Pellicle formation in Shewanella oneidensis

Liang, Yili; Gao, Haichun; Chen, Jingrong; Dong, Yangyang; Wu, Lin; He, Zhili; Liu, Xueduan; Qiu, Guanzhou; Zhou, Jizhong

doi:10.1186/1471-2180-10-291

Cited by 58 publications

(75 citation statements)

References 59 publications

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“…Results showed that the EPS profiles of these two strains were virtually identical, eliminating the possibility. Notably, in agreement with the previous finding by Liang et al (44), D-glucose and D-mannose were the major monosaccharide units of EPS in S. oneidensis. These data collectively suggest that the rugose morphotype of fliF1 is due to a mechanism other than increased production of EPS.…”

Section: Resultssupporting

confidence: 82%

Exoprotein Production Correlates with Morphotype Changes of Nonmotile Shewanella oneidensis Mutants

Shi

Xia

et al. 2013

J Bacteriol

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We report a previously undescribed mechanism for the rugose morphotype in Shewanella oneidensis, a research model for investigating redox transformations of environmental contaminants. Bacteria may form smooth or rugose colonies on agar plates. In general, conversion from the smooth to rugose colony morphotype is attributed to increased production of exopolysaccharide (EPS). In this work, we discovered that aflagellate S. oneidensis mutants grew into rugose colonies, whereas those with nonfunctional flagellar filaments remained smooth. EPS production was not altered in either case, but mutants with the rugose morphotype showed significantly reduced exoprotein secretion. The idea that exoproteins at a reduced level correlate with rugosity gained support from smooth suppressor strains of an aflagellate rugose fliD (encoding the capping protein) mutant, which restored the exoprotein level to the levels of the wild-type and mutant strains with a smooth morphotype. Further analyses revealed that SO1072 (a putative GlcNAc-binding protein) was one of the highly upregulated exoproteins in these suppressor strains. Most intriguingly, this study identified a compensatory mechanism of SO1072 to flagellins possibly mediated by bis-(3=-5=)-cyclic dimeric GMP. Bacteria live in environments abundant with various disturbances. To elevate their ability to persist and survive, bacterial cells often form large assemblages (in multicellularity), which are advantageous in comparison with single cells (1). In the laboratory, the most common multicellular form is colonies resulting from growing populations on top of an agar surface. Depending on the strain and the surrounding conditions, the morphology of colonies (morphotype) varies substantially (2, 3). Colony morphotypes of well-studied bacteria, including Vibrio cholerae, Pseudomonas aeruginosa, Salmonella enterica serovar Typhimurium, Escherichia coli, and Bacillus subtilis, are either smooth or rugose (also called wrinkling), in general (4-10). The rugosity promotes persistence under unfavorable conditions, such as conditions of exposure to toxins, UV light, osmotic and oxidative stresses, low pH, low temperatures, and starvation (5,8,(11)(12)(13), and enhances virulence and transmission, such as adherence and invasion of epithelial cells (7,14,15).It is now well acknowledged that in most bacteria the rugosity is due to overproduction of exopolysaccharide (EPS) (2, 4, 9). Diverse genetic screens for genes essential for the rugose phenotype have identified many genes required for EPS synthesis, such as bcsABZC in Acetobacter xylinus, S. enterica serovar Typhimurium, and E. coli (10), pel in P. aeruginosa (16), vps in V. cholerae (17, 18), and eps in B. subtilis, to name a few (19,20). Additionally, extracellular structures such as curli fibers and flagella have been found to be important in determination of colony morphotypes. In S. enterica serovar Typhimurium and E. coli, the rugose morphotype appears only when curli fibers are abundant due to overexpression of CsgD (curli fibe...

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Section: Resultssupporting

confidence: 82%

Exoprotein Production Correlates with Morphotype Changes of Nonmotile Shewanella oneidensis Mutants

Shi

Xia

et al. 2013

J Bacteriol

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“…The bpfA operon in Shewanella species such as S. oneidensis MR-1 and S. putrefaciens CN32 commonly contains seven genes, including a TISS for BpfA translocation. Disruption of the TISS blocks formation of pellicle, a type of biofilm formed at the air-liquid interface which is probably caused by interruption of BpfA translocation (21). A hyper-aggregating mutant of S. oneidensis MR-1 with enhanced biofilm formation exhibits increased transcription of a TISS component up to about 5-fold, and inactivation of the TISS results in the loss of the hyper-aggregation phenotype (22).…”

mentioning

confidence: 99%

FlrA Represses Transcription of the Biofilm-Associated bpfA Operon in Shewanella putrefaciens

Cheng

et al. 2017

Appl Environ Microbiol

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Manipulation of biofilm formation in Shewanella is beneficial for application to industrial and environmental biotechnology. BpfA is an adhesin largely responsible for biofilm formation in many Shewanella species. However, the mechanism underlying BpfA production and the resulting biofilm remains vaguely understood. We previously described the finding that BpfA expression is enhanced by DosD, an oxygen-stimulated diguanylate cyclase, under aerobic growth. In the present work, we identify FlrA as a critical transcription regulator of the bpfA operon in Shewanella putrefaciens CN32 by transposon mutagenesis. FlrA acted as a repressor of the operon promoter by binding to two boxes overlapping the Ϫ10 and Ϫ35 sites recognized by 70 . DosD regulation of the expression of the bpfA operon was mediated by FlrA, and cyclic diguanylic acid (c-di-GMP) abolished FlrA binding to the operon promoter. We also demonstrate that FlhG, an accessory protein for flagellum synthesis, antagonized FlrA repression of the expression of the bpfA operon. Collectively, this work demonstrates that FlrA acts as a central mediator in the signaling pathway from c-di-GMP to BpfA-associated biofilm formation in S. putrefaciens CN32.IMPORTANCE Motility and biofilm are mutually exclusive lifestyles, shifts between which are under the strict regulation of bacteria attempting to adapt to the fluctuation of diverse environmental conditions. The FlrA protein in many bacteria is known to control motility as a master regulator of flagellum synthesis. This work elucidates its effect on biofilm formation by controlling the expression of the adhesin BpfA in S. putrefaciens CN32 in response to c-di-GMP. Therefore, FlrA plays a dual role in controlling motility and biofilm formation in S. putrefaciens CN32. The cooccurrence of flrA, bpfA, and the FlrA box in the promoter region of the bpfA operon in diverse Shewanella strains suggests that bpfA is a common mechanism that controls biofilm formation in this bacterial species.KEYWORDS FlrA, Shewanella, biofilm, cyclic di-GMP, transcriptional factor B iofilm formed by bacteria is a multicell architecture for adaptation to diverse niches (1). Shewanella can form biofilm on a variety of surfaces, such as ferric oxides, electrodes, stainless steel, and glass (2-4). This genus is also renowned for an extracellular respiration ability to reduce iron oxide, electrodes, and other extracellular electron acceptors, including heavy metal ions. Such an ability has diverse potential applications in bioengineering and bioremediation (5). Biofilm formation in Shewanella benefits close contact with solid electron acceptors, thereby accelerating iron oxide reduction and improving current output, as well as inducing spatially stratified metabolic responses during contaminant exposure (4, 6, 7). Biofilm formed by Shewanella prevents microbially induced corrosion of steel and cast iron pipes (8, 9). On the other hand, biofilm formation of Shewanella also causes problems in some circumstances. For

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“…The beakers were kept still for pellicle formation at the room temperature. Cells in pellicle and underneath were separated based on published paper (Liang et al 2010). To quantify the pellicles formed by the S. oneidensis wild-type and mutant strains, cells from pellicles were collected, suspended in 30 ml fresh LB, violently vortexed, and applied to the spectrometer at 600 nm.…”

Section: Methodsmentioning

confidence: 99%

“…Three genes encoding TISS proteins were consistently up-regulated in pellicle cells. Our previous data showed that the pellicle was severely deWcient in the in-frame deletion mutant of aggA which blocked secretion via TISS (Liang et al 2010). Mutants carrying in-frame deletion in one of targeted genes were constructed.…”

Section: Mutational Analysis Of Candidate Genesmentioning

confidence: 99%

“…Because of the potential use of this organism for the bioremediation of metal/radionuclide contaminants in the environment, S. oneidensis MR-1 bioWlm has been extensively studied, including pellicle development (Bagge et al 2001;Vriendt et al 2005;Windt et al 2006;Teal et al 2006;Thormann et al 2004Thormann et al , 2005Liang et al 2010). In order to characterize features of the pellicle lifestyle, a microarray analysis on pellicle and planktonic cells of S. oneidensis was performed.…”

Section: Introductionmentioning

confidence: 99%

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Transcriptome analysis of pellicle formation of Shewanella oneidensis

et al. 2012

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Although the pellicle is one of the major growth modes of microorganisms, the metabolic features of pellicle cells and the determinative factors for pellicle formation are largely unknown. In recent years, biofilm development of Shewanella oneidensis, an important model organism for bioremediation studies, has been extensively studied. In this paper, a transcriptional profiling of pellicle cells relative to planktonic cells indicated that cells in pellicles were more metabolically active than the planktonic cells. Most notably, up-transcription of general secretion system proteins and iron/heme uptake and transport proteins was observed in pellicle cells. Unexpectedly, neither the hmuT nor hugA heme transport mutant exhibited a significant defect in pellicle formation. Expectedly, three type I secretion system mutants were severely deficient in pellicle formation, suggesting an essential role of these proteins.

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Pellicle formation in Shewanella oneidensis

Cited by 58 publications

References 59 publications

Exoprotein Production Correlates with Morphotype Changes of Nonmotile Shewanella oneidensis Mutants

Exoprotein Production Correlates with Morphotype Changes of Nonmotile Shewanella oneidensis Mutants

FlrA Represses Transcription of the Biofilm-Associated bpfA Operon in Shewanella putrefaciens

Transcriptome analysis of pellicle formation of Shewanella oneidensis

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