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Giardia duodenalis induces pathogenic dysbiosis of human intestinal microbiota biofilms

Beatty, Jennifer K., Akierman, Sarah V., Motta, Jean-Paul, Muise, Stacy, Workentine, Matthew L., Harrison, Joe J., Bhargava, Amol, Beck, Paul L., Rioux, Kevin P., McKnight, Gordon Webb, Wallace, John L., Buret, Andre G.·2017·International Journal for Parasitology
DOI 10.1016/j.ijpara.2016.11.010
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Image 1
CC-BY-NC-ND · From the PDF
Fig. 1 Outline of experimental procedure. Human mucosal biopsies were collected from healthy donors (see Section 2.2), and mucosal bacteria were isolated and seeded into the Calgary Biofilm Device. Microbiota biofilms were cultivated on the Calgary Biofilm Device for 72 h and exposed to live Giardia duodenalis , spent medium, or control conditions for 24 h. Following exposure, biofilms were processed for microscopic analysis, intestinal epithelial monolayer challenge, or inoculation into germ-free C57BL/6 mice. Multiple aliquots of three biopsies, from a total of six donors, were used to seed biofilms used for all experiments.
Fig. 1 Outline of experimental procedure. Human mucosal biopsies were collected from healthy donors (see Section 2.2), and mucosal bacteria were isolated and seeded into the Calgary Biofilm Device. Microbiota biofilms were cultivated on the Calgary Biofilm Device for 72 h and exposed to live Giardia duodenalis , spent medium, or control conditions for 24 h. Following exposure, biofilms were processed for microscopic analysis, intestinal epithelial monolayer challenge, or inoculation into germ-free C57BL/6 mice. Multiple aliquots of three biopsies, from a total of six donors, were used to seed biofilms used for all experiments.CC-BY-NC-ND · From the PDF
log2 fold-change in Giardia relative to control
log2 fold-change in Giardia relative to controlCC-BY-NC-ND · From the PDF
Fig. 2 Community profiles of faecal microbiota of germ-free mice reconstituted with human microbiota biofilms; mice were given either untreated microbiota (Control), or microbiota challenged with Giardia duodenalis ( Giardia ). Germ-free C57Bl6 mice were administered two rounds of human microbiota biofilm communities exposed to G. duodenalis , or control medium containing no parisites, and were euthanised after 14 days ( n = 5 per group). Faecal samples were collected from each animal and analysed via 16S amplicon sequencing of the V3-V4 rRNA region. (A) Operational taxomomic units in faeces of mice either given untreated microbiota (Control), or microbiota challenged with G. duodenalis ( Giardia ). (B) Changes in operational taxomomic unit abundance by phylum in the same samples. (C) Non-metric multidimensional scaling ordination plot of b -diversity using the Bray-Curtis metric in the same samples. (D) a -Diversity of the same samples as assessed using the Shannon diversity index.
Fig. 2 Community profiles of faecal microbiota of germ-free mice reconstituted with human microbiota biofilms; mice were given either untreated microbiota (Control), or microbiota challenged with Giardia duodenalis ( Giardia ). Germ-free C57Bl6 mice were administered two rounds of human microbiota biofilm communities exposed to G. duodenalis , or control medium containing no parisites, and were euthanised after 14 days ( n = 5 per group). Faecal samples were collected from each animal and analysed via 16S amplicon sequencing of the V3-V4 rRNA region. (A) Operational taxomomic units in faeces of mice either given untreated microbiota (Control), or microbiota challenged with G. duodenalis ( Giardia ). (B) Changes in operational taxomomic unit abundance by phylum in the same samples. (C) Non-metric multidimensional scaling ordination plot of b -diversity using the Bray-Curtis metric in the same samples. (D) a -Diversity of the same samples as assessed using the Shannon diversity index.CC-BY-NC-ND · From the PDF
Fig. 3 Giardia -exposed microbiota biofilm communities promote B cell-containing lymphocyte follicles in the colonic epithelium of reconstituted germ-free mice. Sections of colon tissue from reconstituted germ-free C57Bl/6 mice. Animals were given intercolonic administration of two rounds of human microbiota biofilm communities exposed, or not, to Giardia and were euthanised after 14 days ( n = 5-10 per group). Representative pictures of colon tissue stained with H&E from mice receiving either control biofilms CoMBBF (A), or those exposed to Giardia GMBBF (B). The average number (C) and average size (D) (recorded blindly) of colonic lymphocyte follicles per microscopic field (200X) in groups of mice receiving control microbiota biofilms (CoMBBF), and mice receiving Giardia -exposed microbiota biofilms (GMBBF) (  four different fields were analysed per animal. True germ-free animals were neither exposed to CoMBBF nor GMBBF, but represented a measure of baseline colonisation following transfer from germfree facilities to the environment where experimentation took place. (E) Immunohistochemistry was performed on colonic sections of reconstituted germ-free mice. Representative images of animals receiving Giardia -exposed microbiota biofilms are presented as stained for T and B cell phenotypes. Host nuclei were coloured in blue (DAPI), Thy-1.2 (CD90-pan T cell marker), and CD45r-positive cells in red (rat polyclonal anti-CD45R coupled with alexa455). Lymphocyte aggregates were negative for Thy1.2 (CD90-pan T cell marker) staining. Negative control staining used rat IgG coupled with the same fluorochrome. Scale bars represent 50 m mfor E and represent the limit of intraepithelial lymphocyte follicles ( n  4 different fields were analysed per animal). / P < 0.05, // P < 0.01 (ANOVA and Tukey's multiple comparison test for data in C and D).
Fig. 3 Giardia -exposed microbiota biofilm communities promote B cell-containing lymphocyte follicles in the colonic epithelium of reconstituted germ-free mice. Sections of colon tissue from reconstituted germ-free C57Bl/6 mice. Animals were given intercolonic administration of two rounds of human microbiota biofilm communities exposed, or not, to Giardia and were euthanised after 14 days ( n = 5-10 per group). Representative pictures of colon tissue stained with H&E from mice receiving either control biofilms CoMBBF (A), or those exposed to Giardia GMBBF (B). The average number (C) and average size (D) (recorded blindly) of colonic lymphocyte follicles per microscopic field (200X) in groups of mice receiving control microbiota biofilms (CoMBBF), and mice receiving Giardia -exposed microbiota biofilms (GMBBF) (  four different fields were analysed per animal. True germ-free animals were neither exposed to CoMBBF nor GMBBF, but represented a measure of baseline colonisation following transfer from germfree facilities to the environment where experimentation took place. (E) Immunohistochemistry was performed on colonic sections of reconstituted germ-free mice. Representative images of animals receiving Giardia -exposed microbiota biofilms are presented as stained for T and B cell phenotypes. Host nuclei were coloured in blue (DAPI), Thy-1.2 (CD90-pan T cell marker), and CD45r-positive cells in red (rat polyclonal anti-CD45R coupled with alexa455). Lymphocyte aggregates were negative for Thy1.2 (CD90-pan T cell marker) staining. Negative control staining used rat IgG coupled with the same fluorochrome. Scale bars represent 50 m mfor E and represent the limit of intraepithelial lymphocyte follicles ( n  4 different fields were analysed per animal). / P < 0.05, // P < 0.01 (ANOVA and Tukey's multiple comparison test for data in C and D).CC-BY-NC-ND · From the PDF
Fig. 4 Germ-free mice receiving Giardia -exposed microbiota biofilm communities (GMBBF) show increased colonic IL-1 b protein levels. Animals were given intracolonic administration of two rounds of human microbiota biofilm communities exposed, or not, to Giardia and were euthanised after 14 days ( n = 4-5 per group). Protein expression of IL-1 b was measured in colonic segments collected from germ-free C57Bl/6 mice reconstituted with differential microbiota biofilm communities using the multiplex technology of the Eve Technologies Luminex platform. Mice receiving Giardia -exposed microbiota biofilm communities exhibited greater expression of IL-1 b compared with those receiving control microbiota biofilms (CoMBBF). * P < 0.05 (Student's t -test).
Fig. 4 Germ-free mice receiving Giardia -exposed microbiota biofilm communities (GMBBF) show increased colonic IL-1 b protein levels. Animals were given intracolonic administration of two rounds of human microbiota biofilm communities exposed, or not, to Giardia and were euthanised after 14 days ( n = 4-5 per group). Protein expression of IL-1 b was measured in colonic segments collected from germ-free C57Bl/6 mice reconstituted with differential microbiota biofilm communities using the multiplex technology of the Eve Technologies Luminex platform. Mice receiving Giardia -exposed microbiota biofilm communities exhibited greater expression of IL-1 b compared with those receiving control microbiota biofilms (CoMBBF). * P < 0.05 (Student's t -test).CC-BY-NC-ND · From the PDF
Image 7
CC-BY-NC-ND · From the PDF
Fig. 6 Planktonic bacteria from human microbiota biofilms exposed to Giardia spent medium promote heightened rates of epithelial apoptosis. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium) or exposure to Giardia spent medium. Caco-2 monolayers co-incubated, for 24 h, with planktonic constituents of microbiota biofilms exposed to Giardia spent medium (Caco-2 + Giardia MBBPlank) exhibited significantly higher rates of apoptosis compared with cells incubated with microbiota biofilm communities exposed to fresh sTSY (Caco-2 + Control MBBPlank). Caco-2 cells incubated with fresh cell medium served as baseline indicators of cell apoptosis. Values were calculated as absorbance ratios versus control: the mean of all control values was calculated and set at 1.0, and ratio changes were calculated for each measurement in each group against this calculated control mean. Values are mean ± S.E.M. n = 3/group. * P < 0.05 versus Caco-2 + Medium (ANOVA and Tukey's multiple comparison test).
Fig. 6 Planktonic bacteria from human microbiota biofilms exposed to Giardia spent medium promote heightened rates of epithelial apoptosis. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium) or exposure to Giardia spent medium. Caco-2 monolayers co-incubated, for 24 h, with planktonic constituents of microbiota biofilms exposed to Giardia spent medium (Caco-2 + Giardia MBBPlank) exhibited significantly higher rates of apoptosis compared with cells incubated with microbiota biofilm communities exposed to fresh sTSY (Caco-2 + Control MBBPlank). Caco-2 cells incubated with fresh cell medium served as baseline indicators of cell apoptosis. Values were calculated as absorbance ratios versus control: the mean of all control values was calculated and set at 1.0, and ratio changes were calculated for each measurement in each group against this calculated control mean. Values are mean ± S.E.M. n = 3/group. * P < 0.05 versus Caco-2 + Medium (ANOVA and Tukey's multiple comparison test).CC-BY-NC-ND · From the PDF
Fig. 7 Planktonic bacteria from human microbiota biofilms exposed to Giardia spent medium more readily translocate across epithelial monolayers. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium), or exposure to Giardia spent medium. Bacteria released from human microbiota biofilm communities exposed to Giardia spent medium translocate at significantly higher levels than those exposed to fresh sTSY (Control), and this effect was inhibited by pre-treatment with E-64 ( Giardia spent medium + E-64). DMSO pre-treatment served as the E-64 vehicle control. Values were calculated as log colony forming unit (CFU)/mL ratios versus Control CFU/mL, arbitrarily set to 1.0. Values are mean ± S.E.M. n = 3/group. * P < 0.05 versus Control (ANOVA and Tukey's multiple comparison test).
Fig. 7 Planktonic bacteria from human microbiota biofilms exposed to Giardia spent medium more readily translocate across epithelial monolayers. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium), or exposure to Giardia spent medium. Bacteria released from human microbiota biofilm communities exposed to Giardia spent medium translocate at significantly higher levels than those exposed to fresh sTSY (Control), and this effect was inhibited by pre-treatment with E-64 ( Giardia spent medium + E-64). DMSO pre-treatment served as the E-64 vehicle control. Values were calculated as log colony forming unit (CFU)/mL ratios versus Control CFU/mL, arbitrarily set to 1.0. Values are mean ± S.E.M. n = 3/group. * P < 0.05 versus Control (ANOVA and Tukey's multiple comparison test).CC-BY-NC-ND · From the PDF
Fig. 8 Planktonic bacteria from human microbiota biofilms exposed to Giardia spent medium reduce zonula occludens (ZO)-1 protein and modify ZO-1 distribution in Caco-2 epithelial monolayers. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium), or exposure to Giardia spent medium. Cell monolayers were challenged with planktonic constituents released from microbiota biofilms, either exposed to Giardia spent medium or fresh sTSY (Control) in the presence/absence of broad-spectrum, E-64, pre-treatment on trophozoites, for 24 h, and immunoblotted for ZO-1 (A). Western blots (densitometry and representative blots images) illustrate that Caco-2 monolayers co-incubated with planktonic constituents released from Giardia spent medium- exposed microbiota biofilm communities contain significantly decreased ZO-1 protein levels. Pre-treatment of trophozoites with E-64 inhibited this decrease. (B) Representative immunostaining for ZO-1 (red) reveals a mislocalization, and loss in stain intensity in Caco-2 monolayers co-incubated with planktonic constituents released from microbiota biofilm communities modified by exposure to Giardia spent medium. Densitometry data are presented as % glyceraldehyde 3 phosphate dehydrogenase. Values were calculated as % glyceraldehyde 3 phosphate dehydrogenase ratios versus control, arbitrarily set to 1.0 (A). Values are mean ± S.E.M. n = 3/group. * P < 0.05 versus Control (ANOVA and Tukey's multiple comparison test).
Fig. 8 Planktonic bacteria from human microbiota biofilms exposed to Giardia spent medium reduce zonula occludens (ZO)-1 protein and modify ZO-1 distribution in Caco-2 epithelial monolayers. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium), or exposure to Giardia spent medium. Cell monolayers were challenged with planktonic constituents released from microbiota biofilms, either exposed to Giardia spent medium or fresh sTSY (Control) in the presence/absence of broad-spectrum, E-64, pre-treatment on trophozoites, for 24 h, and immunoblotted for ZO-1 (A). Western blots (densitometry and representative blots images) illustrate that Caco-2 monolayers co-incubated with planktonic constituents released from Giardia spent medium- exposed microbiota biofilm communities contain significantly decreased ZO-1 protein levels. Pre-treatment of trophozoites with E-64 inhibited this decrease. (B) Representative immunostaining for ZO-1 (red) reveals a mislocalization, and loss in stain intensity in Caco-2 monolayers co-incubated with planktonic constituents released from microbiota biofilm communities modified by exposure to Giardia spent medium. Densitometry data are presented as % glyceraldehyde 3 phosphate dehydrogenase. Values were calculated as % glyceraldehyde 3 phosphate dehydrogenase ratios versus control, arbitrarily set to 1.0 (A). Values are mean ± S.E.M. n = 3/group. * P < 0.05 versus Control (ANOVA and Tukey's multiple comparison test).CC-BY-NC-ND · From the PDF
Image 11
CC-BY-NC-ND · From the PDF
Fig. 9 Planktonic bacteria from human microbiota biofilms exposed to Giardia spent medium increase Toll-like receptor 4 expression in Caco-2 monolayers. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium), and either control conditions (Control MBBPlank whereby no exposure to Giardia occured; or fresh sTSY medium), or exposure to Giardia spent medium (where trophozoites had been pre-treated with cysteine protease inhibitor E-64 or not), or exposure to the known pro-inflammatory cytokine IL1 beta. Data were also obtained from plain, untreated, CaCo-2 monolayers (Caco-2). (A) Caco-2 monolayers co-incubated with planktonic constituents released from human microbiota biofilms exposed to Giardia spent medium show a significant increase in TLR4 protein levels. Pre-treatment of trophozoites with E-64 prevented this increase of TLR4 protein levels in the monolayers. Densitometry data are presented as % glyceraldehyde 3 phosphate dehydrogenase. Values were calculated as % glyceraldehyde 3 phosphate dehydrogenase ratios versus control, arbitrarily set to 1.0. Values are mean ± S.E.M. n = 3/group. * P < 0.05 versus Control (ANOVA and Tukey's multiple comparison test). Numbers were representative of separate experiments conducted with microbiota biofilm cultures cultivated from colonic samples of multiple patients in order to ensure reproducibility. (B) Caco-2 monolayers co-incubated with planktonic constituents released from human microbiota biofilms exposed to Giardia spent medium show a significant increase in secreted CXCL-8. To further identify the mechanisms of epithelial pathophysiology induced by enteropathogen-modified MBBFs, we assessed the consequences of exposure to Giardia -modified microbiota constituents on the production of pro-inflammatory CXCL-8. Pre-treatment of trophozoites with E-64 inhibited this increase. Values were calculated as % control arbitrarily set to 1.0. Values are mean ± S.E.M. n = 3/group. / P < 0.05 versus Control (ANOVA and Tukey's multiple comparison test).
Fig. 9 Planktonic bacteria from human microbiota biofilms exposed to Giardia spent medium increase Toll-like receptor 4 expression in Caco-2 monolayers. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium), and either control conditions (Control MBBPlank whereby no exposure to Giardia occured; or fresh sTSY medium), or exposure to Giardia spent medium (where trophozoites had been pre-treated with cysteine protease inhibitor E-64 or not), or exposure to the known pro-inflammatory cytokine IL1 beta. Data were also obtained from plain, untreated, CaCo-2 monolayers (Caco-2). (A) Caco-2 monolayers co-incubated with planktonic constituents released from human microbiota biofilms exposed to Giardia spent medium show a significant increase in TLR4 protein levels. Pre-treatment of trophozoites with E-64 prevented this increase of TLR4 protein levels in the monolayers. Densitometry data are presented as % glyceraldehyde 3 phosphate dehydrogenase. Values were calculated as % glyceraldehyde 3 phosphate dehydrogenase ratios versus control, arbitrarily set to 1.0. Values are mean ± S.E.M. n = 3/group. * P < 0.05 versus Control (ANOVA and Tukey's multiple comparison test). Numbers were representative of separate experiments conducted with microbiota biofilm cultures cultivated from colonic samples of multiple patients in order to ensure reproducibility. (B) Caco-2 monolayers co-incubated with planktonic constituents released from human microbiota biofilms exposed to Giardia spent medium show a significant increase in secreted CXCL-8. To further identify the mechanisms of epithelial pathophysiology induced by enteropathogen-modified MBBFs, we assessed the consequences of exposure to Giardia -modified microbiota constituents on the production of pro-inflammatory CXCL-8. Pre-treatment of trophozoites with E-64 inhibited this increase. Values were calculated as % control arbitrarily set to 1.0. Values are mean ± S.E.M. n = 3/group. / P < 0.05 versus Control (ANOVA and Tukey's multiple comparison test).CC-BY-NC-ND · From the PDF
Fig. 10 Giardia spent medium-exposed microbiota biofilms planktonic constituents (MBBPlank) promote increased CXCL-8 protein levels secreted from Caco-2 monolayers. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium), or exposure to Giardia spent medium. Caco-2 monolayers co-incubated with planktonic constituents released from Giardia spent medium-exposed microbiota biofilm communities showed a significant increase in secreted CXCL-8. Pre-treatment of trophozoites with cysteine protease inhibitor E-64 prevented increased secreted CXCL-8 levels in stimulated Caco-2 monolayers challenged with planktonic microbial constituents released from microbiota biofilms. Values were calculated as % control, arbitrarily set to 1.0. Values are mean ± S.E.M. n = 3/group. * P < 0.05, ** P < 0.01 versus Control (ANOVA and Tukey's multiple comparison test). Cells given IL-1 beta served as a positive ''pro-inflammatory'' control.
Fig. 10 Giardia spent medium-exposed microbiota biofilms planktonic constituents (MBBPlank) promote increased CXCL-8 protein levels secreted from Caco-2 monolayers. Human microbiota biofilm communities were cultivated on the Calgary Biofilm Device using colonic biopsies collected from healthy human donors. Following a 72 h growth period, microbiota biofilms were subjected to either control conditions (fresh sTSY medium), or exposure to Giardia spent medium. Caco-2 monolayers co-incubated with planktonic constituents released from Giardia spent medium-exposed microbiota biofilm communities showed a significant increase in secreted CXCL-8. Pre-treatment of trophozoites with cysteine protease inhibitor E-64 prevented increased secreted CXCL-8 levels in stimulated Caco-2 monolayers challenged with planktonic microbial constituents released from microbiota biofilms. Values were calculated as % control, arbitrarily set to 1.0. Values are mean ± S.E.M. n = 3/group. * P < 0.05, ** P < 0.01 versus Control (ANOVA and Tukey's multiple comparison test). Cells given IL-1 beta served as a positive ''pro-inflammatory'' control.CC-BY-NC-ND · From the PDF

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Metadata

Authors
Beatty, J. K., Akierman, S. V., Motta, J.-P., Muise, S., Workentine, M. L., Harrison, J. J., Bhargava, A., Beck, P. L., Rioux, K. P., McKnight, G. W., Wallace, J. L., & Buret, A. G.
Venue
International Journal for Parasitology
Publisher
Elsevier BV
Published
2017-05
Volume
47
Issue
6
Pages
311-326
ISSN
0020-7519
DOI
10.1016/j.ijpara.2016.11.010
Cited by
157
References
8
Language
en
Licence

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CoChat. (2026). Citation check: Giardia duodenalis induces pathogenic dysbiosis of human intestinal microbiota biofilms. https://app.cochat.ai/papers/10.1016/j.ijpara.2016.11.010
The paper
Beatty, J. K., Akierman, S. V., Motta, J.-P., Muise, S., Workentine, M. L., Harrison, J. J., Bhargava, A., Beck, P. L., Rioux, K. P., McKnight, G. W., Wallace, J. L., & Buret, A. G. (2017). Giardia duodenalis induces pathogenic dysbiosis of human intestinal microbiota biofilms. International Journal for Parasitology. https://doi.org/10.1016/j.ijpara.2016.11.010