroC, csrB, dsrA, oxyS, and rprA) associated with biofilm formation in Salmonella and its closely related bacteria have been identified. These can be divided into two groups as positively regulating biofilm formation and negatively regulating biofilm formation. arcZ, sroC and csrB are sRNAs that positively regulate biofilm formation and were observed to be significantly down-regulated in anaerobiosis. However, in microaerobiosis, no significant difference of these three sRNAs was observed. Additionally, dsrA, oxyS and rprA are sRNAs that negatively regulate biofilm formation. These three exhibited differences in transcription patterns, both based on atmospheric oxygen level and culture medium [43, 45, 46].
The function of sRNAs in regulating biofilm formation occurs through two general mechanisms: sRNAs that act via base pairing with other RNAs and protein binding. Protein binding sRNAs mimic the protein binding sequences found in various mRNAs, antagonizing and separating their cognate regulatory proteins. Base pairing sRNAs are categorized as cis or trans in their position within the bacterial genome relative to their mRNA targets. The sRNAs that are copied from the DNA strand directly opposite the mRNA targets are called cis-encoded sRNAs. cis-encoded sRNAs generally add extensive complementarity to their targets. In contrast, trans-coded sRNAs reside elsewhere on the genome, function as transduced molecules and add only limited (10–25 bp) complementarity to base pairing interactions [43, 47, 48].
dam and seqA
DNA methylation status in specific GATC sequences in promoters of some genes besides the dnaA gene can activate or suppress transcription by affecting the binding of RNA polymerases or transcription factors [49–51]. It has been determined that the SeqA protein regulates the transcription of some genes in bacteria, just like the Dam methylase enzyme. It performs this function through a GATC methylation or by acting as a co-activator . It has been found that Dam and SeqA activity is involved in the regulation of different genes in Salmonella, and in mutants of the dam and seqA genes, attachment to host cells and especially host cell invasion is significantly reduced [53–57]. However, few studies have been conducted describing the effect of Dam methylation on biofilm formation in Salmonella [58, 59]. Aya Castaneda et al. (58) found that DNA methylation in S. Enteritidis increased the expression of biofilm production factors such as cellulose and pleated fimbria by modifying csgD expression. However, only at one study it was found that seqA genes are not effective in biofilm formation .
Uğur et al.  found that the biofilm forming ability on steel and polystyrene surfaces in dam gene mutants of different Salmonella serovars significantly decreased compared to wild type strains. When the dam gene is cloned into a pBAD24 vector containing a promoter induced in the presence of arabinose, recovery of the biofilm-forming ability to the same mutants gives certainty to the findings of the dam mutation. On the other hand, for the first time in this study, it was determined that the SeqA protein played a role in the regulation of biofilm formation in Salmonella serovars. The same results were obtained when the verification tests of biofilm formation on steel and polystyrene surfaces were performed with seqA mutants using the pBAD24 vector mentioned above. In the light of these findings, it has been suggested that the dam and seqA genes carry out their biofilm regulation activities by changing the activities of RNA polymerase or transcription factors in the promoter regions. Studies carried out in wild strain S. Typhimurium 14028 and its dam and seqA mutants have proven that these genes are effective in the regulation of many genes related to biofilm formation, virulence and motility (Akçelik, M. unpublished data)
The MarT protein, a close homologue of the ToxR-like regulatory protein family, was first identified by Tükel et al.  as a positive regulator of the misL autotransporter protein in S. Typhimurium. Later as a result of microarray studies conducted by Akkoç et al. , using S. Typhimurium 14028 wild type strain and marT mutant, it was determined that the gene in question could be a positive regulator of many properties related to bacterial physiology. In the latest sudy, Eran et al.  determined that the marT gene is a positive regulator of 14 genes in Salmonella, called fimA, fimD, fimF, fimH, stjB, stjC, csgA, csgD, ompC, sthB, sthE, rmbA, fliZ and yaiC. As a result of QRT-PCR studies, it has also been proven that the protein encoded by the marT gene is an autoregulator that positively regulates its own promoter. All these data indicate that the MarT protein not only regulates misL gene expression but also acts as a global regulator in Salmonella. When the participation of these genes subjected to marT gene regulation to biofilm formation on polystyrene surfaces was examined, it was determined that the biofilm production capacity in mutant strains for each gene was statistically significantly decreased (p = 0.05). These results showed that all genes tested were associated with biofilm production.
Biofilms are the main cause of persistent contaminations, which evoke serious economic losses and hygienic problems in the food industry and medicine. Improperly cleaned food production surfaces contribute to biofilm formation for different food spoilage bacteria and food-borne pathogens such as Salmonella, possessing high adhesive characteristics for biotic and abiotic materials. Detached cells from biofilms, yielding by the effects of the aerosols from contaminated equipments and products flow from contaminated surfaces, create cross contamination. Thus, development of effective strategies to prevent biofilm formation and to eradicate mature biofilm forms from food producing environments are crucial for food industry and human health. Understanding the molecular patterns of biofilm formation and determining the biofilm behavior under different environmental conditions and disinfection applications, are necessary to developt these effective antibiofilm strategies.
Nadell C.D., Xavier J.B., Foster K.R.: The sociobiology of biofilms. FEMS Microbiol. Rev, 33, 206–224 (2009)NadellC.D.XavierJ.B.FosterK.R.The sociobiology of biofilms33206224200910.1111/j.1574-6976.2008.00150.x19067751Search in Google Scholar
Flemming H.C., Wingender J.: The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633 (2010)FlemmingH.C.WingenderJ.The biofilm matrix8623633201010.1038/nrmicro241520676145Search in Google Scholar
Burmolle M, Webb J.S, Rao D., Hansen L.H., Sorensen S.J., Kjelleberg S.: Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl. Environ. Microbiol. 72, 3916–3923 (2006)BurmolleMWebbJ.SRaoD.HansenL.H.SorensenS.J.KjellebergS.Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms7239163923200610.1128/AEM.03022-05148963016751497Search in Google Scholar
Ren D., Madsen J.S., Sorensen S.J., Burmolle M.: High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. ISME J. 9, 81–89 (2015)RenD.MadsenJ.S.SorensenS.J.BurmolleM.High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation98189201510.1038/ismej.2014.96427443324936766Search in Google Scholar
Fiegna F., Moreno-Letelier A., Bell T., Barraclough T.G.: Evolution of species interactions determines microbial community productivity in new environments, ISME J. 9, 1235–1245 (2015)FiegnaF.Moreno-LetelierA.BellT.BarracloughT.G.Evolution of species interactions determines microbial community productivity in new environments912351245201510.1038/ismej.2014.215440916625387206Search in Google Scholar
Fujishige N.A., Kapadia N.N., Hirsch A.M.: A feeling for the microorganism: structure on a small scale. Biofilms on plant roots. Bot. J. Linnean Soc. 150, 79–88 (2006)FujishigeN.A.KapadiaN.N.HirschA.M.A feeling for the microorganism: structure on a small scale. Biofilms on plant roots1507988200610.1111/j.1095-8339.2006.00492.xSearch in Google Scholar
Kim S. J., Chang J., Rimal B., Yang H., Schaefer J.: Surface proteins and the formation of biofilms by Staphylococcus aureus. Biochim. Biophys. Acta Biomembr. 1860, 749–756 (2018)KimS. J.ChangJ.RimalB.YangH.SchaeferJ.Surface proteins and the formation of biofilms by Staphylococcus aureus1860749756201810.1016/j.bbamem.2017.12.003578020029229527Search in Google Scholar
Rinaudi L.V., Giordano W. An integrated view of biofilm formation in rhizobia. FEMS Microbiol Lett. 304, 1–11 (2010)RinaudiL.V.GiordanoW.An integrated view of biofilm formation in rhizobia304111201010.1111/j.1574-6968.2009.01840.x19930462Search in Google Scholar
Armbruster C.R., Parsek M.R.: New insight into the early stages of biofilm formation. Proc. Natl. Acad. Sci. USA, 115, 4317–4319 (2018)ArmbrusterC.R.ParsekM.R.New insight into the early stages of biofilm formation11543174319201810.1073/pnas.1804084115592493929632199Search in Google Scholar
Prouty A.M., Gunn J.S.: Comparative analysis of Salmonella enterica serovar Typhimurium biofilm formation on gallstones and on glass. Infect. Immun. 71, 7154–7158 (2003)ProutyA.M.GunnJ.S.Comparative analysis of Salmonella enterica serovar Typhimurium biofilm formation on gallstones and on glass7171547158200310.1128/IAI.71.12.7154-7158.200330889414638807Search in Google Scholar
Ledeboer N.A., Jones, B.D.: Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar typhimurium on HEp-2 cells and chicken intestinal epithelium. J. Bacteriol. 187: 3214–3226 (2005)LedeboerN.A.JonesB.D.Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar typhimurium on HEp-2 cells and chicken intestinal epithelium18732143226200510.1128/JB.187.9.3214-3226.2005108282415838049Search in Google Scholar
Olsen A., Arnqvist A., Hammar M., Normark S.: Environmental regulation of curli production in Escherichia coli. Infect. Agents Dis. 2, 272–274 (1993)OlsenA.ArnqvistA.HammarM.NormarkS.Environmental regulation of curli production in Escherichia coli22722741993Search in Google Scholar
Vidal O., Longin R., Prigent-Combaret C., Dorel C., Hooreman M., Lejeune, P.: Isolation of an Escherichia coli K12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J. Bacteriol. 180, 2442–2449 (1998)VidalO.LonginR.Prigent-CombaretC.DorelC.HooremanM.LejeuneP.Isolation of an Escherichia coli K12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression18024422449199810.1128/JB.180.9.2442-2449.19981071879573197Search in Google Scholar
Romling U., Bokranz W., Rabsch W., Zogaj X., Nimtz M., Tschape H.: Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease. Int. J. Med. Microbiol. 293, 273–285 (2002)RomlingU.BokranzW.RabschW.ZogajX.NimtzM.TschapeH.Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease293273285200210.1078/1438-4221-0026814503792Search in Google Scholar
Prigent-Combaret C., Brombacher E., Vidal O., Ambert A., Lejeune P., Landini P., Dorel C.: Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J. Bacteriol. 183, 7213–7223 (2001)Prigent-CombaretC.BrombacherE.VidalO.AmbertA.LejeuneP.LandiniP.DorelC.Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene18372137223200110.1128/JB.183.24.7213-7223.20019557111717281Search in Google Scholar
Cookson A.L., Cooley W.A., Woodward M.J.: The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence to abiotic surfaces. Int. J. Med. Microbiol. 292, 195–205 (200).CooksonA.L.CooleyW.A.WoodwardM.J.The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence to abiotic surfaces29219520520010.1078/1438-4221-0020312398210Search in Google Scholar
Monteiro C., Fang X., Ahmad I., Gonelsky M., Römling U.: Regulation of biofilm components in Salmonella enterica serovar Typhimurium by lytic transglycosylases involved in cell wall turnover. J. Bacteriol. 193, 6443–6451 (2011)MonteiroC.FangX.AhmadI.GonelskyM.RömlingU.Regulation of biofilm components in Salmonella enterica serovar Typhimurium by lytic transglycosylases involved in cell wall turnover19364436451201110.1128/JB.00425-11323290621965572Search in Google Scholar
Collinson S.K., Clouthier S.C., Doran J. L., Banser P.A., Kay W.W.: Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae. J. Bacteriol. 178, 662–667 (1996)CollinsonS.K.ClouthierS.C.DoranJ. L.BanserP.A.KayW.W.Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae178662667199610.1128/jb.178.3.662-667.19961777098550497Search in Google Scholar
Zogaj X., Nimtz M., Rohde M., Bokranz W., Romling U.: The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39, 1452–1463 (2001)ZogajX.NimtzM.RohdeM.BokranzW.RomlingU.The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix3914521463200110.1046/j.1365-2958.2001.02337.x11260463Search in Google Scholar
Solano C., Garcia B., Valle J., Berasain C., Ghigo J.M., Gamazo C. Genetic analysis of Salmonella Enteritidis biofilm formation: Critical role of cellulose. Mol. Microbiol. 43, 793–808 (2002)SolanoC.GarciaB.ValleJ.BerasainC.GhigoJ.M.GamazoC.Genetic analysis of Salmonella Enteritidis biofilm formation: Critical role of cellulose43793808200210.1046/j.1365-2958.2002.02802.x11929533Search in Google Scholar
Römling, U.: Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell. Mol. Life Sci. 62, 1234–1246 (2005)RömlingU.Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae6212341246200510.1007/s00018-005-4557-x15818467Search in Google Scholar
Zakikhany K., Harrington C.R., Nimtz M., Hinton J.C.D., Romling U.: Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 77, 771–786 (2010)ZakikhanyK.HarringtonC.R.NimtzM.HintonJ.C.D.RomlingU.Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium77771786201010.1111/j.1365-2958.2010.07247.x20545866Search in Google Scholar
Simm R., Morr M., Kader A., Nimtz M., Romling U.: GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol. 53, 1123–1134 (2004)SimmR.MorrM.KaderA.NimtzM.RomlingU.GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility5311231134200410.1111/j.1365-2958.2004.04206.x15306016Search in Google Scholar
Davidson C.J., White A.P., Surette, M.G.: Evolutionary loss of the rdar morphotype in Salmonella as a result of high mutation rates during laboratory passage. The ISME Journal, 2, 293–307 (2008)DavidsonC.J.WhiteA.P.SuretteM.G.Evolutionary loss of the rdar morphotype in Salmonella as a result of high mutation rates during laboratory passage2293307200810.1038/ismej.2008.418256702Search in Google Scholar
Teplitski M., Al-Agely A., Ahmer B.M.: Contribution of the sirA regulon to biofilm formation in Salmonella enterica serovar Typhimurium. Microbiology, 152, 3411–3424 (2006)TeplitskiM.Al-AgelyA.AhmerB.M.Contribution of the sirA regulon to biofilm formation in Salmonella enterica serovar Typhimurium15234113424200610.1099/mic.0.29118-017074910Search in Google Scholar
Altier C., Suyemoto, M., Ruiz A.I., Burnham K.D., Maurer R.: Characterization of two novel regulatory genes affecting Salmonella invasion gene expression. Mol. Microbiol. 35, 635–646 (2000)AltierC.SuyemotoM.RuizA.I.BurnhamK.D.MaurerR.Characterization of two novel regulatory genes affecting Salmonella invasion gene expression35635646200010.1046/j.1365-2958.2000.01734.x10672185Search in Google Scholar
Pernestig A.K., Melefors O., Georgellis D.: Identification of UvrY as the cognate response regulator for the BarA sensor kinase in Escherichia coli. J. Biol. Chem. 276, 225–231 (2001)PernestigA.K.MeleforsO.GeorgellisD.Identification of UvrY as the cognate response regulator for the BarA sensor kinase in Escherichia coli276225231200110.1074/jbc.M00155020011022030Search in Google Scholar
Lawhon S.D., Maurer R., Suyemoto M. Altier C.: Intestinal short-chain fatty acids alter Salmonella Typhimurium invasion gene expression and virulence through BarA/SirA. Mol. Microbiol. 46, 1451–1464 (2002)LawhonS.D.MaurerR.SuyemotoM.AltierC.Intestinal short-chain fatty acids alter Salmonella Typhimurium invasion gene expression and virulence through BarA/SirA4614511464200210.1046/j.1365-2958.2002.03268.x12453229Search in Google Scholar
Kato A., Groisman E.A.: The PhoQ/PhoP regulatory network of Salmonella enterica. Adv. Exp. Med. Biol. 631, 7–21 (2008)KatoA.GroismanE.A.The PhoQ/PhoP regulatory network of Salmonella enterica631721200810.1007/978-0-387-78885-2_218792679Search in Google Scholar
Charles R.C., Harris J.B., Chase M.R., Lebrun L.M., Sheikh A., LaRocque R.C.: Comparative proteomic analysis of the PhoP regulon in Salmonella enterica serovar Typhi versus Typhimurium. PLoS ONE, 4, e6994 (2009)CharlesR.C.HarrisJ.B.ChaseM.R.LebrunL.M.SheikhA.LaRocqueR.C.Comparative proteomic analysis of the PhoP regulon in Salmonella enterica serovar Typhi versus Typhimurium4e6994200910.1371/journal.pone.0006994273661919746165Search in Google Scholar
Tu X., Latifi T., Bougdour A., Gottesman S., Groisman E.A.: The PhoP/PhoQ two-component system stabilizes the alternative sigma factor RpoS in Salmonella enterica. PNAS, 103, 13503–13508 (2006)TuX.LatifiT.BougdourA.GottesmanS.GroismanE.A.The PhoP/PhoQ two-component system stabilizes the alternative sigma factor RpoS in Salmonella enterica1031350313508200610.1073/pnas.0606026103155738516938894Search in Google Scholar
Choi E., Groisman E.A., Shin D.: Activated by different signals, the PhoP/PhoQ two-component system differentially regulates metal uptake. J. Bacteriol. 191, 7174–7181 (2009)ChoiE.GroismanE.A.ShinD.Activated by different signals, the PhoP/PhoQ two-component system differentially regulates metal uptake19171747181200910.1128/JB.00958-09278656419801407Search in Google Scholar
Cabeza M.L., Aguirre A., Soncini F.C., Vescovi E.G.: Induction of RpoS degradation by the two-component system regulator RstA in Salmonella enterica. J. Bacteriol. 189, 7335–7342 (2007)CabezaM.L.AguirreA.SonciniF.C.VescoviE.G.Induction of RpoS degradation by the two-component system regulator RstA in Salmonella enterica18973357342200710.1128/JB.00801-07216845317704217Search in Google Scholar
Ogasawara H., Hasegawa A., Kanda E., Miki T., Yamamoto K., Ishihama A.: Genomic SELEX search for target promoters under the control of the PhoQP-RstBA signal relay cascade. J. Bacteriol. 189, 4791–4799 (2007)OgasawaraH.HasegawaA.KandaE.MikiT.YamamotoK.IshihamaA.Genomic SELEX search for target promoters under the control of the PhoQP-RstBA signal relay cascade18947914799200710.1128/JB.00319-07191343017468243Search in Google Scholar
Camara M., Williams P., Winzer K., Chan W.C.: Look who’s talking: communication and quorum sensing in the bacterial world. Philos. T. R. Soc. Biol. Sci. 362, 1119–1134 (2007)CamaraM.WilliamsP.WinzerK.ChanW.C.Look who’s talking: communication and quorum sensing in the bacterial world36211191134200710.1098/rstb.2007.2039243557717360280Search in Google Scholar
March J. C., Bentley WE.: Quorum sensing and bacterial cross-talk in biotechology. Curr. Opin. Biotechnol. 15, 495–502 (2004)MarchJ. C.BentleyWE.Quorum sensing and bacterial cross-talk in biotechology15495502200410.1016/j.copbio.2004.08.01315464383Search in Google Scholar
Asad S., Opal S.M.: Bench-to-bedside review: Quorum sensing and the role of cell-to-cell communication during invasive bacterial infection. Crit Care. 12, 236–242 (2008)AsadS.OpalS.M.Bench-to-bedside review: Quorum sensing and the role of cell-to-cell communication during invasive bacterial infection12236242200810.1186/cc7101264634019040778Search in Google Scholar
Donabedian H.: Quorum sensing and its relevance to infectious diseases. J Infect. 46, 207–214 (2003)DonabedianH.Quorum sensing and its relevance to infectious diseases46207214200310.1053/jinf.2002.112012799145Search in Google Scholar
Wong C.S., Koh C., Sam C., Chen J.W., Chong Y.M., Yin W., Chan K.: Degradation of bacterial quorum sensing signaling molecules by the microscopic yeast Trichosporon loubieri isolated from tropical wetland waters. Sensors, 13, 12943–12957 (2013)WongC.S.KohC.SamC.ChenJ.W.ChongY.M.YinW.ChanK.Degradation of bacterial quorum sensing signaling molecules by the microscopic yeast Trichosporon loubieri isolated from tropical wetland waters131294312957201310.3390/s131012943385904324072030Search in Google Scholar
Parsek M.R., Greenberg E.P.: Sociomicrobiology: The connections between quorum sensing and biofilms, Trends Microbiol. 13, 27–33 (2005)ParsekM.R.GreenbergE.P.Sociomicrobiology: The connections between quorum sensing and biofilms132733200510.1016/j.tim.2004.11.00715639629Search in Google Scholar
Federle M.J., Bassler B.L.: Interspecies communication in bacteria. J. Clin. Invest. 112, 1291–1299 (2003)FederleM.J.BasslerB.L.Interspecies communication in bacteria11212911299200310.1172/JCI2019522848314597753Search in Google Scholar
Flemming H.C., Wingender J., Szewzyk U., Steinberg P., Rice S.A., Kjelleberg S.: Biofilms: An emergent form of bacterial life. Nat. Rev. Microbiol. 14, 563–575 (2016)FlemmingH.C.WingenderJ.SzewzykU.SteinbergP.RiceS.A.KjellebergS.Biofilms: An emergent form of bacterial life14563575201610.1038/nrmicro.2016.9427510863Search in Google Scholar
Jennings M.E., Quick L.N., Soni A., Davis R.R., Crosby K., Ott C.M., Nickerson C.A., Wilson J.W.: Characterization of the Salmonella enterica serovar Typhimurium ydcI gene, which encodes a conserved DNA binding protein required for full acid stress resistance. J. Bacteriol. 193, 2208–2217 (2011)JenningsM.E.QuickL.N.SoniA.DavisR.R.CrosbyK.OttC.M.NickersonC.A.WilsonJ.W.Characterization of the Salmonella enterica serovar Typhimurium ydcI gene, which encodes a conserved DNA binding protein required for full acid stress resistance19322082217201110.1128/JB.01335-10313308921398541Search in Google Scholar
Sheffield C.L., Crippen T.L., Andrews K., Bongaerts R.J., Nisbet D.J.: Planktonic and biofilm communities from 7-day-old chicken cecal microflora cultures: characterization and resistance to Salmonella colonization. J. Food Protect. 72, 1812–1820 (2009)SheffieldC.L.CrippenT.L.AndrewsK.BongaertsR.J.NisbetD.J.Planktonic and biofilm communities from 7-day-old chicken cecal microflora cultures: characterization and resistance to Salmonella colonization7218121820200910.4315/0362-028X-72.9.181219777880Search in Google Scholar
Chambers J. R., Sauer K.: Small RNAs and their role in biofilm formation. Trends Microbiol. 21, 39–49 (2013)ChambersJ. R.SauerK.Small RNAs and their role in biofilm formation213949201310.1016/j.tim.2012.10.008375238623178000Search in Google Scholar
Lamas A., Regal P., Vázquez B., Miranda J.M., Cepeda A., Franco C.M.: Influence of milk, chicken residues and oxygen levels on biofilm formation on stainless steel, gene expression and small RNAs in Salmonella enterica. Food Control, 90, 1–9 (2018)LamasA.RegalP.VázquezB.MirandaJ.M.CepedaA.FrancoC.M.Influence of milk, chicken residues and oxygen levels on biofilm formation on stainless steel, gene expression and small RNAs in Salmonella enterica9019201810.1016/j.foodcont.2018.02.023Search in Google Scholar
Bak G., Lee J., Suk S., Kim D., Young Lee J., Kim K., Lee Y.: Identification of novel sRNAs involved in biofilm formation, motility and fimbriae formation in Escherichia coli. Sci. Rep. 5, 15287–15306 (2015)BakG.LeeJ.SukS.KimD.Young LeeJ.KimK.LeeY.Identification of novel sRNAs involved in biofilm formation, motility and fimbriae formation in Escherichia coli51528715306201510.1038/srep15287460681326469694Search in Google Scholar
Zhou Y., Smith D.R., Hufnagel D.A., Chapman M.R.: Experimental manipulation of the microbial functional amyloid called curli. Methods Mol. Biol. 966, 53–75 (2013)ZhouY.SmithD.R.HufnagelD.A.ChapmanM.R.Experimental manipulation of the microbial functional amyloid called curli9665375201310.1007/978-1-62703-245-2_4377321223299728Search in Google Scholar
Polaczek P., Kwan K., Campbell J.L.: GATC motifs may alter the conformation of DNA depending on sequence context and N6-adenine methylation status: possible implications for DNA-protein recognition. Mol. Gen. 258, 488–493 (1998)PolaczekP.KwanK.CampbellJ.L.GATC motifs may alter the conformation of DNA depending on sequence context and N6-adenine methylation status: possible implications for DNA-protein recognition258488493199810.1007/s0043800507599669330Search in Google Scholar
Oshima T.C., Wada Y., Kawagoe T., Ara M., Maeda Y., Masuda S., Hiraga H.: Genome-wide analysis of deoxyadenosine methyltransferase-mediated control of gene expression in Escherichia coli. Mol. Microbiol. 45, 673–695 (2002)OshimaT.C.WadaY.KawagoeT.AraM.MaedaY.MasudaS.HiragaH.Genome-wide analysis of deoxyadenosine methyltransferase-mediated control of gene expression in Escherichia coli45673695200210.1046/j.1365-2958.2002.03037.x12139615Search in Google Scholar
Robbins-Manke J.L., Zdraveski Z.Z., Marinus M., Essigman J.M.: Analysis of global gene expression and double-strand-break formation in DNA adenine methyltransferase- and mismatch repair-deficient Escherichia coli. J. Bacteriol. 187, 7027–7037 (2005)Robbins-MankeJ.L.ZdraveskiZ.Z.MarinusM.EssigmanJ.M.Analysis of global gene expression and double-strand-break formation in DNA adenine methyltransferase- and mismatch repair-deficient Escherichia coli18770277037200510.1128/JB.187.20.7027-7037.2005125162816199573Search in Google Scholar
Prieto A. I., Jakomin M., Segura I., Pucciarelli M. G., Ramos-Morales F., del Portillo F.G., Casadesus J.: The GATC-binding protein SeqA is required for bile resistance and virulence in Salmonella enterica Serovar Typhimurium. J. Bacteriol. 189, 8496–8502 (2007)PrietoA. I.JakominM.SeguraI.PucciarelliM. G.Ramos-MoralesF.del PortilloF.G.CasadesusJ.The GATC-binding protein SeqA is required for bile resistance and virulence in Salmonella enterica Serovar Typhimurium18984968502200710.1128/JB.01156-07216893617905993Search in Google Scholar
García-del-Portillo F., Pucciarelli M. G., Casadesús J.: DNA adenine methylase mutants of Salmonella Typhimurium are deficient in protein secretion, cell invasion and M cell cytotoxicity. PNAS, 96, 11584–11588 (1999)García-del-PortilloF.PucciarelliM. G.CasadesúsJ.DNA adenine methylase mutants of Salmonella Typhimurium are deficient in protein secretion, cell invasion and M cell cytotoxicity961158411588199910.1073/pnas.96.20.115781807610500219Search in Google Scholar
Heithoff D.M., Sinsheimer R.L., Low D.A., Mahan M.J.: An essential role for DNA adenine methylation in bacterial virulence. Science, 284, 967–970 (1999)HeithoffD.M.SinsheimerR.L.LowD.A.MahanM.J.An essential role for DNA adenine methylation in bacterial virulence284967970199910.1126/science.284.5416.96710320378Search in Google Scholar
Chatti A., Daghfous D., Landoulsi A.: Effect of seqA mutation on Salmonella typhimurium virulence. J. Infect. 54, 241–245 (2007)ChattiA.DaghfousD.LandoulsiA.Effect of seqA mutation on Salmonella typhimurium virulence54241245200710.1016/j.jinf.2007.01.00217327135Search in Google Scholar
Chatti A., Aloui M., Tagourti J., Mihoub M., Landoulsi A.: Novobiocin sensitivity of Salmonella typhimurium dam and/or seqA mutants. Pol. J. Microbiol. 63, 51–56 (2014)ChattiA.AlouiM.TagourtiJ.MihoubM.LandoulsiA.Novobiocin sensitivity of Salmonella typhimurium dam and/or seqA mutants635156201410.33073/pjm-2014-007Search in Google Scholar
Jakomin M., Chessa D., Baumler A.J., Casadesus J.: Regulation of the Salmonella enterica std fimbrial operon by DNA adenine methylation, SeqA, and HdfR. J. Bacteriol. 190, 7406–7413 (2008)JakominM.ChessaD.BaumlerA.J.CasadesusJ.Regulation of the Salmonella enterica std fimbrial operon by DNA adenine methylation, SeqA, and HdfR19074067413200810.1128/JB.01136-08257664818805972Search in Google Scholar
Aya Castaneda M.R., Sarnacki S.H., Noto L.M.: Dam methylation is required for efficient biofilm production in Salmonella enterica serovar Enteritidis. Int. J. Food Microbiol. 16, 15–22 (2015)Aya CastanedaM.R.SarnackiS.H.NotoL.M.Dam methylation is required for efficient biofilm production in Salmonella enterica serovar Enteritidis161522201510.1016/j.ijfoodmicro.2014.10.00325462918Search in Google Scholar
Uğur S., Akçelik M., Yüksel F.N., Karatuğ N.T., Akçelik M.: Effects of dam and seqA genes on biofilm and pellicle formation in Salmonella. Pat. Glob. Health, 112, 368–377 (2018)UğurS.AkçelikM.YükselF.N.KaratuğN.T.AkçelikM.Effects of dam and seqA genes on biofilm and pellicle formation in Salmonella112368377201810.1080/20477724.2018.1539803630073730433856Search in Google Scholar
Tükel Ç, Akçelik M., de Jong M.F., Şimşek Ö., Tsolis R.M., Baumler A.J.: MarT activates expression of the MisL autotransporter protein of Salmonella enterica serotype Typhimurium. J Bacteriol. 189, 3922–3926 (2007)TükelÇAkçelikM.de JongM.F.ŞimşekÖ.TsolisR.M.BaumlerA.J.MarT activates expression of the MisL autotransporter protein of Salmonella enterica serotype Typhimurium18939223926200710.1128/JB.01746-06191333717351045Search in Google Scholar
İlçe B.Y., Akçelik N.: The effect of marT gene on biofilm production of Salmonella Typhimurium. Turk. J. of Biol. 39, 722–731.İlçeB.Y.AkçelikN.The effect of marT gene on biofilm production of Salmonella Typhimurium3972273110.3906/biy-1501-25Search in Google Scholar
Eran Z., Akçelik M., Özcengiz G., Akçelik N.: Regulation of biofilm formation by marT in Salmonella Typhimurium. Mol. Biol. Rep. 47, 5041–5050 (2020)EranZ.AkçelikM.ÖzcengizG.AkçelikN.Regulation of biofilm formation by marT in Salmonella Typhimurium4750415050202010.1007/s11033-020-05573-632529277Search in Google Scholar