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Biofilm spatial organization by the emerging pathogen Campylobacter jejuni: comparison between NCTC 11168 and 81-176 strains under microaerobic and oxygen-enriched conditions.

Turonova H, Briandet R, Rodrigues R, Hernould M, Hayek N, Stintzi A, Pazlarova J, Tresse O - Front Microbiol (2015)

Bottom Line: Acclimation of cells to oxygen-enriched conditions led to significant enhancement of biofilm formation during the early stages of the process.Exposure to these conditions during biofilm cultivation induced an even greater biofilm development for both strains, indicating that oxygen demand for biofilm formation is higher than for planktonic growth counterparts.These findings constitute a clear example of a survival strategy used by this emerging human pathogen.

View Article: PubMed Central - PubMed

Affiliation: SECALIM UMR1014, Institut National de la Recherche Agronomique Nantes, France ; LUNAM Université, Oniris, Université de Nantes Nantes, France ; Department of Biochemistry and Microbiology, Faculty of Food and Biochemical Technology, University of Chemistry and Technology Prague, Czech Republic.

ABSTRACT
During the last years, Campylobacter has emerged as the leading cause of bacterial foodborne infections in developed countries. Described as an obligate microaerophile, Campylobacter has puzzled scientists by surviving a wide range of environmental oxidative stresses on foods farm to retail, and thereafter intestinal transit and oxidative damage from macrophages to cause human infection. In this study, confocal laser scanning microscopy (CLSM) was used to explore the biofilm development of two well-described Campylobacter jejuni strains (NCTC 11168 and 81-176) prior to or during cultivation under oxygen-enriched conditions. Quantitative and qualitative appraisal indicated that C. jejuni formed finger-like biofilm structures with an open ultrastructure for 81-176 and a multilayer-like structure for NCTC 11168 under microaerobic conditions (MAC). The presence of motile cells within the biofilm confirmed the maturation of the C. jejuni 81-176 biofilm. Acclimation of cells to oxygen-enriched conditions led to significant enhancement of biofilm formation during the early stages of the process. Exposure to these conditions during biofilm cultivation induced an even greater biofilm development for both strains, indicating that oxygen demand for biofilm formation is higher than for planktonic growth counterparts. Overexpression of cosR in the poorer biofilm-forming strain, NCTC 11168, enhanced biofilm development dramatically by promoting an open ultrastructure similar to that observed for 81-176. Consequently, the regulator CosR is likely to be a key protein in the maturation of C. jejuni biofilm, although it is not linked to oxygen stimulation. These unexpected data advocate challenging studies by reconsidering the paradigm of fastidious requirements for C. jejuni growth when various subpopulations (from quiescent to motile cells) coexist in biofilms. These findings constitute a clear example of a survival strategy used by this emerging human pathogen.

No MeSH data available.


Related in: MedlinePlus

Oxygen-enriched conditions enhanced biofilm development prior to and during biofilm formation ofC. jejuni. Fold changes (FC) of biofilm development of C. jejuni strains NCTC 11168 (black bars) and 81-176 (white bars) as expressed by maximum height and biomass volume. (A) FC representing biofilm formation of cells acclimatized to OEC (OECa: 19% O2, 10% CO2, 71% N2) and to MAC (MACa: 5% O2, 10% CO2, 85% N2) prior to biofilm formation in MAC. (B) FC of biofilm development of cells submitted to OEC (OECc) during biofilm cultivation and cells submitted to OEC (OECa) prior to biofilm cultivation in MAC. Statistical data are presented in Supplementary Tables 2, 3.
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Figure 3: Oxygen-enriched conditions enhanced biofilm development prior to and during biofilm formation ofC. jejuni. Fold changes (FC) of biofilm development of C. jejuni strains NCTC 11168 (black bars) and 81-176 (white bars) as expressed by maximum height and biomass volume. (A) FC representing biofilm formation of cells acclimatized to OEC (OECa: 19% O2, 10% CO2, 71% N2) and to MAC (MACa: 5% O2, 10% CO2, 85% N2) prior to biofilm formation in MAC. (B) FC of biofilm development of cells submitted to OEC (OECc) during biofilm cultivation and cells submitted to OEC (OECa) prior to biofilm cultivation in MAC. Statistical data are presented in Supplementary Tables 2, 3.

Mentions: In the second approach, both strains were acclimatized to OEC (OECa) prior to biofilm formation in MAC. Acclimatized cells of both strains formed significantly larger biofilms than non-acclimatized ones after 24 h of cultivation, as expressed by the fold changes in maximum height and biomass volume values (Figure 3A). Conversely, the acclimatization of cells to OEC was no longer an advantage for biofilm formation after 48 h, as demonstrated by reduction of biofilm formation for both strains. This was also confirmed by statistical analyses, with the highest F-ratios of the interaction effect between “Incubation time” and “O2 pretreatment,” showing higher variation in maximum height and biomass volume, than for the other factors (Supplementary Table 2).


Biofilm spatial organization by the emerging pathogen Campylobacter jejuni: comparison between NCTC 11168 and 81-176 strains under microaerobic and oxygen-enriched conditions.

Turonova H, Briandet R, Rodrigues R, Hernould M, Hayek N, Stintzi A, Pazlarova J, Tresse O - Front Microbiol (2015)

Oxygen-enriched conditions enhanced biofilm development prior to and during biofilm formation ofC. jejuni. Fold changes (FC) of biofilm development of C. jejuni strains NCTC 11168 (black bars) and 81-176 (white bars) as expressed by maximum height and biomass volume. (A) FC representing biofilm formation of cells acclimatized to OEC (OECa: 19% O2, 10% CO2, 71% N2) and to MAC (MACa: 5% O2, 10% CO2, 85% N2) prior to biofilm formation in MAC. (B) FC of biofilm development of cells submitted to OEC (OECc) during biofilm cultivation and cells submitted to OEC (OECa) prior to biofilm cultivation in MAC. Statistical data are presented in Supplementary Tables 2, 3.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4499754&req=5

Figure 3: Oxygen-enriched conditions enhanced biofilm development prior to and during biofilm formation ofC. jejuni. Fold changes (FC) of biofilm development of C. jejuni strains NCTC 11168 (black bars) and 81-176 (white bars) as expressed by maximum height and biomass volume. (A) FC representing biofilm formation of cells acclimatized to OEC (OECa: 19% O2, 10% CO2, 71% N2) and to MAC (MACa: 5% O2, 10% CO2, 85% N2) prior to biofilm formation in MAC. (B) FC of biofilm development of cells submitted to OEC (OECc) during biofilm cultivation and cells submitted to OEC (OECa) prior to biofilm cultivation in MAC. Statistical data are presented in Supplementary Tables 2, 3.
Mentions: In the second approach, both strains were acclimatized to OEC (OECa) prior to biofilm formation in MAC. Acclimatized cells of both strains formed significantly larger biofilms than non-acclimatized ones after 24 h of cultivation, as expressed by the fold changes in maximum height and biomass volume values (Figure 3A). Conversely, the acclimatization of cells to OEC was no longer an advantage for biofilm formation after 48 h, as demonstrated by reduction of biofilm formation for both strains. This was also confirmed by statistical analyses, with the highest F-ratios of the interaction effect between “Incubation time” and “O2 pretreatment,” showing higher variation in maximum height and biomass volume, than for the other factors (Supplementary Table 2).

Bottom Line: Acclimation of cells to oxygen-enriched conditions led to significant enhancement of biofilm formation during the early stages of the process.Exposure to these conditions during biofilm cultivation induced an even greater biofilm development for both strains, indicating that oxygen demand for biofilm formation is higher than for planktonic growth counterparts.These findings constitute a clear example of a survival strategy used by this emerging human pathogen.

View Article: PubMed Central - PubMed

Affiliation: SECALIM UMR1014, Institut National de la Recherche Agronomique Nantes, France ; LUNAM Université, Oniris, Université de Nantes Nantes, France ; Department of Biochemistry and Microbiology, Faculty of Food and Biochemical Technology, University of Chemistry and Technology Prague, Czech Republic.

ABSTRACT
During the last years, Campylobacter has emerged as the leading cause of bacterial foodborne infections in developed countries. Described as an obligate microaerophile, Campylobacter has puzzled scientists by surviving a wide range of environmental oxidative stresses on foods farm to retail, and thereafter intestinal transit and oxidative damage from macrophages to cause human infection. In this study, confocal laser scanning microscopy (CLSM) was used to explore the biofilm development of two well-described Campylobacter jejuni strains (NCTC 11168 and 81-176) prior to or during cultivation under oxygen-enriched conditions. Quantitative and qualitative appraisal indicated that C. jejuni formed finger-like biofilm structures with an open ultrastructure for 81-176 and a multilayer-like structure for NCTC 11168 under microaerobic conditions (MAC). The presence of motile cells within the biofilm confirmed the maturation of the C. jejuni 81-176 biofilm. Acclimation of cells to oxygen-enriched conditions led to significant enhancement of biofilm formation during the early stages of the process. Exposure to these conditions during biofilm cultivation induced an even greater biofilm development for both strains, indicating that oxygen demand for biofilm formation is higher than for planktonic growth counterparts. Overexpression of cosR in the poorer biofilm-forming strain, NCTC 11168, enhanced biofilm development dramatically by promoting an open ultrastructure similar to that observed for 81-176. Consequently, the regulator CosR is likely to be a key protein in the maturation of C. jejuni biofilm, although it is not linked to oxygen stimulation. These unexpected data advocate challenging studies by reconsidering the paradigm of fastidious requirements for C. jejuni growth when various subpopulations (from quiescent to motile cells) coexist in biofilms. These findings constitute a clear example of a survival strategy used by this emerging human pathogen.

No MeSH data available.


Related in: MedlinePlus