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The microbiota and helminths: sharing the same niche in the human host

Published online by Cambridge University Press:  05 June 2014

LAURA GLENDINNING Open the ORCID record for LAURA GLENDINNING [Opens in a new window] ,
NORMAN NAUSCH ,
ANDREW FREE ,
DAVID W. TAYLOR  and
FRANCISCA MUTAPI
LAURA GLENDINNING*
Affiliation:
Institute of Immunology and Infection Research, Centre for Immunity, Infection and Evolution, School of Biological Sciences, Ashworth Laboratories, University of Edinburgh, Edinburgh EH9 3JT, UK
NORMAN NAUSCH
Affiliation:
Institute of Immunology and Infection Research, Centre for Immunity, Infection and Evolution, School of Biological Sciences, Ashworth Laboratories, University of Edinburgh, Edinburgh EH9 3JT, UK
ANDREW FREE
Affiliation:
Institute of Cell Biology, University of Edinburgh, The King's Buildings, Mayfield Road, Edinburgh EH9 3JR, UK
DAVID W. TAYLOR
Affiliation:
Division of Pathway Medicine, School of Biomedical Sciences, Ashworth Laboratories, University of Edinburgh, Edinburgh EH9 3JT, UK
FRANCISCA MUTAPI
Affiliation:
Institute of Immunology and Infection Research, Centre for Immunity, Infection and Evolution, School of Biological Sciences, Ashworth Laboratories, University of Edinburgh, Edinburgh EH9 3JT, UK
*
* Corresponding author: Desk 01.143N, Roslin Institute, University of Edinburgh, Easter Bush, Edinburgh EH25 9RG, UK. E-mail: [email protected]
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Summary

Human gastrointestinal bacteria often share their environment with parasitic worms, allowing physical and physiological interaction between the two groups. Such associations have the potential to affect host health as well as the bacterial and helminth populations. Although still in its early stages, research on the interaction between the microbiome and parasitic helminths in humans offers the potential to improve health by manipulating the microbiome. Previously, supplementation with various nutritional compounds has been found to increase the abundance of potentially beneficial gut commensal bacteria. Thus, nutritional microbiome manipulation to produce an environment which may decrease malnutrition associated with helminth infection and/or aid host recovery from disease is conceivable. This review discusses the influence of the gut microbiota and helminths on host nutrition and immunity and the subsequent effects on the human host's overall health. It also discusses changes occurring in the microbiota upon helminth infections and the underlying mechanisms leading to these changes. There are still significant knowledge gaps which need to be filled before meaningful progress can be made in translating knowledge from studying the human gut microbiome into therapeutic strategies. Ultimately this review aims to discuss our current knowledge as well as highlight areas requiring further investigation.

Keywords

microbiotahelminthsbacterianutritionimmunologyco-infectionhomoeostasispublic health
Type
Review Article
Information
Parasitology , Volume 141 , Issue 10 , September 2014 , pp. 1255 - 1271
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Abreu, M. T., Vora, P., Faure, E., Thomas, L. S., Arnold, E. T. and Arditi, M. (2001). Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. Journal of Immunology 167, 1609–1616.CrossRefGoogle ScholarPubMed
Altier, C. (2005). Genetic and environmental control of salmonella invasion. Journal of Microbiology 43, 85–92.Google Scholar
Anderson, R. M. and May, R. M. (1992). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford, UK.Google Scholar
Anthony, R. M., Rutitzky, L. I., Urban, J. F. Jr., Stadecker, M. J. and Gause, W. C. (2007). Protective immune mechanisms in helminth infection. Nature Reviews Immunology 7, 975–987. doi: 10.1038/nri2199.Google Scholar
Archibald, F. (1983). Lactobacillus plantarum, an organism not requiring iron. Federation of European Microbiological Societies Microbiology Letters 19, 29–32. doi: 10.1111/j.1574-6968.1983.tb00504.x.Google Scholar
Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., Batto, J.-M., Bertalan, M., Borruel, N., Casellas, F., Fernandez, L., Gautier, L., Hansen, T., Hattori, M., Hayashi, T., Kleerebezem, M., Kurokawa, K., Leclerc, M., Levenez, F., Manichanh, C., Nielsen, H. B., Nielsen, T., Pons, N., Poulain, J., Qin, J., Sicheritz-Ponten, T., Tims, S., Torrents, D., Ugarte, E., Zoetendal, E. G., Wang, J., Guarner, F., Perderson, O., de Vos, W. M., Brunak, S., Doré, J., MetaHIT Consortium, Weissenbach, J., Ehrlich, S. D. and Bork, P. (2011). Enterotypes of the human gut microbiome. Nature 473, 174–180. doi: 10.1038/nature09944.Google Scholar
Attinkara, R., Mwinyi, J., Truninger, K., Regula, J., Gaj, P., Rogler, G., Kullak-Ublick, G. A., Eloranta, J. J. and The Swiss IBD Cohort Study Group (2012). Association of genetic variation in the NR1H4 gene, encoding the nuclear bile acid receptor FXR, with inflammatory bowel disease. BMC Research Notes 5, 461. doi: 10.1186/1756-0500-5-461.Google Scholar
Bäckhed, F., Fraser, C. M., Ringel, Y., Sanders, M. E., Sartor, R. B., Sherman, P. M., Versalovic, J., Young, V. and Finlay, B. B. (2012). Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host and Microbe 12, 611–622. doi: 10.1016/j.chom.2012.10.012.Google Scholar
Balog, C. I. A., Meissner, A., Göraler, S., Bladergroen, M. R., Vennervald, B. J., Mayboroda, O. A. and Deelder, A. M. (2011). Metabonomic investigation of human Schistosoma mansoni infection. Molecular Biosystems 7, 1473–1480. doi: 10.1039/c0mb00262c.Google Scholar
Bialonska, D., Ramnani, P., Kasimsetty, S. G., Muntha, K. R., Gibson, G. R. and Ferreira, D. (2010). The influence of pomegranate by-product and punicalagins on selected groups of human intestinal microbiota. International Journal of Food Microbiology 140, 175–182. doi: 10.1016/j.ijfoodmicro.2010.03.038.Google Scholar
Brestoff, J. R. and Artis, D. (2013). Commensal bacteria at the interface of host metabolism and the immune system. Nature Immunology 14, 676–684. doi: 10.1038/ni.2640.Google Scholar
Breznak, J. A. and Kane, M. D. (1990). Microbial H2/CO2 acetogenesis in animal guts: nature and nutritional significance. Federation of European Microbiological Societies Microbiology Letters 87, 309–313. doi: 10.1111/j.1574-6968.1990.tb04929.x.CrossRefGoogle Scholar
Britton, R. A. and Young, V. B. (2012). Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance. Trends in Microbiology 20, 313–319. doi: 10.1016/j.tim.2012.04.001.Google Scholar
Broadhurst, M. J., Leung, J. M., Kashyap, V., McCune, J. M., Mahadevan, U., McKerrow, J. H. and Loke, P. (2010). IL-22+ CD4+ T cells are associated with therapeutic Trichuris trichiura infection in an ulcerative colitis patient. Science Translational Medicine 2, 60–88. doi: 10.1126/scitranslmed.3001500.CrossRefGoogle Scholar
Broadhurst, M. J., Ardeshir, A., Kanwar, B., Mirpuri, J., Gundra, U. M., Leung, J. M., Wiens, K. E., Vujkovic-Cvijin, I., Kim, C. C., Yarovinsky, F., Lerche, N. W., McCune, J. M. and Loke, P. (2012). Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLOS Pathogens 8, e1003000. doi: 10.1371/journal.ppat.1003000.CrossRefGoogle ScholarPubMed
Brown, K., DeCoffe, D., Molcan, E. and Gibson, D. L. (2012). Diet-induced dysbiosis of the intestinal microbiota and the effects on immunity and disease. Nutrients 4, 1095–1119. doi: 10.3390/nu4081095.Google Scholar
Chandra, R. K. (1992). Effect of vitamin and trace-element supplementation on immune responses and infection in elderly subjects. Lancet 340, 1124–1127. doi: 10.1016/0140-6736(92)93151-C.Google Scholar
Chang, J. and Wescott, R. B. (1972). Infectivity, fecundity, and survival of Nematospiroides dubius in gnotobiotic mice. Experimental Parasitology 32, 327–334. doi: 10.1016/0014-4894(72)90060-4.CrossRefGoogle ScholarPubMed
Chen, F., Liu, Z., Wu, W., Rozo, C., Bowdridge, S., Millman, A., Van Rooijen, N., Urban, J. F. Jr., Wynn, T. A. and Gause, W. C. (2012). An essential role for Th2-type responses in limiting acute tissue damage during experimental helminth infection. Nature Medicine 18, 260–266. doi: 10.1038/nm.2628.Google Scholar
Cherrington, C. A., Hinton, M., Pearson, G. R. and Chopra, I. (1991). Short-chain organic acids at pH 5·0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation. Journal of Applied Microbiology 70, 161–165. doi: 10.1111/j.1365-2672.1991.tb04442.x.Google Scholar
Chinen, T. and Rudensky, A. Y. (2012). The effects of commensal microbiota on immune cell subsets and inflammatory responses. Immunological Reviews 245, 45–55. doi: 10.1111/j.1600-065X.2011.01083.x.Google Scholar
Chung, H., Pamp, S. J., Hill, J. A., Surana, N. K., Edelman, S. M., Troy, E. B., Reading, N. C., Villablanca, E. J., Wang, S., Mora, J. R., Umesaki, Y., Mathis, D., Benoist, C., Relman, D. A. and Kasper, D. L. (2012). Gut immune maturation depends on colonization with a host-specific microbiota. Cell 149, 1578–1593. doi: 10.1016/j.cell.2012.04.037.Google Scholar
Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O'Connor, E. M., Cusack, S., Harris, H. M. B., Coakley, M., Lakshminarayanan, B., O'Sullivan, O., Fitzgerald, G. F., Deane, J., O'Connor, M., Harnedy, N., O'Connor, K., O'Mahony, D., van Sinderen, D., Wallace, M., Brennan, L., Stanton, C., Marchesi, J. R., Fitzgerald, A. P., Shanahan, F., Hill, C., Ross, R. P. and O'Toole, P. W. (2012). Gut microbiota composition correlates with diet and health in the elderly. Nature 488, 178–184. doi: 10.1038/nature11319.Google Scholar
Collado, M. C., Calabuig, M. and Sanz, Y. (2007). Differences between the fecal microbiota of coeliac infants and healthy controls. Current Issues in Intestinal Microbiology 8, 9–14.Google Scholar
Collado, M. C., Isolauri, E., Laitinen, K. and Salminen, S. (2010). Effect of mother's weight on infant's microbiota acquisition, composition, and activity during early infancy: a prospective follow-up study initiated in early pregnancy. American Journal of Clinical Nutrition 92, 1023–1030. doi: 10.3945/ajcn.2010.29877.Google Scholar
Conroy, M. E., Shi, H. N. and Walker, W. A. (2009). The long-term health effects of neonatal microbial flora. Current Opinion in Allergy and Clinical Immunology 9, 197–201. doi: 10.1097/ACI.0b013e32832b3f1d.Google Scholar
Cooper, P., Walker, A. W., Reyes, J., Chico, M., Salter, S. J., Vaca, M. and Parkhill, J. (2013). Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLOS ONE, 8, e76573. doi: 10.1371/journal.pone.0076573.Google Scholar
Costabile, A., Fava, F., Röytiö, H., Forssten, S. D., Olli, K., Klievink, J., Rowland, I. R., Ouwehand, A. C., Rastall, R. A., Gibson, G. R. and Walton, G. E. (2012). Impact of polydextrose on the faecal microbiota: a double-blind, crossover, placebo-controlled feeding study in healthy human subjects. British Journal of Nutrition 108, 471–481. doi: 10.1017/S0007114511005782.Google Scholar
Croese, J., O'Neil, J., Masson, J., Cooke, S., Melrose, W., Pritchard, D. and Speare, R. (2006). A proof of concept study establishing Necator americanus in Crohn's patients and reservoir donors. Gut 55, 136–137. doi: 10.1136/gut.2005.079129.Google Scholar
Daveson, A. J., Jones, D. M., Gaze, S., McSorley, H., Clouston, A., Pascoe, A., Cooke, S., Speare, R., Macdonald, G. A., Anderson, R., McCarthy, J. S., Loukas, A. and Croese, J. (2011). Effect of hookworm infection on wheat challenge in celiac disease – a randomised double-blinded placebo controlled trial. PLOS ONE 6, e17366. doi: 10.1371/journal.pone.0017366.Google Scholar
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., Biddinger, S. B., Dutton, R. J. and Turnbaugh, P. J. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563. doi: 10.1038/nature12820.Google Scholar
De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J. B., Massart, S., Collini, S., Pieraccini, G. and Lionetti, P. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proceedings of the National Academy of Sciences USA 107, 14691–14696. doi: 10.1073/pnas.1005963107.Google Scholar
Derrien, M., Collado, M. C., Ben-Amor, K., Salminen, S. and de Vos, W. M. (2008). The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Applied and Environmental Microbiology 74, 1646–1648. doi: 10.1128/aem.01226-07.Google Scholar
Dethlefsen, L. and Relman, D. A. (2011). Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proceedings of the National Academy of Sciences USA 108, 4554–4561. doi: 10.1073/pnas.1000087107.Google Scholar
Dorny, P., Praet, N., Deckers, N. and Gabriel, S. (2009). Emerging food-borne parasites. Veterinary Parasitology 163, 196–206. doi: 10.1016/j.vetpar.2009.05.026.CrossRefGoogle ScholarPubMed
Ellis, R. J., Bruce, K. D., Jenkins, C., Stothard, J. R., Ajarova, L., Mugisha, L. and Viney, M. E. (2013). Comparison of the distal gut microbiota from people and animals in Africa. PLOS ONE 8, e54783. doi: 10.1371/journal.pone.0054783.Google Scholar
Fallani, M., Young, D., Scott, J., Norin, E., Amarri, S., Adam, R., Aguilera, M., Khanna, S., Gil, A., Edwards, C. A. and Doré, J. (2010). Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. Journal of Pediatric Gastroenterology and Nutrition 51, 77–84. doi: 10.1097/MPG.0b013e3181d1b11e.Google Scholar
Feary, J. R., Venn, A. J., Mortimer, K., Brown, A. P., Hooi, D., Falcone, F. H., Pritchard, D. I. and Britton, J. R. (2010). Experimental hookworm infection: a randomized placebo-controlled trial in asthma. Clinical and Experimental Allergy 40, 299–306. doi: 10.1111/j.1365-2222.2009.03433.x.Google Scholar
Ferguson, A. D., Hofmann, E., Coulton, J. W., Diederichs, K. and Welte, W. (1998). Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282, 2215–2220. doi: 10.1126/science.282.5397.2215.Google Scholar
Fite, A., Macfarlane, S., Furrie, E., Bahrami, B., Cummings, J. H., Steinke, D. T. and Macfarlane, G. T. (2013). Longitudinal analyses of gut mucosal microbiotas in ulcerative colitis in relation to patient age and disease severity and duration. Journal of Clinical Microbiology 51, 849–856. doi: 10.1128/jcm.02574-12.Google Scholar
Flint, H. J., Bayer, E. A., Rincon, M. T., Lamed, R. and White, B. A. (2008). Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature Reviews Microbiology 6, 121–131. doi: 10.1038/nrmicro1817.Google Scholar
Forman, R. A., deSchoolmeester, M. L., Hurst, R. J. M., Wright, S. H., Pemberton, A. D. and Else, K. J. (2012). The goblet cell is the cellular source of the anti-microbial angiogenin 4 in the large intestine post Trichuris muris infection. PLOS ONE 7, e42248. doi: 10.1371/journal.pone.0042248.Google Scholar
Franchi, L., Kamada, N., Nakamura, Y., Burberry, A., Kuffa, P., Suzuki, S., Shaw, M. H., Kim, Y.-G. and Nunez, G. (2012). NLRC4-driven production of IL-1 beta discriminates between pathogenic and commensal bacteria and promotes host intestinal defense. Nature Immunology 13, 449–456. doi: 10.1038/ni.2263.Google Scholar
Friberg, I. M., Little, S., Ralli, C., Lowe, A., Hall, A., Jackson, J. A. and Bradley, J. E. (2013). Macroparasites at peripheral sites of infection are major and dynamic modifiers of systemic antimicrobial pattern recognition responses. Molecular Ecology 22, 2810–2826. doi: 10.1111/mec.12212.Google Scholar
Friedman, J. F., Kanzaria, H. K. and McGarvey, S. T. (2005). Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends in Parasitology 21, 386–392. doi: 10.1016/j.pt.2005.06.006.Google Scholar
Friis, H., Ndhlovu, P., Kaondera, K., Sandström, B., Michaelsen, K. F., Vennervald, B. J. and Christensen, N. O. (1996). Serum concentration of micronutrients in relation to schistosomiasis and indicators of infection: a cross-sectional study among rural Zimbabwean schoolchildren. European Journal of Clinical Nutrition 50, 386–391.Google Scholar
Fukuda, S., Toh, H., Hase, K., Oshima, K., Nakanishi, Y., Yoshimura, K., Tobe, T., Clarke, J. M., Topping, D. L., Suzuki, T., Taylor, T. D., Itoh, K., Kikuchi, J., Morite, H., Hattori, M. and Ohno, H. (2011). Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543–547. doi: 10.1038/nature09646.Google Scholar
Gantois, I., Ducatelle, R., Pasmans, F., Haesebrouck, F., Hautefort, I., Thompson, A., Hinton, J. C. and Van Immerseel, F. (2006). Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression. Applied and Environmental Microbiology 72, 946–949. doi: 10.1128/AEM.72.1.946-949.2006.Google Scholar
Ganz, T. (2003). Defensins: antimicrobial peptides of innate immunity. Nature Reviews Immunology 3, 710–720. doi: 10.1038/nri1180.Google Scholar
Gareau, M. G., Sherman, P. M. and Walker, W. A. (2010). Probiotics and the gut microbiota in intestinal health and disease. Nature Reviews Gastroenterology and Hepatology 7, 503–514. doi: 10.1038/nrgastro.2010.117.Google Scholar
Gazzinelli, A., Correa-Oliveira, R., Yang, G.-J., Boatin, B. A. and Kloos, H. (2012). A research agenda for helminth diseases of humans: social ecology, environmental determinants, and health systems. PLOS Neglected Tropical Diseases 6, e1603. doi: 10.1371/journal.pntd.0001603.Google Scholar
Gill, S. R., Pop, M., DeBoy, R. T., Eckburg, P. B., Turnbaugh, P. J., Samuel, B. S., Gordon, J. I., Relman, D. A., Fraser-Liggett, C. M. and Nelson, K. E. (2006). Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359. doi: 10.1126/science.1124234.Google Scholar
Gilles, H. M., Williams, E. J. W. and Ball, P. A. J. (1964). Hookworm infection and anaemia: an epidemiological, clinical, and laboratory study. Quarterly Journal of Medicine 33, 1–24.Google Scholar
Göker, M., Gronow, S., Zeytun, A., Nolan, M., Lucas, S., Lapidus, A., Hammon, N., Deshpande, S., Cheng, J.-F., Pitluck, S., Liolios, K., Pagani, I., Ivanova, N., Mavromatis, K., Ovchinnikova, G., Pati, A., Tapia, R., Han, C., Goodwin, L., Chen, A., Palaniappan, K., Land, M., Hauser, L., Jeffries, C. D., Brambilla, E. M., Rohde, M., Detter, J. C., Woyke, T., Bristow, J., Markowitz, V., Hugenholtz, P., Eisen, J. A., Kyrpides, N. C. and Klenk, H.-P. (2011). Complete genome sequence of Odoribacter splanchnicus type strain (1651/6T). Standards in Genomic Sciences 4, 200–209. doi: 10.4056/sigs.1714269.Google Scholar
Hall, A., Zhang, Y., MacArthur, C. and Baker, S. (2012). The role of nutrition in integrated programs to control neglected tropical diseases. BioMed Central Medicine 10, 41. doi: 10.1186/1741-7015-10-41.Google Scholar
Hamrick, H. J., Bowdre, J. H. and Church, S. M. (1990). Rat tapeworm (Hymenolepis diminuta) infection in a child. Pediatric Infectious Disease Journal 9, 216–219. doi: 10.1097/00006454-199003000-00016.Google Scholar
Haque, R., Ahmed, T., Wahed, M. A., Mondal, D., Rahman, A. S. M. H. and Albert, M. J. (2010). Low-dose β-carotene supplementation and deworming improve serum vitamin A and β-carotene concentrations in preschool children of Bangladesh. Journal of Health, Population, and Nutrition 28, 230–237. doi: 10.3329/jhpn.v28i3.5549.Google Scholar
Harmsen, H. J. M., Wildeboer-Veloo, A. C. M., Raangs, G. C., Wagendorp, A. A., Klijn, N., Bindels, J. G. and Welling, G. W. (2006). Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. Journal of Pediatric Gastroenterology and Nutrition 30, 61–67. doi: 10.1097/00005176-200001000-00019.Google Scholar
Hayashi, H., Takahashi, R., Nishi, T., Sakamoto, M. and Benno, Y. (2005). Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. Journal of Medical Microbiology 54, 1093–1101. doi: 10.1099/jmm.0.45935-0.CrossRefGoogle ScholarPubMed
Hayes, K. S., Bancroft, A. J., Goldrick, M., Portsmouth, C., Roberts, I. S. and Grencis, R. K. (2010). Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris . Science 328, 1391–1394. doi: 10.1126/science.1187703.CrossRefGoogle ScholarPubMed
Hoffmann, C., Dollive, S., Grunberg, S., Chen, J., Li, H., Wu, G. D., Lewis, J. D. and Bushman, F. D. (2013). Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLOS ONE 8, e66019. doi: 10.1371/journal.pone.0066019.Google Scholar
Holzscheiter, M., Layland, L. E., Loffredo-Verde, E., Mair, K., Vogelmann, R., Langer, R., Wagner, H. and Prazeres da Costa, C. (2014). Lack of host gut microbiota alters immune responses and intestinal granuloma formation during schistosomiasis. Clinical and Experimental Immunology 175, 246–257. doi: 10.1111/cei.12230.Google Scholar
Hosseini, E., Grootaert, C., Verstraete, W. and Van de Wiele, T. (2011). Propionate as a health-promoting microbial metabolite in the human gut. Nutrition Reviews 69, 245–258. doi: 10.1111/j.1753-4887.2011.00388.x.Google Scholar
Hotez, P. J., Brindley, P. J., Bethony, J. M., King, C. H., Pearce, E. J. and Jacobson, J. (2008). Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 1311–1321. doi: 10.1172/jci34261.CrossRefGoogle ScholarPubMed
Imaoka, A., Shima, T., Kato, K., Mizuno, S., Uehara, T., Matsumoto, S., Setoyama, H., Hara, T. and Umesaki, Y. (2008). Anti-inflammatory activity of probiotic Bifidobacterium: enhancement of IL-10 production in peripheral blood mononuclear cells from ulcerative colitis patients and inhibition of IL-8 secretion in HT-29 cells. World Journal of Gastroenterology 14, 2511–2516. doi: 10.3748/wjg.14.2511.Google Scholar
Jeffery, I. B., Claesson, M. J., O'Toole, P. W. and Shanahan, F. (2012). Categorization of the gut microbiota: enterotypes or gradients? Nature Reviews Microbiology 10, 591–592. doi: 10.1038/nrmicro2859.Google Scholar
Jenq, R. R., Ubeda, C., Taur, Y., Menezes, C. C., Khanin, R., Dudakov, J. A., Liu, C., West, M. L., Singer, N. V., Equinda, M. J., Gobourne, A., Lipuma, L., Young, L. F., Smith, O. M., Ghosh, A., Hanash, A. M., Goldberg, J. D., Aoyama, K., Blazar, B. R., Pamer, E. G. and van den Brink, M. R. M. (2012). Regulation of intestinal inflammation by microbiota following allogeneic bone marrow transplantation. Journal of Experimental Medicine 209, 903–911. doi: 10.1084/jem.20112408.Google Scholar
Johnson, J. and Reid, W. M. (1973). Ascaridia galli (Nematoda): development and survival in gnotobiotic chickens. Experimental Parasitology 33, 95–99. doi: 10.1016/0014-4894(73)90013-1.Google Scholar
Jose, D. G. and Good, R. A. (1973). Quantitative effects of nutritional essential amino acid deficiency upon immune responses to tumors in mice. Journal of Experimental Medicine 137, 1–9. doi: 10.1084/jem.137.1.1.Google Scholar
Kaci, G., Lakhdari, O., Doré, J., Ehrlich, S. D., Renault, P., Blottière, H. M. and Delorme, C. (2011). Inhibition of the NF-κB pathway in human intestinal epithelial cells by commensal Streptococcus salivarius . Applied and Environmental Microbiology 77, 4681–4684. doi: 10.1128/aem.03021-10.Google Scholar
Kelly, D., Campbell, J. I., King, T. P., Grant, G., Jansson, E. A., Coutts, A. G., Pettersson, S. and Conway, S. (2004). Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nature Immunology 5, 104–112. doi: 10.1038/ni1018.Google Scholar
Khokhlova, E. V., Smeianov, V. V., Efimov, B. A., Kafarskaia, L. I., Pavlova, S. I. and Shkoporov, A. N. (2012). Anti-inflammatory properties of intestinal Bifidobacterium strains isolated from healthy infants. Microbiology and Immunology 56, 27–39. doi: 10.1111/j.1348-0421.2011.00398.x.Google Scholar
Khoruts, A., Dicksved, J., Jansson, J. K. and Sadowsky, M. J. (2010). Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent Clostridium difficile-associated diarrhea. Journal of Clinical Gastroenterology 44, 354–360. doi: 10.1097/MCG.0b013e3181c87e02.CrossRefGoogle ScholarPubMed
Kim, M. and Yu, Z. (2012). Quantitative comparisons of select cultured and uncultured microbial populations in the rumen of cattle fed different diets. Journal of Animal Science and Biotechnology 3, 28. doi: 10.1186/2049-1891-3-28.Google Scholar
King, C. H. and Dangerfield-Cha, M. (2008). The unacknowledged impact of chronic schistosomiasis. Chronic Illness 4, 65–79. doi: 10.1177/1742395307084407.Google Scholar
Koren, O., Knights, D., Gonzalez, A., Waldron, L., Segata, N., Knight, R., Huttenhower, C. and Ley, R. E. (2013). A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLOS Computational Biology 9, e1002863. doi: 10.1371/journal.pcbi.1002863.Google Scholar
Kosik-Bogacka, D. I., Wojtkowiak-Giera, A., Kolasa, A., Salamatin, R., Jagodzinski, P. P. and Wandurska-Nowak, E. (2012). Hymenolepis diminuta: analysis of the expression of Toll-like receptor genes (TLR2 and TLR4) in the small and large intestines of rats. Experimental Parasitology 130, 261–266. doi: 10.1016/j.exppara.2011.12.002.Google Scholar
Kostic, A. D., Gevers, D., Pedamallu, C. S., Michaud, M., Duke, F., Earl, A. M., Ojesina, A. I., Jung, J., Bass, A. J., Tabernero, J., Baselga, J., Liu, C., Shivdasani, R. A., Ogino, S., Birren, B. W., Huttenhower, C., Garrett, W. S. and Meyerson, M. (2012). Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Research 22, 292–298. doi: 10.1101/gr.126573.111.Google Scholar
Kumar, A., Wu, H., Collier-Hyams, L. S., Hansen, J. M., Li, T., Yamoah, K., Pan, Z. Q., Jones, D. P. and Neish, A. S. (2007). Commensal bacteria modulate cullin-dependent signaling via generation of reactive oxygen species. European Molecular Biology Organization Journal 26, 4457–4466. doi: 10.1038/sj.emboj.7601867.Google Scholar
Lakhdari, O., Tap, J., Béguet-Crespel, F., Le Roux, K., de Wouters, T., Cultrone, A., Nepelska, M., Lefèvre, F., Doré, J. and Blottière, H. M. (2011). Identification of NFkB modulation capabilities within human intestinal commensal bacteria. Journal of Biomedicine and Biotechnology 2011, 1–9. doi: 10.1155/2011/282356.Google Scholar
Larsen, J. M., Steen-Jensen, D. B., Laursen, J. M., Søndergaard, J. N., Musavian, H. S., Butt, T. M. and Brix, S. (2012). Divergent pro-inflammatory profile of human dendritic cells in response to commensal and pathogenic bacteria associated with the airway microbiota. PLOS ONE 7, e31976. doi: 10.1371/journal.pone.0031976.Google Scholar
Lawley, T. D. and Walker, A. W. (2013). Intestinal colonization resistance. Immunology 138, 1–11. doi: 10.1111/j.1365-2567.2012.03616.x.Google Scholar
LeBlanc, J. G., Milani, C., de Giori, G. S., Sesma, F., van Sinderen, D. and Ventura, M. (2013). Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Current Opinion in Biotechnology 24, 160–168. doi: 10.1016/j.copbio.2012.08.005.Google Scholar
Lee, G.-H., Kumar, S., Lee, J.-H., Chang, D.-H., Kim, D.-S., Choi, S.-H., Rhee, M.-S., Lee, D.-W., Yoon, M.-H. and Kim, B.-C. (2012). Genome sequence of Oscillibacter ruminantium strain GH1, isolated from rumen of Korean native cattle. Journal of Bacteriology 194, 6362. doi: 10.1128/jb.01677-12.Google Scholar
Leung, J. M. and Loke, P. (2013). A role for IL-22 in the relationship between intestinal helminths, gut microbiota and mucosal immunity. International Journal for Parasitology 43, 253–257. doi: 10.1016/j.ijpara.2012.10.015.CrossRefGoogle ScholarPubMed
Ley, R. E., Bäckhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D. and Gordon, J. I. (2005). Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences USA 102, 11070–11075. doi: 10.1073/pnas.0504978102.CrossRefGoogle ScholarPubMed
Ley, R. E., Peterson, D. A. and Gordon, J. I. (2006 a). Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837–848. doi: 10.1016/j.cell.2006.02.017.Google Scholar
Ley, R. E., Turnbaugh, P. J., Klein, S. and Gordon, J. I. (2006 b). Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023. doi: 10.1038/4441022a.Google Scholar
Li, R. W., Wu, S., Li, W., Navarro, K., Couch, R. D., Hill, D. and Urban, J. F. Jr. (2012). Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis . Infection and Immunity 80, 2150–2157. doi: 10.1128/iai.00141-12.Google Scholar
Liang, S. C., Tan, X.-Y., Luxenberg, D. P., Karim, R., Dunussi-Joannopoulos, K., Collins, M. and Fouser, L. A. (2006). Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. Journal of Experimental Medicine 203, 2271–2279. doi: 10.1084/jem.20061308.Google Scholar
Lin, P. W., Myers, L. E. S., Ray, L., Song, S.-C., Nasr, T. R., Berardinelli, A. J., Kundu, K., Murthy, N., Hansen, J. M. and Neish, A. S. (2009). Lactobacillus rhamnosus blocks inflammatory signaling in vivo via reactive oxygen species generation. Free Radical Biology and Medicine 47, 1205–1211. doi: 10.1016/j.freeradbiomed.2009.07.033.CrossRefGoogle ScholarPubMed
Lorvik, K. B., Haabeth, O. A. W., Clancy, T., Bogen, B. and Corthay, A. (2013). Molecular profiling of tumor-specific Th1 cells activated in vivo . Oncoimmunology 2, e24383. doi: 10.4161/onci.24383.Google Scholar
Louis, P. and Flint, H. J. (2009). Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. Federation of European Microbiological Societies Microbiology Letters 294, 1–8. doi: 10.1111/j.1574-6968.2009.01514.x.Google Scholar
Lwanga, F., Kirunda, B. E. and Orach, C. G. (2012). Intestinal helminth infections and nutritional status of children attending primary schools in Wakiso district, Central Uganda. International Journal of Environmental Research and Public Health 9, 2910–2921. doi: 10.3390/ijerph9082910.Google Scholar
Macho Fernandez, E., Valenti, V., Rockel, C., Hermann, C., Pot, B., Boneca, I. G. and Grangette, C. (2011). Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 60, 1050–1059. doi: 10.1136/gut.2010.232918.Google Scholar
MacRae, J. C. (1993). Metabolic consequences of intestinal parasitism. Proceedings of the Nutrition Society 52, 121–130. doi: 10.1079/PNS19930044.Google Scholar
Mahmoud, A. A. F. (2001). Schistosomiasis. Imperial College Press, London, UK.Google Scholar
Manco, M., Putignani, L. and Bottazzo, G. F. (2010). Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocrine Reviews 31, 817–844. doi: 10.1210/er.2009-0030.Google Scholar
Mañé, J., Lorén, V., Pedrosa, E., Ojanguren, I., Xaus, J., Cabré, E., Domènech, E. and Gassull, M. A. (2009). Lactobacillus fermentum CECT 5716 prevents and reverts intestinal damage on TNBS-induced colitis in mice. Inflammatory Bowel Diseases 15, 1155–1163. doi: 10.1002/ibd.20908.Google Scholar
Mansfield, L. S. and Urban, J. F. Jr. (1996). The pathogenesis of necrotic proliferative colitis in swine is linked to whipworm induced suppression of mucosal immunity to resident bacteria. Veterinary Immunology and Immunopathology 50, 1–17. doi: 10.1016/0165-2427(95)05482-0.Google Scholar
Mariat, D., Firmesse, O., Levenez, F., Guimarăes, V., Sokol, H., Doré, J., Corthier, G. and Furet, J.-P. (2009). The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BioMed Central Microbiology 9, 123. doi: 10.1186/1471-2180-9-123.Google Scholar
Marteau, P., Pochart, P., Doré, J., Béra-Maillet, C., Bernalier, A. and Corthier, G. (2001). Comparative study of bacterial groups within the human cecal and fecal microbiota. Applied and Environmental Microbiology 67, 4939–4942. doi: 10.1128/aem.67.10.4939-4942.2001.Google Scholar
Martinez-Medina, M., Aldeguer, X., Gonzalez-Huix, F., Acero, D. and Garcia-Gil, L. J. (2006). Abnormal microbiota composition in the ileocolonic mucosa of Crohn's disease patients as revealed by polymerase chain reaction-denaturing gradient gel electrophoresis. Inflammatory Bowel Diseases 12, 1136–1145. doi: 10.1097/01.mib.0000235828.09305.0c.Google Scholar
Maslowski, K. M., Vieira, A. T., Ng, A., Kranich, J., Sierro, F., Yu, D., Schilter, H. C., Rolph, M. S., Mackay, F., Artis, D., Xavier, R. J., Teixeira, M. M. and Mackay, C. R. (2009). Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461, 1282–1286. doi: 10.1038/nature08530.Google Scholar
Maurice, C. F., Haiser, H. J. and Turnbaugh, P. J. (2013). Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 152, 39–50. doi: 10.1016/j.cell.2012.10.052.Google Scholar
McAuley, J. L., Linden, S. K., Png, C. W., King, R. M., Pennington, H. L., Gendler, S. J., Florin, T. H., Hill, G. R., Korolik, V. and McGuckin, M. A. (2007). MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. Journal of Clinical Investigation 117, 2313–2324. doi: 10.1172/jci26705.Google Scholar
McKenna, P., Hoffmann, C., Minkah, N., Aye, P. P., Lackner, A., Liu, Z., Lozupone, C. A., Hamady, M., Knight, R. and Bushman, F. D. (2008). The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLOS Pathogens 4, e20. doi: 10.1371/journal.ppat.0040020.Google Scholar
McSorley, H. J. and Maizels, R. M. (2012). Helminth infections and host immune regulation. Clinical Microbiology Reviews 25, 585–608. doi: 10.1128/cmr.05040-11.Google Scholar
McSorley, H. J., Gaze, S., Daveson, J., Jones, D., Anderson, R. P., Clouston, A., Ruyssers, N. E., Speare, R., McCarthy, J. S., Engwerda, C. R., Croese, J. and Loukas, A. (2011). Suppression of inflammatory immune responses in celiac disease by experimental hookworm infection. PLOS ONE 6, e24092. doi: 10.1371/journal.pone.0024092.Google Scholar
Monira, S., Nakamura, S., Gotoh, K., Izutsu, K., Watanabe, H., Alam, N. H., Nakaya, T., Horii, T., Ali, S. I., Iida, T. and Alan, M. (2013). Metagenomic profile of gut microbiota in children during cholera and recovery. Gut Pathogens 5, 1. doi: 10.1186/1757-4749-5-1.Google Scholar
Muller, R. (2001). Worms and Human Disease, 2nd Edn. CABI Publishing, Wallingford, UK.Google Scholar
Niess, J. H. and Reinecker, H.-C. (2005). Lamina propria dendritic cells in the physiology and pathology of the gastrointestinal tract. Current Opinion in Gastroenterology 21, 687–691. doi: 10.1097/01.mog.0000181710.96904.58.Google Scholar
Odogwu, S. E., Ramamurthy, N. K., Kabatereine, N. B., Kazibwe, F., Tukahebwa, E., Webster, J. P., Fenwick, A. and Stothard, J. R. (2006). Schistosoma mansoni in infants (aged <3 years) along the Ugandan shoreline of Lake Victoria. Annals of Tropical Medicine and Parasitology 100, 315–326. doi: 10.1179/136485906×105552.Google Scholar
Onguru, D., Liang, Y., Griffith, Q., Nikolajczyk, B., Mwinzi, P. and Ganley-Leal, L. (2011). Human schistosomiasis is associated with endotoxemia and Toll-like receptor 2- and 4-bearing B cells. American Journal of Tropical Medicine and Hygiene 84, 321–324. doi: 10.4269/ajtmh.2011.10-0397.Google Scholar
Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A. and Brown, P. O. (2007). Development of the human infant intestinal microbiota. PLOS Biology 5, e177. doi: 10.1371/journal.pbio.0050177.Google Scholar
Pandey, A., Bringel, F. and Meyer, J.-M. (1994). Iron requirement and search for siderophores in lactic acid bacteria. Applied Microbiology and Biotechnology 40, 735–739. doi: 10.1007/bf00173337.Google Scholar
Parfrey, L. W., Walters, W. A. and Knight, R. (2011). Microbial eukaryotes in the human microbiome: ecology, evolution, and future directions. Frontiers in Microbiology 2, 153. doi: 10.3389/fmicb.2011.00153.Google Scholar
Philpott, D. J. and Girardin, S. E. (2004). The role of Toll-like receptors and Nod proteins in bacterial infection. Molecular Immunology 41, 1099–1108. doi: 10.1016/j.molimm.2004.06.012.Google Scholar
Plieskatt, J. L., Deenonpoe, R., Mulvenna, J. P., Krause, L., Sripa, B., Bethony, J. M. and Brindley, P. J. (2013). Infection with the carcinogenic liver fluke Opisthorchis viverrini modifies intestinal and biliary microbiome. Journal of the Federation of American Societies for Experimental Biology 27, 4572–4584. doi: 10.1096/fj.13-232751.Google Scholar
Polderman, A. M., Krepel, H. P., Baeta, S., Blotkamp, J. and Gigase, P. (1991). Oesophagostomiasis, a common infection of man in northern Togo and Ghana. American Journal of Tropical Medicine and Hygiene 44, 336–344.Google Scholar
Preston, C. M. and Jenkins, T. (1985). Trichuris muris: structure and formation of the egg polar plugs. Parasitology Research 71, 373–381. doi: 10.1007/bf00928339.Google Scholar
Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., Yamada, T., Mende, D. R., Li, J., Xu, J., Li, S., Li, D., Cao, J., Wang, B., Liang, H., Zheng, H., Xie, Y., Tap, J., Lepage, P., Bertalan, M., Batto, J.-M., Hansen, T., Le Paslier, D., Linneberg, A., Nielsen, H. B., Pelletier, E., Renault, P., Sicheritz-Ponten, T., Turner, K., Zhu, H., Yu, C., Li, S., Jian, M., Zhou, Y., Li, Y., Zhang, X., Li, S., Qin, N., Yang, H., Wang, J., Brunak, S., Doré, J., Guarner, F., Kristiansen, K., Pedersen, O., Parkhill, J., Weissenbach, J., MetaHIT Consortium, Bork, P., Ehrlich, S. D. and Wang, J. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65. doi: 10.1038/nature08821.Google Scholar
Rajilić-Stojanović, M., Smidt, H. and de Vos, W. M. (2007). Diversity of the human gastrointestinal tract microbiota revisited. Environmental Microbiology 9, 2125–2136. doi: 10.1111/j.1462-2920.2007.01369.x.Google Scholar
Ramirez-Farias, C., Slezak, K., Fuller, Z., Duncan, A., Holtrop, G. and Louis, P. (2009). Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii . British Journal of Nutrition 101, 541–550. doi: 10.1017/S0007114508019880.Google Scholar
Reinhardt, C., Bergentall, M., Greiner, T. U., Schaffner, F., Östergren-Lundén, G., Petersen, L. C., Ruf, W. and Bäckhed, F. (2012). Tissue factor and PAR1 promote microbiota-induced intestinal vascular remodelling. Nature 483, 627–631. doi: 10.1038/nature10893.Google Scholar
Reissbrodt, R. and Rabsch, W. (1988). Further differentiation of Enterobacteriaceae by means of siderophore-pattern analysis. Zentralblatt für Bakteriologie, Mikrobiologie und Hygiene. Series A: Medical Microbiology, Infectious Diseases, Virology, Parasitology 268, 306–317. doi: 10.1016/S0176-6724(88)80015-4.CrossRefGoogle ScholarPubMed
Rizzetto, L., Buschow, S. I., Beltrame, L., Figdor, C. G., Schierer, S., Schuler, G. and Cavalieri, D. (2012). The modular nature of dendritic cell responses to commensal and pathogenic fungi. PLOS ONE 7, e42430. doi: 10.1371/journal.pone.0042430.Google Scholar
Round, J. L. and Mazmanian, S. K. (2010). Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proceedings of the National Academy of Sciences USA 107, 12204–12209. doi: 10.1073/pnas.0909122107.Google Scholar
Rutter, J. M. and Beer, R. J. (1975). Synergism between Trichuris suis and the microbial flora of the large intestine causing dysentery in pigs. Infection and Immunity 11, 395–404.Google Scholar
Sabat, R., Witte, E., Witte, K. and Wolk, K. (2013). IL-22 and IL-17: an overview. In IL-17, IL-22 and Their Producing Cells: Role in Inflammation and Autoimmunity (ed. Quesniaux, V., Ryffel, B. and Padova, F.), pp. 11–35. Springer, Basel, Switzerland.Google Scholar
Sayin, S. I., Wahlström, A., Felin, J., Jäntti, S., Marschall, H.-U., Bamberg, K., Angelin, B., Hyötyläinen, T., Orešič, M. and Bäckhed, F. (2013). Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metabolism 17, 225–235. doi: 10.1016/j.cmet.2013.01.003.Google Scholar
Scales, B. S. and Huffnagle, G. B. (2013). The microbiome in wound repair and tissue fibrosis. Journal of Pathology 229, 323–331. doi: 10.1002/path.4118.Google Scholar
Schulz, S. M., Köhler, G., Schütze, N., Knauer, J., Straubinger, R. K., Chackerian, A. A., Witte, E., Wolk, K., Sabat, R., Iwakura, Y., Holscher, C., Müller, U., Kastelein, R. A. and Alber, G. (2008). Protective immunity to systemic infection with attenuated Salmonella enterica serovar Enteritidis in the absence of IL-12 is associated with IL-23-dependent IL-22, but not IL-17. Journal of Immunology 181, 7891–7901.Google Scholar
Sekirov, I., Russell, S. L., Antunes, L. C. M. and Finlay, B. B. (2010). Gut microbiota in health and disease. Physiological Reviews 90, 859–904. doi: 10.1152/physrev.00045.2009.Google Scholar
Sharon, I., Morowitz, M. J., Thomas, B. C., Costello, E. K., Relman, D. A. and Banfield, J. F. (2013). Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Research 23, 111–120. doi: 10.1101/gr.142315.112.Google Scholar
Shimazu, T., Villena, J., Tohno, M., Fujie, H., Hosoya, S., Shimosato, T., Aso, H., Suda, Y., Kawai, Y., Saito, T., Makino, S., Ikegami, S., Itoh, H. and Kitazawa, H. (2012). Immunobiotic Lactobacillus jensenii elicits anti-inflammatory activity in porcine intestinal epithelial cells by modulating negative regulators of the Toll-like receptor signaling pathway. Infection and Immunity 80, 276–288. doi: 10.1128/iai.05729-11.Google Scholar
Shin, J. L., Gardiner, G. W., Deitel, W. and Kandel, G. (2004). Does whipworm increase the pathogenicity of Campylobacter jejuni: a clinical correlate of an experimental observation. Canadian Journal of Gastroenterology=Journal Canadien de Gastroenterologie 18, 175–177.Google Scholar
Smith, M. I., Yatsunenko, T., Manary, M. J., Trehan, I., Mkakosya, R., Cheng, J., Kau, A. L., Rich, S. S., Concannon, P., Mychaleckyj, J. C., Liu, J., Houpt, E., Li, J. V., Holmes, E., Nicholson, J., Knights, D., Ursell, L. K., Knight, R. and Gordon, J. I. (2013). Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339, 548–554. doi: 10.1126/science.1229000.Google Scholar
Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermúdez-Humarán, L. G., Gratadoux, J. J., Blugeon, S., Bridonneau, C., Furet, J. P., Corthier, G., Grangette, C., Vasquez, N., Pochart, P., Trugnan, G., Thomas, G., Blottière, H. M., Doré, J., Marteau, P., Seksik, P. and Langella, P. (2008). Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proceedings of the National Academy of Sciences USA 105, 16731–16736. doi: 10.1073/pnas.0804812105.Google Scholar
Stecher, B., Robbiani, R., Walker, A. W., Westendorf, A. M., Barthel, M., Kremer, M., Chaffron, S., Macpherson, A. J., Buer, J., Parkhill, J., Dougan, G., von Mering, C. and Hardt, W.-D. (2007). Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLOS Biology 5, e244. doi: 10.1371/journal.pbio.0050244.Google Scholar
Stephenson, L. S., Latham, M. C. and Ottesen, E. A. (2000). Malnutrition and parasitic helminth infections. Parasitology 121, S23–S38. doi: 10.1017/S0031182000006491.Google Scholar
Stevenson, D. M. and Weimer, P. J. (2007). Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Applied Microbiology and Biotechnology 75, 165–174. doi: 10.1007/s00253-006-0802-y.Google Scholar
Stothard, J. R., Sousa-Figueiredo, J. C., Betson, M., Bustinduy, A. and Reinhard-Rupp, J. (2013). Schistosomiasis in African infants and preschool children: let them now be treated! Trends in Parasitology 29, 197–205. doi: 10.1016/j.pt.2013.02.001.Google Scholar
Summers, R. W., Elliott, D. E., Urban, J. F. Jr., Thompson, R. and Weinstock, J. V. (2005 a). Trichuris suis therapy in Crohn's disease. Gut 54, 87–90. doi: 10.1136/gut.2004.041749.Google Scholar
Summers, R. W., Elliott, D. E., Urban, J. F. Jr., Thompson, R. A. and Weinstock, J. V. (2005 b). Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128, 825–832. doi: 10.1053/j.gastro.2005.01.005.Google Scholar
Sutherland, R. E., Xu, X., Kim, S. S., Seeley, E. J., Caughey, G. H. and Wolters, P. J. (2011). Parasitic infection improves survival from septic peritonitis by enhancing mast cell responses to bacteria in mice. PLOS ONE 6, e27564. doi: 10.1371/journal.pone.0027564.Google Scholar
Swidsinski, A., Dörffel, Y., Loening-Baucke, V., Tertychnyy, A., Biche-ool, S., Stonogin, S., Guo, Y. and Sun, N.-D. (2012). Mucosal invasion by fusobacteria is a common feature of acute appendicitis in Germany, Russia, and China. Saudi Journal of Gastroenterology 18, 55–58. doi: 10.4103/1319-3767.91734.Google Scholar
Symons, L. E. A. (1985). Anorexia: occurrence, pathophysiology and possible causes in parasitic infections. Advances in Parasitology 24, 103–133. doi: 10.1016/S0065-308X(08)60562-X.Google Scholar
Tremaroli, V. and Bäckhed, F. (2012). Functional interactions between the gut microbiota and host metabolism. Nature 489, 242–249. doi: 10.1038/nature11552.Google Scholar
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., Egholm, M., Henrissat, B., Heath, A. C., Knight, R. and Gordon, J. I. (2009). A core gut microbiome in obese and lean twins. Nature 457, 480–484. doi: 10.1038/nature07540.Google Scholar
van Baarlen, P., Wells, J. M. and Kleerebezem, M. (2013). Regulation of intestinal homeostasis and immunity with probiotic lactobacilli. Trends in Immunology 34, 208–215. doi: 10.1016/j.it.2013.01.005.Google Scholar
van Nimwegen, F. A., Penders, J., Stobberingh, E. E., Postma, D. S., Koppelman, G. H., Kerkhof, M., Reijmerink, N. E., Dompeling, E., van den Brandt, P. A., Ferreira, I., Mommers, M. and Thijs, C. (2011). Mode and place of delivery, gastrointestinal microbiota, and their influence on asthma and atopy. Journal of Allergy and Clinical Immunology 128, 948–955. doi: 10.1016/j.jaci.2011.07.027.Google Scholar
Walk, S. T., Blum, A. M., Ewing, S. A.-S., Weinstock, J. V. and Young, V. B. (2010). Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus . Inflammatory Bowel Diseases 16, 1841–1849. doi: 10.1002/ibd.21299.Google Scholar
Wang, T., Cai, G., Qiu, Y., Fei, N., Zhang, M., Pang, X., Jia, W., Cai, S. and Zhao, L. (2011 a). Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME Journal 6, 320–329. doi: 10.1038/ismej.2011.109.Google Scholar
Wang, Y., Holmes, E., Nicholson, J. K., Cloarec, O., Chollet, J., Tanner, M., Singer, B. H. and Utzinger, J. (2004). Metabonomic investigations in mice infected with Schistosoma mansoni: an approach for biomarker identification. Proceedings of the National Academy of Sciences USA 101, 12676–12681. doi: 10.1073/pnas.0404878101.Google Scholar
Wang, Y., Xiao, S.-H., Xue, J., Singer, B. H., Utzinger, J. and Holmes, E. (2009). Systems metabolic effects of a Necator americanus infection in Syrian hamster. Journal of Proteome Research 8, 5442–5450. doi: 10.1021/pr900711j.Google Scholar
Wang, Y.-D., Chen, W.-D., Yu, D., Forman, B. M. and Huang, W. (2011 b). The G-Protein-coupled bile acid receptor, Gpbar1 (TGR5), negatively regulates hepatic inflammatory response through antagonizing nuclear factor kappa light-chain enhancer of activated B cells (NF-κB) in mice. Hepatology 54, 1421–1432. doi: 10.1002/hep.24525.Google Scholar
Wescott, R. B. (1968). Experimental Nematospiroides dubius infection in germfree and conventional mice. Experimental Parasitology 22, 245–249. doi: 10.1016/0014-4894(68)90099-4.Google Scholar
Wilson, M. S., Feng, C. G., Barber, D. L., Yarovinsky, F., Cheever, A. W., Sher, A., Grigg, M., Collins, M., Fouser, L. and Wynn, T. A. (2010). Redundant and pathogenic roles for IL-22 in mycobacterial, protozoan, and helminth infections. Journal of Immunology 184, 4378–4390. doi: 10.4049/jimmunol.0903416.Google Scholar
Wolk, K., Kunz, S., Witte, E., Friedrich, M., Asadullah, K. and Sabat, R. (2004). IL-22 increases the innate immunity of tissues. Immunity 21, 241–254. doi: 10.1016/j.immuni.2004.07.007.Google Scholar
Woolhouse, M. E. J. (1998). Patterns in parasite epidemiology: the peak shift. Parasitology Today 14, 428–434. doi: 10.1016/S0169-4758(98)01318-0.Google Scholar
World Health Organization (2012). Soil-Transmitted Helminth Infections. Fact Sheet No. 336. World Health Organisation, Geneva, Switzerland.Google Scholar
Wu, S., Li, R. W., Li, W., Beshah, E., Dawson, H. D. and Urban, J. F. Jr. (2012). Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLOS ONE 7, e35470. doi: 10.1371/journal.pone.0035470.Google Scholar
Yang, Y., Van den Broeck, J. and Wein, L. M. (2013). Ready-to-use food-allocation policy to reduce the effects of childhood undernutrition in developing countries. Proceedings of the National Academy of Sciences USA 110, 4545–4550. doi: 10.1073/pnas.1216075110.Google Scholar
Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., Heath, A. C., Warner, B., Reeder, J., Kuczynski, J., Caporaso, J. G., Lozupone, C. A., Lauber, C., Clemente, J. C., Knights, D., Knight, R. and Gordon, J. I. (2012). Human gut microbiome viewed across age and geography. Nature 486, 222–227. doi: 10.1038/nature11053.Google Scholar
Yu, S.-H., Jiang, Z.-X. and Xu, L.-Q. (1995). Infantile hookworm disease in China. A review. Acta Tropica 59, 265–270. doi: 10.1016/0001-706X(95)00089-W.Google Scholar
Yu, Z.-T., Chen, C., Kling, D. E., Liu, B., McCoy, J. M., Merighi, M., Heidtman, M. and Newburg, D. S. (2013). The principal fucosylated oligosaccharides of human milk exhibit prebiotic properties on cultured infant microbiota. Glycobiology 23, 169–177. doi: 10.1093/glycob/cws138.Google Scholar
Zhang, C. H., Zhang, M. H., Wang, S. Y., Han, R. J., Cao, Y. F., Hua, W. Y., Mao, Y. J., Zhang, X. J., Pang, X. Y., Wei, C. C., Zhao, G. P., Chen, Y. and Zhao, L. P. (2010). Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME 4, 232–241. doi: 10.1038/ismej.2009.112.Google Scholar
Zheng, Y., Valdez, P. A., Danilenko, D. M., Hu, Y., Sa, S. M., Gong, Q., Abbas, A. R., Modrusan, Z., Ghilardi, N., de Sauvage, F. J. and Ouyang, W. (2008). Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nature Medicine 14, 282–289. doi: 10.1038/nm1720.Google Scholar
Zimmermann, M. B., Chassard, C., Rohner, F., N'Goran, E. K., Nindjin, C., Dostal, A., Utzinger, J., Ghattas, H., Lacroix, C. and Hurrell, R. F. (2010). The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Côte d'Ivoire. American Journal of Clinical Nutrition 92, 1406–1415. doi: 10.3945/ajcn.110.004564.Google Scholar
Zupancic, M. L., Cantarel, B. L., Liu, Z., Drabek, E. F., Ryan, K. A., Cirimotich, S., Jones, C., Knight, R., Walters, W. A., Knights, D., Mongodin, E. F., Horenstein, R. B., Mitchell, B. D., Steinle, N., Snitker, S., Shuldiner, A. R. and Fraser, C. M. (2012). Analysis of the gut microbiota in the old order Amish and its relation to the metabolic syndrome. PLOS ONE 7, e43052. doi: 10.1371/journal.pone.0043052.Google Scholar