Erratum: Dysbiosis-Associated Change in Host Metabolism Generates Lactate to Support Salmonella Growth (Cell Host & Microbe (2018) 23(1) (54–64.e6) (S1931312817305000) (10.1016/j.chom.2017.11.006));Dysbiosis-Associated Change in Host Metabolism Generates Lactate to Support Salmonella Growth

Cell Host and Microbe

Volumn 23, Issue 1, 2018, Pages 54-64.e6

  Gillis, Caroline C ^a   Hughes, Elizabeth R ^a   Spiga, Luisella ^a   Winter, Maria G ^a   Zhu, Wenhan ^a   Furtado de Carvalho, Tatiane ^b   Chanin, Rachael B ^a   Behrendt, Cassie L ^c   Hooper, Lora V ^c   Santos, Renato L ^b   Winter, Sebastian E ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

gut microbiota; host metabolism during infection; host microbe interaction; microbial metabolism; Salmonella

Indexed keywords

BUTYRIC ACID; LACTIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; TRIBUTYRIN; ANTIINFECTIVE AGENT; LACTATE DEHYDROGENASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRIACYLGLYCEROL;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; CLOSTRIDIA; CONTROLLED STUDY; DYSBIOSIS; FERMENTATION; HOST; HOST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; TYPHOID FEVER; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CLOSTRIDIUM; DRUG EFFECT; FEMALE; GASTROENTERITIS; GROWTH, DEVELOPMENT AND AGING; INTESTINE FLORA; INTESTINE MUCOSA; MALE; METABOLISM; MICROBIOLOGY; PATHOLOGY; SALMONELLOSIS;

ANIMALS; ANTI-BACTERIAL AGENTS; BUTYRIC ACID; CLOSTRIDIUM; DYSBIOSIS; FEMALE; FERMENTATION; GASTROENTERITIS; GASTROINTESTINAL MICROBIOME; INTESTINAL MUCOSA; L-LACTATE DEHYDROGENASE; LACTIC ACID; MALE; MICE; MICE, INBRED C57BL; PPAR GAMMA; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; TRIGLYCERIDES;

EID: 85038815699     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2018.03.013     Document Type: Erratum

References (61)

1. Ackermann, M., Stecher, B., Freed, N.E., Songhet, P., Hardt, W.D., Doebeli, M., Self-destructive cooperation mediated by phenotypic noise. Nature 454 (2008), 987–990.
2. Adachi, M., Kurotani, R., Morimura, K., Shah, Y., Sanford, M., Madison, B.B., Gumucio, D.L., Marin, H.E., Peters, J.M., Young, H.A., et al. Peroxisome proliferator activated receptor gamma in colonic epithelial cells protects against experimental inflammatory bowel disease. Gut 55 (2006), 1104–1113.
3. Ahmad, M.S., Krishnan, S., Ramakrishna, B.S., Mathan, M., Pulimood, A.B., Murthy, S.N., Butyrate and glucose metabolism by colonocytes in experimental colitis in mice. Gut 46 (2000), 493–499.
4. Ali, M.M., Newsom, D.L., Gonzalez, J.F., Sabag-Daigle, A., Stahl, C., Steidley, B., Dubena, J., Dyszel, J.L., Smith, J.N., Dieye, Y., et al. Fructose-asparagine is a primary nutrient during growth of Salmonella in the inflamed intestine. PLoS Pathog., 10, 2014, e1004209.
5. Augoff, K., Hryniewicz-Jankowska, A., Tabola, R., Lactate dehydrogenase 5: an old friend and a new hope in the war on cancer. Cancer Lett. 358 (2015), 1–7.
6. Barcenilla, A., Pryde, S.E., Martin, J.C., Duncan, S.H., Stewart, C.S., Henderson, C., Flint, H.J., Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl. Environ. Microbiol. 66 (2000), 1654–1661.
7. Barman, M., Unold, D., Shifley, K., Amir, E., Hung, K., Bos, N., Salzman, N., Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect. Immun. 76 (2008), 907–915.
8. Becker, D., Selbach, M., Rollenhagen, C., Ballmaier, M., Meyer, T.F., Mann, M., Bumann, D., Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature 440 (2006), 303–307.
9. Belenguer, A., Duncan, S.H., Holtrop, G., Anderson, S.E., Lobley, G.E., Flint, H.J., Impact of pH on lactate formation and utilization by human fecal microbial communities. Appl. Environ. Microbiol. 73 (2007), 6526–6533.
10. Berkowitz, D., Hushon, J.M., Whitfield, H.J. Jr., Roth, J., Ames, B.N., Procedure for identifying nonsense mutations. J. Bacteriol. 96 (1968), 215–220.
11. Bjerrum, J.T., Wang, Y., Hao, F., Coskun, M., Ludwig, C., Gunther, U., Nielsen, O.H., Metabonomics of human fecal extracts characterize ulcerative colitis, Crohn's disease and healthy individuals. Metabolomics 11 (2015), 122–133.
12. Byndloss, M.X., Olsan, E.E., Rivera-Chavez, F., Tiffany, C.R., Cevallos, S.A., Lokken, K.L., Torres, T.P., Byndloss, A.J., Faber, F., Gao, Y., et al. Microbiota-activated PPAR-gamma signaling inhibits dysbiotic Enterobacteriaceae expansion. Science 357 (2017), 570–575.
13. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G., Goodrich, J.K., Gordon, J.I., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 (2010), 335–336.
14. Donohoe, D.R., Wali, A., Brylawski, B.P., Bultman, S.J., Microbial regulation of glucose metabolism and cell-cycle progression in mammalian colonocytes. PLoS One, 7, 2012, e46589.
15. Eisele, N.A., Ruby, T., Jacobson, A., Manzanillo, P.S., Cox, J.S., Lam, L., Mukundan, L., Chawla, A., Monack, D.M., Salmonella require the fatty acid regulator PPARdelta for the establishment of a metabolic environment essential for long-term persistence. Cell Host Microbe 14 (2013), 171–182.
16. Faber, F., Thiennimitr, P., Spiga, L., Byndloss, M.X., Litvak, Y., Lawhon, S., Andrews-Polymenis, H.L., Winter, S.E., Baumler, A.J., Respiration of microbiota-derived 1,2-propanediol drives Salmonella expansion during colitis. PLoS Pathog., 13, 2017, e1006129.
17. Faber, F., Tran, L., Byndloss, M.X., Lopez, C.A., Velazquez, E.M., Kerrinnes, T., Nuccio, S.P., Wangdi, T., Fiehn, O., Tsolis, R.M., et al. Host-mediated sugar oxidation promotes post-antibiotic pathogen expansion. Nature 534 (2016), 697–699.
18. Ferreyra, J.A., Wu, K.J., Hryckowian, A.J., Bouley, D.M., Weimer, B.C., Sonnenburg, J.L., Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe 16 (2014), 770–777.
19. Galan, J.E., Curtiss, R. 3rd, Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA 86 (1989), 6383–6387.
20. Gutnick, D., Calvo, J.M., Klopotowski, T., Ames, B.N., Compounds which serve as the sole source of carbon or nitrogen for Salmonella Typhimurium LT-2. J. Bacteriol. 100 (1969), 215–219.
21. Hensel, M., Shea, J.E., Gleeson, C., Jones, M.D., Dalton, E., Holden, D.W., Simultaneous identification of bacterial virulence genes by negative selection. Science 269 (1995), 400–403.
22. Hove, H., Holtug, K., Jeppesen, P.B., Mortensen, P.B., Butyrate absorption and lactate secretion in ulcerative colitis. Dis. Colon Rectum 38 (1995), 519–525.
23. Hove, H., Mortensen, P.B., Influence of intestinal inflammation (IBD) and small and large bowel length on fecal short-chain fatty acids and lactate. Dig. Dis. Sci. 40 (1995), 1372–1380.
24. Hughes, E.R., Winter, M.G., Duerkop, B.A., Spiga, L., Furtado de Carvalho, T., Zhu, W., Gillis, C.C., Buttner, L., Smoot, M.P., Behrendt, C.L., et al. Microbial respiration and formate oxidation as metabolic signatures of inflammation-associated dysbiosis. Cell Host Microbe 21 (2017), 208–219.
25. Kelly, C.J., Zheng, L., Campbell, E.L., Saeedi, B., Scholz, C.C., Bayless, A.J., Wilson, K.E., Glover, L.E., Kominsky, D.J., Magnuson, A., et al. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe 17 (2015), 662–671.
26. Kingsley, R.A., Reissbrodt, R., Rabsch, W., Ketley, J.M., Tsolis, R.M., Everest, P., Dougan, G., Baumler, A.J., Roberts, M., Williams, P.H., Ferrioxamine-mediated iron(III) utilization by Salmonella enterica. Appl. Environ. Microbiol. 65 (1999), 1610–1618.
27. Kingsley, R.A., Humphries, A.D., Weening, E.H., De Zoete, M.R., Winter, S., Papaconstantinopoulou, A., Dougan, G., Baumler, A.J., Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype typhimurium: identification of intestinal colonization and persistence determinants. Infect. Immun. 71 (2003), 629–640.
28. Lopez, C.A., Rivera-Chavez, F., Byndloss, M.X., Baumler, A.J., The periplasmic nitrate reductase NapABC supports luminal growth of Salmonella enterica serovar Typhimurium during colitis. Infect. Immun. 83 (2015), 3470–3478.
29. Lopez, C.A., Winter, S.E., Rivera-Chavez, F., Xavier, M.N., Poon, V., Nuccio, S.P., Tsolis, R.M., Baumler, A.J., Phage-mediated acquisition of a type III secreted effector protein boosts growth of Salmonella by nitrate respiration. MBio, 3, 2012, 10.1128/mBio.00143-12.
30. Macdonald, R.H., Beck, M., Neomycin: a review with particular reference to dermatological usage. Clin. Exp. Dermatol. 8 (1983), 249–258.
31. McClelland, M., Sanderson, K.E., Spieth, J., Clifton, S.W., Latreille, P., Courtney, L., Porwollik, S., Ali, J., Dante, M., Du, F., et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413 (2001), 852–856.
32. McCoy, M.W., Moreland, S.M., Detweiler, C.S., Hemophagocytic macrophages in murine typhoid fever have an anti-inflammatory phenotype. Infect. Immun. 80 (2012), 3642–3649.
33. Miller, V.L., Mekalanos, J.J., A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170 (1988), 2575–2583.
34. Monack, D.M., Helicobacter and Salmonella persistent infection strategies. Cold Spring Harb. Perspect. Med., 3, 2013, a010348.
35. Montgomery, R.D., Frazer, A.C., Hood, C., Goodhart, J.M., Holland, M.R., Schneider, R., Studies of intestinal fermentation in ulcerative colitis. Gut 9 (1968), 521–526.
36. Ng, K.M., Ferreyra, J.A., Higginbottom, S.K., Lynch, J.B., Kashyap, P.C., Gopinath, S., Naidu, N., Choudhury, B., Weimer, B.C., Monack, D.M., et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502 (2013), 96–99.
37. Nix, R.N., Altschuler, S.E., Henson, P.M., Detweiler, C.S., Hemophagocytic macrophages harbor Salmonella enterica during persistent infection. PLoS Pathog., 3, 2007, e193.
38. Pal, D., Venkova-Canova, T., Srivastava, P., Chattoraj, D.K., Multipartite regulation of rctB, the replication initiator gene of Vibrio cholerae chromosome II. J. Bacteriol. 187 (2005), 7167–7175.
39. Pavia, A.T., Shipman, L.D., Wells, J.G., Puhr, N.D., Smith, J.D., McKinley, T.W., Tauxe, R.V., Epidemiologic evidence that prior antimicrobial exposure decreases resistance to infection by antimicrobial-sensitive Salmonella. J. Infect. Dis. 161 (1990), 255–260.
40. Pryde, S.E., Duncan, S.H., Hold, G.L., Stewart, C.S., Flint, H.J., The microbiology of butyrate formation in the human colon. FEMS Microbiol. Lett. 217 (2002), 133–139.
41. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glockner, F.O., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:Database issue (2013), D590–D596.
42. Rivera-Chavez, F., Baumler, A.J., The pyromaniac inside you: Salmonella metabolism in the host gut. Annu. Rev. Microbiol. 69 (2015), 31–48.
43. Rivera-Chavez, F., Winter, S.E., Lopez, C.A., Xavier, M.N., Winter, M.G., Nuccio, S.P., Russell, J.M., Laughlin, R.C., Lawhon, S.D., Sterzenbach, T., et al. Salmonella uses energy taxis to benefit from intestinal inflammation. PLoS Pathog., 9, 2013, e1003267.
44. Rivera-Chavez, F., Zhang, L.F., Faber, F., Lopez, C.A., Byndloss, M.X., Olsan, E.E., Xu, G., Velazquez, E.M., Lebrilla, C.B., Winter, S.E., et al. Depletion of butyrate-producing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella. Cell Host Microbe 19 (2016), 443–454.
45. Santos, R.L., Pathobiology of Salmonella, intestinal microbiota, and the host innate immune response. Front. Immunol., 5, 2014, 252.
46. Sekirov, I., Gill, N., Jogova, M., Tam, N., Robertson, M., de Llanos, R., Li, Y., Finlay, B.B., Salmonella SPI-1-mediated neutrophil recruitment during enteric colitis is associated with reduction and alteration in intestinal microbiota. Gut Microbes 1 (2010), 30–41.
47. Simon, R., Priefer, U., Puhler, A., A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat. Biotechnol. 1 (1983), 784–791.
48. Spiga, L., Winter, M.G., Furtado de Carvalho, T., Zhu, W., Hughes, E.R., Gillis, C.C., Behrendt, C.L., Kim, J., Chessa, D., Andrews-Polymenis, H.L., et al. An oxidative central metabolism enables Salmonella to utilize microbiota-derived succinate. Cell Host Microbe 22 (2017), 291–301.e6.
49. Stecher, B., Robbiani, R., Walker, A.W., Westendorf, A.M., Barthel, M., Kremer, M., Chaffron, S., Macpherson, A.J., Buer, J., Parkhill, J., et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5 (2007), 2177–2189.
50. Steeb, B., Claudi, B., Burton, N.A., Tienz, P., Schmidt, A., Farhan, H., Maze, A., Bumann, D., Parallel exploitation of diverse host nutrients enhances Salmonella virulence. PLoS Pathog., 9, 2013, e1003301.
51. Stojiljkovic, I., Baumler, A.J., Heffron, F., Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J. Bacteriol. 177 (1995), 1357–1366.
52. Thiennimitr, P., Winter, S.E., Winter, M.G., Xavier, M.N., Tolstikov, V., Huseby, D.L., Sterzenbach, T., Tsolis, R.M., Roth, J.R., Baumler, A.J., Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl. Acad. Sci. USA 108 (2011), 17480–17485.
53. Tsolis, R.M., Adams, L.G., Ficht, T.A., Baumler, A.J., Contribution of Salmonella Typhimurium virulence factors to diarrheal disease in calves. Infect. Immun. 67 (1999), 4879–4885.
54. Vazquez-Baeza, Y., Pirrung, M., Gonzalez, A., Knight, R., EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience, 2, 2013, 16.
55. Vernia, P., Caprilli, R., Latella, G., Barbetti, F., Magliocca, F.M., Cittadini, M., Fecal lactate and ulcerative colitis. Gastroenterology 95 (1988), 1564–1568.
56. Vernia, P., Gnaedinger, A., Hauck, W., Breuer, R.I., Organic anions and the diarrhea of inflammatory bowel disease. Dig. Dis. Sci. 33 (1988), 1353–1358.
57. Vogel, H.J., Bonner, D.M., Acetylornithinase of Escherichia coli: partial purification and some properties. J. Biol. Chem. 218 (1956), 97–106.
58. Winter, S.E., Winter, M.G., Thiennimitr, P., Gerriets, V.A., Nuccio, S.P., Russmann, H., Baumler, A.J., The TviA auxiliary protein renders the Salmonella enterica serotype Typhi RcsB regulon responsive to changes in osmolarity. Mol. Microbiol. 74 (2009), 175–193.
59. Winter, S.E., Thiennimitr, P., Winter, M.G., Butler, B.P., Huseby, D.L., Crawford, R.W., Russell, J.M., Bevins, C.L., Adams, L.G., Tsolis, R.M., et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467 (2010), 426–429.
60. Winter, S.E., Winter, M.G., Xavier, M.N., Thiennimitr, P., Poon, V., Keestra, A.M., Laughlin, R.C., Gomez, G., Wu, J., Lawhon, S.D., et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339 (2013), 708–711.
61. Zhang, S., Santos, R.L., Tsolis, R.M., Stender, S., Hardt, W.D., Baumler, A.J., Adams, L.G., The Salmonella enterica serotype typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect. Immun. 70 (2002), 3843–3855.