Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-25T22:11:22.428Z Has data issue: false hasContentIssue false
  • English
  • Français

Helminths and microbes within the vertebrate gut – not all studies are created equal

Published online by Cambridge University Press:  31 July 2019

Alba Cortés ,
Laura E. Peachey ,
Timothy P. Jenkins ,
Riccardo Scotti  and
Cinzia Cantacessi Open the ORCID record for Cinzia Cantacessi [Opens in a new window]
Alba Cortés
Affiliation:
Department of Veterinary Medicine, University of Cambridge, Madingley Road CB3 0ES, Cambridge, UK
Laura E. Peachey
Affiliation:
Department of Veterinary Medicine, University of Cambridge, Madingley Road CB3 0ES, Cambridge, UK Bristol Veterinary School, Faculty of Health Sciences, University of Bristol, Langford House, Langford, BS40 5DU, Bristol, UK
Timothy P. Jenkins
Affiliation:
Department of Veterinary Medicine, University of Cambridge, Madingley Road CB3 0ES, Cambridge, UK
Riccardo Scotti
Affiliation:
Department of Veterinary Medicine, University of Cambridge, Madingley Road CB3 0ES, Cambridge, UK
Cinzia Cantacessi*
Affiliation:
Department of Veterinary Medicine, University of Cambridge, Madingley Road CB3 0ES, Cambridge, UK
*
Author for correspondence: Cinzia Cantacessi, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The multifaceted interactions occurring between gastrointestinal (GI) parasitic helminths and the host gut microbiota are emerging as a key area of study within the broader research domain of host-pathogen relationships. Over the past few years, a wealth of investigations has demonstrated that GI helminths interact with the host gut flora, and that such interactions result in modifications of the host immune and metabolic statuses. Nevertheless, whilst selected changes in gut microbial composition are consistently observed in response to GI helminth infections across several host-parasite systems, research in this area to date is largely characterised by inconsistent findings. These discrepancies are particularly evident when data from studies of GI helminth-microbiota interactions conducted in humans from parasite-endemic regions are compared. In this review, we provide an overview of the main sources of variance that affect investigations on helminth-gut microbiota interactions in humans, and propose a series of methodological approaches that, whilst accounting for the inevitable constraints of fieldwork, are aimed at minimising confounding factors and draw biologically meaningful interpretations from highly variable datasets.

Keywords

Helminth-microbiota interactionssoil-transmitted helminthsanthelminticsbacterial 16S rRNA sequencingconfounding factors
Type
Review Article
Information
Parasitology , Volume 146 , Issue 11 , September 2019 , pp. 1371 - 1378
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Almeida, A, Mitchell, AL, Tarkowska, A and Finn, RD (2018) Benchmarking taxonomic assignments based on 16S rRNA gene profiling of the microbiota from commonly sampled environments. GigaScience 7, 1–10.Google Scholar
Barbour, AD and Kafetzaki, M (1991) Modeling the overdispersion of parasite loads. Mathematical Biosciences 107, 249–253.Google Scholar
Broadhurst, MJ, Ardeshir, A, Kanwar, B, Mirpuri, J, Gundra, UM, Leung, JM, Wiens, KE, Vujkovic-Cvijin, I, Kim, CC, Yarovinsky, F, Lerche, NW, McCune, JM 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.Google Scholar
Brosschot, TP and Reynolds, LA (2018) The impact of a helminth-modified microbiome on host immunity. Mucosal Immunology 11, 1039–1046.Google Scholar
Campbell, SJ, Biritwum, NK, Woods, G, Velleman, Y, Fleming, F and Stothard, JR (2018) Tailoring water, sanitation, and hygiene (WASH) targets for soil-transmitted helminthiasis and schistosomiasis control. Trends in Parasitology 34, 53–63.Google Scholar
Cantacessi, C, Giacomin, P, Croese, J, Zakrzewski, M, Sotillo, J, McCann, L, Nolan, MJ, Mitreva, M, Krause, L and Loukas, A (2014) Impact of experimental hookworm infection on the human gut microbiota. The Journal of Infectious Diseases 210, 1431–1434.Google Scholar
Cattadori, IM, Sebastian, A, Hao, H, Katani, R, Albert, I, Eilertson, KE, Kapur, V, Pathak, A and Mitchell, S (2016) Impact of helminth infections and nutritional constraints on the small intestine microbiota. PLoS One 11, e0159770.Google Scholar
Chabé, M, Lokmer, A and Segurel, L (2017) Gut protozoa: friends or foes of the human gut microbiota? Trends in Parasitology 33, 925–934.Google Scholar
Churcher, TS, Ferguson, NM and Basáñez, MG (2005) Density dependence and overdispersion in the transmission of helminth parasites. Parasitology 131(Pt 1), 121–132.Google Scholar
Cliffe, LJ and Grencis, RK (2004) The Trichuris muris system: a paradigm of resistance and susceptibility to intestinal nematode infection. Advances in Parasitology 57, 255–307.Google Scholar
Cooper, P, Walker, AW, Reyes, J, Chico, M, Salter, SJ, 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.Google Scholar
Cortés, A, Toledo, R and Cantacessi, C (2018) Classic models for new perspectives: delving into helminth-microbiota-immune system interactions. Trends in Parasitology 34, 640–654.Google Scholar
Cortés, A, Wills, J, Su, X, Hewitt, R, Scotti, R, Robertson, J, Price, DRG, Bartley, Y, McNeilly, TN, Krause, L, Powell, JJ, Nisbet, AJ, Cantacessi, C (Submitted) Infection with the gastrointestinal nematode Teladorsagia circumcincta increases tissue T cell numbers and luminal pathobionts.Google Scholar
Costea, PI, Zeller, G, Sunagawa, S, Pelletier, E, Alberti, A, Levenez, F, Tramontano, M, Driessen, M, Hercog, R, Jung, FE, Kultima, JR, Hayward, MR, Coelho, LP, Allen-Vercoe, E, Bertrand, L, Blaut, M, Brown, JRM, Carton, T, Cools-Portier, S, Daigneault, M, Derrien, M, Druesne, A, de Vos, WM, Finlay, BB, Flint, HJ, Guarner, F, Hattori, M, Heilig, H, Luna, RA, van Hylckama Vlieg, J, Junick, J, Klymiuk, I, Langella, P, Le Chatelier, E, Mai, V, Manichanh, C, Martin, JC, Mery, C, Morita, H, O'Toole, PW, Orvain, C, Patil, KR, Penders, J, Persson, S, Pons, N, Popova, M, Salonen, A, Saulnier, D, Scott, KP, Singh, B, Slezak, K, Veiga, P, Versalovic, J, Zhao, L, Zoetendal, EG, Ehrlich, SD, Dore, J and Bork, P (2017) Towards standards for human fecal sample processing in metagenomic studies. Nature Biotechnology 35, 1069–1076.Google Scholar
De Nardi, R, Marchesini, G, Li, S, Khafipour, E, Plaizier, KJ, Gianesella, M, Ricci, R, Andrighetto, I and Segato, S (2016) Metagenomic analysis of rumen microbial population in dairy heifers fed a high grain diet supplemented with dicarboxylic acids or polyphenols. BMC Veterinary Research 12, 29.Google Scholar
Duarte, AM, Jenkins, TP, Latrofa, MS, Giannelli, A, Papadopoulos, E, de Carvalho, LM, Nolan, MJ, Otranto, D and Cantacessi, C (2016) Helminth infections and gut microbiota – a feline perspective. Parasites & Vectors 9, 625.Google Scholar
Giacomin, P, Zakrzewski, M, Croese, J, Su, X, Sotillo, J, McCann, L, Navarro, S, Mitreva, M, Krause, L, Loukas, A and Cantacessi, C (2015) Experimental hookworm infection and escalating gluten challenges are associated with increased microbial richness in celiac subjects. Scientific Reports 5, 13797.Google Scholar
Giacomin, P, Zakrzewski, M, Jenkins, TP, Su, X, Al-Hallaf, R, Croese, J, de Vries, S, Grant, A, Mitreva, M, Loukas, A, Krause, L and Cantacessi, C (2016) Changes in duodenal tissue-associated microbiota following hookworm infection and consecutive gluten challenges in humans with coeliac disease. Scientific Reports 6, 36797.Google Scholar
Glendinning, L, Nausch, N, Free, A, Taylor, DW and Mutapi, F (2014) The microbiota and helminths: sharing the same niche in the human host. Parasitology 141, 1255–1271.Google Scholar
Golob, JL, Margolis, E, Hoffman, NG and Fredricks, DN (2017) Evaluating the accuracy of amplicon-based microbiome computational pipelines on simulated human gut microbial communities. BMC Bioinformatics 18, 283.Google Scholar
Greetham, HL, Gibson, GR, Giffard, C, Hippe, H, Merkhoffer, B, Steiner, U, Falsen, E and Collins, MD (2004) Allobaculum stercoricanis gen. nov., sp. nov., isolated from canine feces. Anaerobe 10, 301–307.Google Scholar
Holm, JB, Sorobetea, D, Kiilerich, P, Ramayo-Caldas, Y, Estelle, J, Ma, T, Madsen, L, Kristiansen, K and Svensson-Frej, M (2015) Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of Lactobacilli. PLoS One 10, e0125495.Google Scholar
Hotez, PJ, Alvarado, M, Basanez, MG, Bolliger, I, Bourne, R, Boussinesq, M, Brooker, SJ, Brown, AS, Buckle, G, Budke, CM, Carabin, H, Coffeng, LE, Fevre, EM, Furst, T, Halasa, YA, Jasrasaria, R, Johns, NE, Keiser, J, King, CH, Lozano, R, Murdoch, ME, O'Hanlon, S, Pion, SD, Pullan, RL, Ramaiah, KD, Roberts, T, Shepard, DS, Smith, JL, Stolk, WA, Undurraga, EA, Utzinger, J, Wang, M, Murray, CJ and Naghavi, M (2014) The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Neglected Tropical Diseases 8, e2865.Google Scholar
Houlden, A, Hayes, KS, Bancroft, AJ, Worthington, JJ, Wang, P, Grencis, RK and Roberts, IS (2015) Chronic Trichuris muris infection in C57BL/6 mice causes significant changes in host microbiota and metabolome: effects reversed by pathogen clearance. PLoS One 10, e0125945.Google Scholar
Jenkins, TP, Rathnayaka, Y, Perera, PK, Peachey, LE, Nolan, MJ, Krause, L, Rajakaruna, RS and Cantacessi, C (2017) Infections by human gastrointestinal helminths are associated with changes in faecal microbiota diversity and composition. PLoS One 12, e0184719.Google Scholar
Jenkins, TP, Peachey, LE, Ajami, NJ, MacDonald, AS, Hsieh, MH, Brindley, PJ, Cantacessi, C and Rinaldi, G (2018a) Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota. Scientific Reports 8, 12072.Google Scholar
Jenkins, TP, Formenti, F, Castro, C, Piubelli, C, Perandin, F, Buonfrate, D, Otranto, D, Griffin, JL, Krause, L, Bisoffi, Z and Cantacessi, C (2018b) A comprehensive analysis of the faecal microbiome and metabolome of Strongyloides stercoralis infected volunteers from a non-endemic area. Scientific Reports 8, 15651.Google Scholar
Kay, GL, Millard, A, Sergeant, MJ, Midzi, N, Gwisai, R, Mduluza, T, Ivens, A, Nausch, N, Mutapi, F and Pallen, M (2015) Differences in the faecal microbiome in Schistosoma haematobium infected children vs. uninfected children. PLoS Neglected Tropical Diseases 9, e0003861.Google Scholar
Kelly, BJ, Gross, R, Bittinger, K, Sherrill-Mix, S, Lewis, JD, Collman, RG, Bushman, FD and Li, H (2015) Power and sample-size estimation for microbiome studies using pairwise distances and PERMANOVA. Bioinformatics 31, 2461–2468.Google Scholar
Kim, JY, Kim, EM, Yi, MH, Lee, J, Lee, S, Hwang, Y, Yong, D, Sohn, WM and Yong, TS (2018) Intestinal fluke Metagonimus yokogawai infection increases probiotic Lactobacillus in mouse cecum. Experimental Parasitology 193, 45–50.Google Scholar
Lee, SC, Tang, MS, Lim, YA, Choy, SH, Kurtz, ZD, Cox, LM, Gundra, UM, Cho, I, Bonneau, R, Blaser, MJ, Chua, KH and Loke, P (2014) Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Neglected Tropical Diseases 8, e2880.Google Scholar
Leung, JM, Graham, AL and Knowles, SCL (2018) Parasite-microbiota interactions with the vertebrate gut: synthesis through an ecological lens. Frontiers in Microbiology 9, 843.Google Scholar
Ley, RE, Hamady, M, Lozupone, C, Turnbaugh, PJ, Ramey, RR, Bircher, JS, Schlegel, ML, Tucker, TA, Schrenzel, MD, Knight, R and Gordon, JI (2008) Evolution of mammals and their gut microbes. Science 320, 1647–1651.Google Scholar
Li, RW, Li, W, Sun, J, Yu, P, Baldwin, RL and Urban, JF (2016) The effect of helminth infection on the microbial composition and structure of the caprine abomasal microbiome. Scientific Reports 6, 20606.Google Scholar
Lindgreen, S, Adair, KL and Gardner, PP (2016) An evaluation of the accuracy and speed of metagenome analysis tools. Scientific Reports 6, 19233.Google Scholar
Lozupone, CA, Stombaugh, JI, Gordon, JI, Jansson, JK and Knight, R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230.Google Scholar
Martin, I, Djuardi, Y, Sartono, E, Rosa, BA, Supali, T, Mitreva, M, Houwing-Duistermaat, JJ and Yazdanbakhsh, M (2018) Dynamic changes in human-gut microbiome in relation to a placebo-controlled anthelminthic trial in Indonesia. PLoS Neglected Tropical Diseases 12, e0006620.Google Scholar
Matias Rodrigues, JF, Schmidt, TSB, Tackmann, J and von Mering, C (2017) MAPseq: highly efficient k-mer search with confidence estimates, for rRNA sequence analysis. Bioinformatics 33, 3808–3810.Google Scholar
Mutapi, F (2015) The gut microbiome in the helminth infected host. Trends in Parasitology 31, 405–406.Google Scholar
O'Connell, EM and Nutman, TB (2016) Molecular diagnostics for soil-transmitted helminths. The American Journal of Tropical Medicine and Hygiene 95, 508–513.Google Scholar
Peachey, LE, Jenkins, TP and Cantacessi, C (2017) This gut ain't big enough for both of us. Or is it? Helminth-microbiota interactions in veterinary species. Trends in Parasitology 33, 619–632.Google Scholar
Peachey, LE, Molena, RA, Jenkins, TP, Di Cesare, A, Traversa, D, Hodgkinson, JE and Cantacessi, C (2018) The relationships between faecal egg counts and gut microbial composition in UK thoroughbreds infected by cyathostomins. International Journal for Parasitology 48, 403–412.Google Scholar
Peachey, LE, Castro, C, Molena, RA, Jenkins, TP, Griffin, JL, Cantacessi, C (In press) Dysbiosis associated with acute helminth infections in herbivorous youngstock – observations and implications. Sci Rep.Google Scholar
Pearce, EJ and MacDonald, AS (2002) The immunobiology of schistosomiasis. Nature Reviews Immunology 2, 499–511.Google Scholar
Pérez-Muñoz, ME, Bergstrom, K, Peng, V, Schmaltz, R, Jiménez-Cardona, R, Marsteller, N, McGee, S, Clavel, T, Ley, R, Fu, J, Xia, L and Peterson, DA (2014) Discordance between changes in the gut microbiota and pathogenicity in a mouse model of spontaneous colitis. Gut Microbes 5, 286–295.Google Scholar
Quast, C, Pruesse, E, Yilmaz, P, Gerken, J, Schweer, T, Yarza, P, Peplies, J and Glöckner, FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, 590–596.Google Scholar
Ramanan, D, Bowcutt, R, Lee, SC, Tang, MS, Kurtz, ZD, Ding, Y, Honda, K, Gause, WC, Blaser, MJ, Bonneau, RA, Lim, YA, Loke, P and Cadwell, K (2016) Helminth infection promotes colonization resistance via type 2 immunity. Science 352, 608–612.Google Scholar
Rapin, A and Harris, NL (2018) Helminth-bacterial interactions: cause and consequence. Trends in Immunology 39, 724–733.Google Scholar
Rausch, S, Held, J, Fischer, A, Heimesaat, MM, Kühl, AA, Bereswill, S and Hartmann, S (2013) Small intestinal nematode infection of mice is associated with increased enterobacterial loads alongside the intestinal tract. PLoS One 8, e74026.Google Scholar
Reynolds, LA, Smith, KA, Filbey, KJ, Harcus, Y, Hewitson, JP, Redpath, SA, Valdez, Y, Yebra, MJ, Finlay, BB and Maizels, RM (2014) Commensal-pathogen interactions in the intestinal tract: Lactobacilli promote infection with, and are promoted by, helminth parasites. Gut Microbes 5, 522–532.Google Scholar
Rosa, BA, Supali, T, Gankpala, L, Djuardi, Y, Sartono, E, Zhou, Y, Fischer, K, Martin, J, Tyagi, R, Bolay, FK, Fischer, PU, Yazdanbakhsh, M and Mitreva, M (2018) Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia. Microbiome 6, 33-018-0416-5.Google Scholar
Schneeberger, PHH, Coulibaly, JT, Panic, G, Daubenberger, C, Gueuning, M, Frey, JE and Keiser, J (2018a) Investigations on the interplays between Schistosoma mansoni, praziquantel and the gut microbiome. Parasites & Vectors 11, 168.Google Scholar
Schneeberger, PHH, Coulibaly, JT, Gueuning, M, Moser, W, Coburn, B, Frey, JE and Keiser, J (2018b) Off-target effects of tribendimidine, tribendimidine plus ivermectin, tribendimidine plus oxantel-pamoate, and albendazole plus oxantel-pamoate on the human gut microbiota. International Journal for Parasitology Drugs and Drug Resistance 8, 372–378.Google Scholar
Sekirov, I, Russell, SL, Antunes, LC and Finlay, BB (2010) Gut microbiota in health and disease. Physiological Reviews 90, 859–904.Google Scholar
Stensvold, CR and van der Giezen, M (2018) Associations between gut microbiota and common luminal intestinal parasites. Trends in Parasitology 34, 369–377.Google Scholar
Su, C, Su, L, Li, Y, Long, SR, Chang, J, Zhang, W, Walker, WA, Xavier, RJ, Cherayil, BJ and Shi, HN (2018) Helminth-induced alterations of the gut microbiota exacerbate bacterial colitis. Mucosal Immunology 11, 144–157.Google Scholar
Toro-Londono, M, Bedoya-Urrego, K, Garcia-Montoya, GM, Galvan-Diaz, AL and Alzate, JF (2019) Intestinal parasitic infection alters bacterial gut microbiota in children. PeerJ 7, e6200.Google Scholar
Wang, J, Tang, H, Zhang, C, Zhao, Y, Derrien, M, Rocher, E, van-Hylckama Vlieg, JE, Strissel, K, Zhao, L, Obin, M and Shen, J (2015a) Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. The ISME Journal 9, 1–15.Google Scholar
Wang, WL, Xu, SY, Ren, ZG, Tao, L, Jiang, JW and Zheng, SS (2015b) Application of metagenomics in the human gut microbiome. World Journal of Gastroenterology 21, 803–814.Google Scholar
Wu, S, Li, RW, Li, W, Beshah, E, Dawson, HD and Urban, JF Jr (2012) Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLoS One 7, e35470.Google Scholar
Yatsunenko, T, Rey, FE, Manary, MJ, Trehan, I, Domínguez-Bello, MG, Contreras, M, Magris, M, Hidalgo, G, Baldassano, RN, Anokhin, AP, Heath, AC, Warner, B, Reeder, J, Kuczynski, J, Caporaso, JG, Lozupone, CA, Lauber, C, Clemente, JC, Knights, D, Knight, R and Gordon, JI (2012) Human gut microbiome viewed across age and geography. Nature 486, 222–227.Google Scholar
Zaiss, MM, Rapin, A, Lebon, L, Dubey, LK, Mosconi, I, Sarter, K, Piersigilli, A, Menin, L, Walker, AW, Rougemont, J, Paerewijck, O, Geldhof, P, McCoy, KD, Macpherson, AJ, Croese, J, Giacomin, PR, Loukas, A, Junt, T, Marsland, BJ and Harris, NL (2015) The Intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation. Immunity 43, 998–1010.Google Scholar