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Natural Infection with Giardia Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome

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Natural Infection with Giardia Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome bioRxiv preprint doi: https://doi.org/10.1101/2020.01.13.905604; this version posted January 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Title: Natural infection with Giardia is associated with altered community structure of the human and canine gut microbiome. Running Title: Natural parasite infections perturb the gut microbiome Alexander S.F. Berrya,b#, Kaylynn Johnsona, Rene Martinsc, Megan Sullivana, Camila Farias Amorima, Alexandra Putred, Aiysha Scottd, Shuai Wanga, Brianna Lindsayd, Robert Baldassanob, a a# Thomas J. Nolan , Daniel P. Beiting aDepartment of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA, USA bDepartment of Pediatric Gastroenterology Hepatology and Nutrition, Children’s Hospital of Philadelphia, Philadelphia, PA 19104 cDepartment of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA, USA dDepartment of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, USA Corresponding Author: Daniel P. Beiting, [email protected] Abstract word count: 249 Main text word count: 3711 bioRxiv preprint doi: https://doi.org/10.1101/2020.01.13.905604; this version posted January 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Abstract 2 Enteric parasitic infections are among the most prevalent infections in lower- and 3 middle-income countries (LMICs), and have a profound impact on global public health. While 4 the microbiome is increasingly recognized as a key determinant of gut health and human 5 development, the impact of naturally-acquired parasite infections on microbial community 6 structure in the gut, and the extent to which parasite-induced changes in the microbiome may 7 contribute to gastrointestinal symptoms, is poorly understood. Enteric parasites are routinely 8 identified in companion animals in the United States, presenting a unique opportunity to 9 leverage this animal model to investigate the impact of naturally-acquired parasite infections 10 on the microbiome. Clinical, parasitological, and microbiome profiling of a cohort of 258 dogs 11 revealed a significant correlation between parasite infection and composition of the bacterial 12 community in the gut. Relative to other enteric pathogens, Giardia was associated with a more 13 pronounced perturbation of the microbiome. Using a database mining approach that allowed 14 us to compare our findings to a large-scale epidemiological study of enteric diseases in humans, 15 we also observed a substantial alteration to microbiome structure in Giardia-infected 16 children. Importantly, infection was associated with a reduction in the relative abundance of 17 potential pathobionts, including Gammaproteobacteria, and an increase in Prevotella - a profile 18 often associated with gut health. Taken together, our data show that widespread Giardia 19 infection in young animals and humans is associated with significant remodeling of the gut 20 microbiome, and provide a possible explanation for the high prevalence of asymptomatic 21 Giardia infections observed across host species. 22 bioRxiv preprint doi: https://doi.org/10.1101/2020.01.13.905604; this version posted January 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 23 Importance 24 While enteric parasitic infections are among the most important infections in lower- and 25 middle-income countries, their impact on gut microbiota is poorly understood. We reasoned 26 that clinical symptoms associated with these infections may be influenced by alterations of the 27 microbiome that occur during infection. To explore this notion, we took a two-pronged 28 approach. First, we studied a cohort of dogs naturally infected with various enteric parasites 29 and found a strong association between parasite infection and altered gut microbiota 30 composition. Giardia, one of the most prevalent parasite infections globally, had a particularly 31 large impact on the microbiome. Second, we took a database-driven strategy to integrate 32 microbiome data with clinical data from large human field studies and found that Giardia 33 infection is also associated with marked alteration of the gut microbiome of children, 34 suggesting a possible explanation for why Giardia has been reported to be associated with 35 protection from moderate-to-severe diarrhea. 36 37 38 39 40 41 42 43 bioRxiv preprint doi: https://doi.org/10.1101/2020.01.13.905604; this version posted January 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 44 Introduction 45 Enteric parasites, including helminths and protozoa, are among the most prevalent 46 infections in lower- and middle-income countries (LMICs) with an estimated 3.5 billion people 47 affected worldwide (1, 2). Infection with eukaryotic pathogens often results in acute, 48 moderate-to-severe diarrheal disease and/or chronic malnutrition and stunting, which has 49 significant consequences for morbidity and mortality (3–5). Conversely, some intestinal 50 parasites are frequently associated with asymptomatic infections, or are even considered 51 commensal (6, 7). Giardia, for example, was found in 18 of 1093 (1.6%) of healthy volunteers in 52 Melbourne, Australia (8) and in 286 of 1359 (21%) of healthy schoolchildren in Madrid, Spain 53 (9). It is important to understand whether and how these abundant and pervasive parasites 54 impact gut health. 55 While the microbiome is increasingly recognized as a key determinant of gut health and 56 human development, the impact of naturally-acquired parasite infections on the microbial 57 community in the gut is poorly understood. Many studies of parasites and their impact on the 58 microbiome involve experimental infections of laboratory mice (10–12). While such studies can 59 be powerful for elucidating mechanism, they often involve laboratory-adapted parasite strains, 60 specialized animal husbandry practices, or high infectious doses, all of which can impact host 61 immunity and the composition of the microbiome. Conversely, studies of parasite infections in 62 human populations are challenging due to the relatively low prevalence of these infections in 63 developed countries and the presence of confounding variables, such as malnourishment (13– 64 16). These issues are largely overcome by studying enteric parasite infections in companion bioRxiv preprint doi: https://doi.org/10.1101/2020.01.13.905604; this version posted January 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 65 animals. Various enteric parasites are frequently found in screenings of domestic dogs and cats 66 in the United States (17). For example, a study of over one million dogs throughout the United 67 States in 2006 found that 12.5% were infected with at least one enteric parasite, with the most 68 prevalent being Giardia which infected 4% of dogs (18). As companion animals, dogs are 69 increasingly recognized as an ideal model system for translational gut microbiome research. In 70 addition to a harboring similar gut microbiota as humans, dogs often share their environment 71 with humans, consume a similar omnivorous diet, and can spontaneously develop GI disease 72 that shares many features in common with inflammatory bowel disease in humans (19–26). In 73 addition, like humans, dogs frequently become infected with enteric parasites in early 74 life. Here we performed 16S rRNA sequencing of fecal samples from 258 dogs naturally- 75 infected with one or more eukaryotic parasites to evaluate the impact of parasite infection on 76 gut microbiota composition. We found that parasite infections significantly perturb the 77 microbiome and that Giardia is associated with the largest changes in canine gut microbiota. 78 We also investigated whether Giardia – a frequent infection among humans residing in 79 LMICs – causes similar perturbations in human gut microbiota composition. The Global Enteric 80 Multicenter Study (GEMS) investigated the causes of pediatric moderate-to-severe diarrhea 81 (MSD) in LMICs (27). In addition to reporting a strong association between infection with 82 rotavirus or Cryptosporidium and the development of MSD, this study also described the 83 surprising observation that Giardia was significantly associated with protection from MSD. A 84 follow-up study performed 16S sequencing of fecal samples from approximately 1000 GEMS 85 participants (28), but this study only considered the relationship between the microbiome and 86 MSD, and did not examine a role for parasite infections in influencing this relationship. We bioRxiv preprint doi: https://doi.org/10.1101/2020.01.13.905604; this version posted January 14, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 87 used a database mining approach to determine if Giardia infection perturbs the human gut 88 microbiome similarly to how it perturbs the canine gut microbiome,
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