A Product of Heme Catabolism Modulates Bacterial Function and Survival
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{"title"=>"A Product of Heme Catabolism Modulates Bacterial Function and Survival", "type"=>"journal", "authors"=>[{"first_name"=>"Christopher L.", "last_name"=>"Nobles", "scopus_author_id"=>"48261544700"}, {"first_name"=>"Sabrina I.", "last_name"=>"Green", "scopus_author_id"=>"55894941400"}, {"first_name"=>"Anthony W.", "last_name"=>"Maresso", "scopus_author_id"=>"13613132300"}], "year"=>2013, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "pmid"=>"23935485", "pui"=>"369919450", "scopus"=>"2-s2.0-84884760554", "doi"=>"10.1371/journal.ppat.1003507", "sgr"=>"84884760554"}, "id"=>"f5e464b9-96c0-38ab-ba28-616b6c02269c", "abstract"=>"Bilirubin is the terminal metabolite in heme catabolism in mammals. After deposition into bile, bilirubin is released in large quantities into the mammalian gastrointestinal (GI) tract. We hypothesized that intestinal bilirubin may modulate the function of enteric bacteria. To test this hypothesis, we investigated the effect of bilirubin on two enteric pathogens; enterohemorrhagic E. coli (EHEC), a Gram-negative that causes life-threatening intestinal infections, and E. faecalis, a Gram-positive human commensal bacterium known to be an opportunistic pathogen with broad-spectrum antibiotic resistance. We demonstrate that bilirubin can protect EHEC from exogenous and host-generated reactive oxygen species (ROS) through the absorption of free radicals. In contrast, E. faecalis was highly susceptible to bilirubin, which causes significant membrane disruption and uncoupling of respiratory metabolism in this bacterium. Interestingly, similar results were observed for other Gram-positive bacteria, including B. cereus and S. aureus. A model is proposed whereby bilirubin places distinct selective pressure on enteric bacteria, with Gram-negative bacteria being protected from ROS (positive outcome) and Gram-positive bacteria being susceptible to membrane disruption (negative outcome). This work suggests bilirubin has differential but biologically relevant effects on bacteria and justifies additional efforts to determine the role of this neglected waste catabolite in disease processes, including animal models.", "link"=>"http://www.mendeley.com/research/product-heme-catabolism-modulates-bacterial-function-survival", "reader_count"=>36, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Ph. D. Student"=>15, "Other"=>1, "Student > Bachelor"=>3, "Professor"=>4, "Student > Postgraduate"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Ph. D. Student"=>15, "Other"=>1, "Student > Bachelor"=>3, "Professor"=>4, "Student > Postgraduate"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>21, "Medicine and Dentistry"=>5, "Chemistry"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>21}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}}, "reader_count_by_country"=>{"United States"=>3}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1131395"], "description"=>"<p>(A) Bacteria including EHEC (86-24), <i>E. faecalis</i>, <i>S. aureus</i>, and <i>B. cereus</i> were incubated with heme, biliverdin, bilirubin, and bilirubin ditaurate (0, 1, 5, 10, 20, 50, 75, 100, 250 and 500 µM for heme and bilirubin (B,C), or 500 µM for biliverdin and bilirubin ditaurate (A)) and membrane permeability monitored by propidium iodide fluorescence. (D) <i>E. faecalis</i> OG1RF was cultured to mid-log phase and exposed to bilirubin, alpha-tocopherol, and CCCP (each 100 µM). DiSC<sub>3</sub>(5) (1 µM final concentration), a fluorescent compound which increases in intensity when associated with polarized membranes, was supplemented into cultures before quantifying the fluorescence intensity at excitation 622 nm and emission 670 nm. Error bars represent ± one standard deviation, n = 3, and (*) denotes a significant (P≤0.05) difference while (**) denotes a non-significant difference (P>0.05) between treated samples and solvent-treated samples.</p>", "links"=>[], "tags"=>["microbiology", "Bacterial pathogens", "Gram positive", "Gram negative", "Emerging infectious diseases", "Host-pathogen interaction", "Microbial pathogens", "disruption"], "article_id"=>755369, "categories"=>["Biological Sciences"], "users"=>["Christopher L. Nobles", "Sabrina I. Green", "Anthony W. Maresso"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003507.g005", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Membrane_disruption_by_bilirubin_/755369", "title"=>"Membrane disruption by bilirubin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-25 02:44:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1131393"], "description"=>"<p>EHEC (86-24) was cultured with solvent (white), bilirubin (orange, 250 µM), biliverdin (green, 250 µM) or α-tocopherol (blue, 250 µM), in minimal media for 6 hours before addition to macrophages (J774A.1) at an MOI of approximately 3. (A) The amount of EHEC exposed to the macrophages is compared to the amount internalized by macrophages after 30 minutes. (B) The percentage of internalized EHEC over 2 hours was monitored for bacteria cultured with solvent (white diamonds, NaOH), bilirubin (orange squares), biliverdin (green circles) and α-tocopherol (blue triangles). Error bars represent ± one standard deviation, n = 3. Data are representative of a single experiment repeated three times with similar results and the (*) denotes a significant (P≤0.05) difference while (**) denotes a non-significant difference (P>0.05) between treated samples and solvent-treated samples.</p>", "links"=>[], "tags"=>["microbiology", "Bacterial pathogens", "Gram positive", "Gram negative", "Emerging infectious diseases", "Host-pathogen interaction", "Microbial pathogens", "protects", "ehec"], "article_id"=>755367, "categories"=>["Biological Sciences"], "users"=>["Christopher L. Nobles", "Sabrina I. Green", "Anthony W. Maresso"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003507.g003", "stats"=>{"downloads"=>2, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bilirubin_protects_EHEC_from_killing_by_J774A_1_macrophages_/755367", "title"=>"Bilirubin protects EHEC from killing by J774A.1 macrophages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-25 02:44:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1131394"], "description"=>"<p>(A) An equal number of CFUs of <i>E. faecalis</i> or <i>E. coli</i> (O157:H7 86-24) were mixed with increasing amounts of bilirubin (0, 100, 200, 300, 400, and 500 µM), biliverdin (500 µM), or α-tocopherol (500 µM), before spotting onto LB agar. Plates were grown at 37°C overnight. (B) Densitometry of bacterial lawns was measured using ImageJ software. (C) <i>E. faecalis</i> strains OG1RF (oral origin), X33 (fecal origin), UWH 1936 (blood origin), and NJ-3 (peritoneal fluid origin) were exposed to increasing concentrations of bilirubin (100, 200, or 300 µM) prior to spotting onto an LB-agar plate. Bacterial growth was captured by imaging the plates, and images were modified by adjusting brightness and contrast to best display colony formation (darker areas of image). (D) Growth of <i>E. faecalis</i> with bilirubin (yellow squares) or without bilirubin (white diamonds) was quantified by CFU plating. Bilirubin was titrated into <i>E. faecalis</i> cultures initially with bilirubin (red squares) and initially without bilirubin (orange squares) after 4 hours (marked by arrows). Error bars represent ± one standard deviation, n = 3, and (*) denotes a significant (P≤0.05) difference between treated samples and solvent-treated samples.</p>", "links"=>[], "tags"=>["microbiology", "Bacterial pathogens", "Gram positive", "Gram negative", "Emerging infectious diseases", "Host-pathogen interaction", "Microbial pathogens", "decreases", "viability"], "article_id"=>755368, "categories"=>["Biological Sciences"], "users"=>["Christopher L. Nobles", "Sabrina I. Green", "Anthony W. Maresso"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003507.g004", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bilirubin_decreases_the_viability_of_E_faecalis_/755368", "title"=>"Bilirubin decreases the viability of <i>E. faecalis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-25 02:44:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1131392"], "description"=>"<p>EHEC O157:H7 (EDL933) (A), EAEC O104:H4 (B), or <i>E. coli</i> BL21 (C) cultures were supplemented with plumbagin (50 µM, grey bars) or without plumbagin (white bars) in the presence or absence of bilirubin (BR), biliverdin (BV), or bilirubin ditaurate (BR<sub>dt</sub>). (D) Commensal <i>E. coli</i> strains CN-5 and CN-7 were supplemented with plumbagin (75 µM, grey bars) or without plumbagin (white bars) in the presence or absence of bilirubin (BR). (E) EHEC strain 86-24 was supplemented with Rose Bengal (750 µM, grey bars) or solvent (white bars) with or without bilirubin (200 or 500 µM) and exposed to fluorescent lighting or contained in a dark box for 12 to 14 hours. Terminal culture growth density was quantified by measuring the absorbance at 600 nm. Error bars represent ± one standard deviation, n = 3, and (*) denotes a significant (P≤0.05) difference while (**) denotes a non-significant difference (P>0.05) between treated samples and solvent-treated samples.</p>", "links"=>[], "tags"=>["microbiology", "Bacterial pathogens", "Gram positive", "Gram negative", "Emerging infectious diseases", "Host-pathogen interaction", "Microbial pathogens", "diminishes", "ros-induced"], "article_id"=>755366, "categories"=>["Biological Sciences"], "users"=>["Christopher L. Nobles", "Sabrina I. Green", "Anthony W. Maresso"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003507.g002", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bilirubin_diminishes_ROS_induced_growth_inhibition_/755366", "title"=>"Bilirubin diminishes ROS-induced growth inhibition.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-25 02:44:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1131397"], "description"=>"<p>Mid-log phase bacteria were exposed to 200 µM bilirubin and plated to determine CFUs. Fold reduction was calculated by the quantity of bacteria unexposed to bilirubin divided by the quantity present when exposed to bilirubin, n = 3.</p>", "links"=>[], "tags"=>["microbiology", "Bacterial pathogens", "Gram positive", "Gram negative", "Emerging infectious diseases", "Host-pathogen interaction", "Microbial pathogens", "viability", "exposed"], "article_id"=>755371, "categories"=>["Biological Sciences"], "users"=>["Christopher L. Nobles", "Sabrina I. Green", "Anthony W. Maresso"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003507.t001", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fold_reduction_in_viability_of_bacteria_exposed_to_bilirubin_/755371", "title"=>"Fold reduction in viability of bacteria exposed to bilirubin.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-07-25 02:44:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1131396"], "description"=>"<p>(A) <i>E. coli</i> (86-24), <i>E. faecalis</i>, <i>B. cereus</i>, and <i>S. aureus</i> were supplemented with resazurin and incubated with heme (50 µM), biliverdin (500 µM), bilirubin (50 µM), and bilirubin ditaurate (500 µM) for either 30 minutes or 2 hours. Unreduced resazurin was monitored by absorbance at 600 nm. (B) <i>E. faecalis</i> cultures were supplemented with resazurin and solvent (NaOH, Sol.), bilirubin (100 µM, BR), biliverdin (100 µM, BV), or TTF (1 mM, a known inhibitor of succinate dehydrogenase) while incubated in 1× PBS with 0.5% sucrose for 30 minutes at 37°C. (C) Similar to panel B, <i>E. faecalis</i> cultures were supplemented with resazurin and either superoxide dismutase (SOD, 1000 U/mL) or heat-inactivated superoxide dismutase (SODi, 1000 U/mL). (D) <i>E. faecalis</i> supplemented with resazurin and diluted into 1× PBS with 0.5% sucrose (+Suc.) or without sucrose (−Suc.) and incubated for 30 minutes at 37°C. (E) <i>E. faecalis</i> supplemented with resazurin and increasing amounts of bilirubin (1, 5, 10, 20, 30, 50, and 100 µM) in similar conditions as panels B and C. Error bars represent ± one standard deviation, n = 3, and the (*) denotes a significant (P≤0.05) difference while (**) denotes a non-significant difference (P>0.05) between treated samples and solvent-treated samples.</p>", "links"=>[], "tags"=>["microbiology", "Bacterial pathogens", "Gram positive", "Gram negative", "Emerging infectious diseases", "Host-pathogen interaction", "Microbial pathogens", "metabolism", "decreases"], "article_id"=>755370, "categories"=>["Biological Sciences"], "users"=>["Christopher L. Nobles", "Sabrina I. Green", "Anthony W. Maresso"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003507.g006", "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_E_faecalis_metabolism_decreases_after_exposure_to_bilirubin_/755370", "title"=>"<i>E. faecalis</i> metabolism decreases after exposure to bilirubin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-25 02:44:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1131412", "https://ndownloader.figshare.com/files/1131413", "https://ndownloader.figshare.com/files/1131414", "https://ndownloader.figshare.com/files/1131415", "https://ndownloader.figshare.com/files/1131416", "https://ndownloader.figshare.com/files/1131417", "https://ndownloader.figshare.com/files/1131418"], "description"=>"<div><p>Bilirubin is the terminal metabolite in heme catabolism in mammals. After deposition into bile, bilirubin is released in large quantities into the mammalian gastrointestinal (GI) tract. We hypothesized that intestinal bilirubin may modulate the function of enteric bacteria. To test this hypothesis, we investigated the effect of bilirubin on two enteric pathogens; enterohemorrhagic <i>E. coli</i> (EHEC), a Gram-negative that causes life-threatening intestinal infections, and <i>E. faecalis</i>, a Gram-positive human commensal bacterium known to be an opportunistic pathogen with broad-spectrum antibiotic resistance. We demonstrate that bilirubin can protect EHEC from exogenous and host-generated reactive oxygen species (ROS) through the absorption of free radicals. In contrast, <i>E. faecalis</i> was highly susceptible to bilirubin, which causes significant membrane disruption and uncoupling of respiratory metabolism in this bacterium. Interestingly, similar results were observed for other Gram-positive bacteria, including <i>B. cereus</i> and <i>S. aureus</i>. A model is proposed whereby bilirubin places distinct selective pressure on enteric bacteria, with Gram-negative bacteria being protected from ROS (positive outcome) and Gram-positive bacteria being susceptible to membrane disruption (negative outcome). This work suggests bilirubin has differential but biologically relevant effects on bacteria and justifies additional efforts to determine the role of this neglected waste catabolite in disease processes, including animal models.</p></div>", "links"=>[], "tags"=>["microbiology", "Bacterial pathogens", "Gram positive", "Gram negative", "Emerging infectious diseases", "Host-pathogen interaction", "Microbial pathogens", "heme", "catabolism", "modulates", "bacterial"], "article_id"=>755384, "categories"=>["Biological Sciences"], "users"=>["Christopher L. Nobles", "Sabrina I. Green", "Anthony W. Maresso"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1003507.s001", "https://dx.doi.org/10.1371/journal.ppat.1003507.s002", "https://dx.doi.org/10.1371/journal.ppat.1003507.s003", "https://dx.doi.org/10.1371/journal.ppat.1003507.s004", "https://dx.doi.org/10.1371/journal.ppat.1003507.s005", "https://dx.doi.org/10.1371/journal.ppat.1003507.s006", "https://dx.doi.org/10.1371/journal.ppat.1003507.s007"], "stats"=>{"downloads"=>12, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Product_of_Heme_Catabolism_Modulates_Bacterial_Function_and_Survival_/755384", "title"=>"A Product of Heme Catabolism Modulates Bacterial Function and Survival", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-07-25 02:44:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1131390"], "description"=>"<p>(A, Left) Wideband absorbance (420–580 nm) of EHEC (EDL933) cultures supplemented with plumbagin (0, 25, 50, and 75 µM) was monitored while cultures were grown at 37°C with shaking. (A, Right) The time to mid-log phase of each culture was calculated from the growth curves. (B) EHEC (EDL933) cultures supplemented with (grey bars) or without (white bars) plumbagin (50 µM) and/or BSA (2, 20, and 200 uM BSA) and/or ox bile (50, 100, 500, 1000 ug/mL ox bile). (C) EHEC (86-24) cultures were supplemented with plumbagin (50 µM) (grey bars) or without plumbagin (white bars) and either ox, rabbit (Rb), or human (Hu) bile (1 and 10 mg/mL ox bile; 0.5 and 5.0% rabbit and human bile). Error bars represent ± one standard deviation, n = 3, and (*) denotes a significant (P≤0.05) difference between treated samples and solvent-treated samples.</p>", "links"=>[], "tags"=>["microbiology", "Bacterial pathogens", "Gram positive", "Gram negative", "Emerging infectious diseases", "Host-pathogen interaction", "Microbial pathogens", "bile", "ehec"], "article_id"=>755364, "categories"=>["Biological Sciences"], "users"=>["Christopher L. Nobles", "Sabrina I. Green", "Anthony W. Maresso"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1003507.g001", "stats"=>{"downloads"=>3, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effect_of_bile_on_EHEC_growth_in_the_presence_of_ROS_/755364", "title"=>"The effect of bile on EHEC growth in the presence of ROS.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-25 02:44:16"}

PMC Usage Stats | Further Information

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Relative Metric

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