Impact of intestinal parasites on microbiota and cobalamin gene sequences: a pilot study

Mejia, Rojelio; Damania, Ashish; Jeun, Rebecca; Bryan, Patricia; Vargas, Paola A.; Juárez, Marisa; Cajal, Pamela; Nasser, Julio R.; Krolewiecki, Alejandro; Lefoulon, Emilie; Long, Courtney; Drake, E. T.; Cimino, Rubén O.; Slatko, Barton E.

doi:10.1186/s13071-020-04073-7

Cited by 35 publications

(28 citation statements)

References 63 publications

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“…We reasoned that parasite-induced perturbations in the microbiome could also be an important factor influencing gastrointestinal symptoms. Our results, in combination with similar results from recent smaller-scale mouse and human experiments ( 62 , 63 ), raise the possibility that the shift in microbiome composition during Giardia infection—marked by a reduction in Gammaproteobacteria and an increase in Prevotella —may explain, at least in part, the apparent protective effect of Giardia against diarrhea in some age/site cohorts ( 30 , 34 , 56 ).…”

Section: Discussionsupporting

confidence: 87%

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

Berry

Johnson

Martins

et al. 2020

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Enteric parasitic infections are among the most prevalent infections in lower- and middle-income countries (LMICs) and have a profound impact on global public health. While the microbiome is increasingly recognized as a key determinant of gut health and human development, the impact of naturally acquired parasite infections on microbial community structure in the gut, and the extent to which parasite-induced changes in the microbiome may contribute to gastrointestinal symptoms, is poorly understood. Enteric parasites are routinely identified in companion animals in the United States, presenting a unique opportunity to leverage this animal model to investigate the impact of naturally acquired parasite infections on the microbiome. Clinical, parasitological, and microbiome profiling of a cohort of 258 dogs revealed a significant correlation between parasite infection and composition of the bacterial community in the gut. Relative to other enteric parasites, Giardia was associated with a more pronounced perturbation of the microbiome. To compare our findings to large-scale epidemiological studies of enteric diseases in humans, a database mining approach was employed to integrate clinical and microbiome data. Substantial and consistent alterations to microbiome structure were observed in Giardia-infected children. Importantly, infection was associated with a reduction in the relative abundance of potential pathobionts, including Gammaproteobacteria, and an increase in Prevotella—a profile often associated with gut health. Taken together, these data show that widespread Giardia infection in young animals and humans is associated with significant remodeling of the gut microbiome and provide a possible explanation for the high prevalence of asymptomatic Giardia infections observed across host species. IMPORTANCE While enteric parasitic infections are among the most important infections in lower- and middle-income countries, their impact on gut microbiota is poorly understood. We reasoned that clinical symptoms associated with these infections may be influenced by alterations of the microbiome that occur during infection. To explore this notion, we took a two-pronged approach. First, we studied a cohort of dogs naturally infected with various enteric parasites and found a strong association between parasite infection and altered gut microbiota composition. Giardia, one of the most prevalent parasite infections globally, had a particularly large impact on the microbiome. Second, we took a database-driven strategy to integrate microbiome data with clinical data from large human field studies and found that Giardia infection is also associated with marked alteration of the gut microbiome of children, suggesting a possible explanation for why Giardia has been reported to be associated with protection from moderate to severe diarrhea.

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Section: Discussionsupporting

confidence: 87%

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

Berry

Johnson

Martins

et al. 2020

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“…In this study, children infected with Giardia present a shift from enterotype I to enterotype II, characterized by an increase of Prevotella and a decrease of Bacteroides ( Toro-Londono et al, 2019 ). Significant increases in Prevotella were also observed in Argentinian children infected with Giardia compared to uninfected individuals ( Mejia et al, 2020 ). Interestingly, Giardia infection was associated with a decreased abundance of microbiome Vitamin B12 (cobalamin) biosynthesis genes (CbiM), which has been associated with impaired growth and development in children ( Mejia et al, 2020 ).…”

Section: Alterations To the Microbiota During Giardia mentioning

confidence: 99%

Giardia spp. and the Gut Microbiota: Dangerous Liaisons

et al. 2021

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Alteration of the intestinal microbiome by enteropathogens is commonly associated with gastrointestinal diseases and disorders and has far-reaching consequences for overall health. Significant advances have been made in understanding the role of microbial dysbiosis during intestinal infections, including infection with the protozoan parasite Giardia duodenalis, one of the most prevalent gut protozoa. Altered species composition and diversity, functional changes in the commensal microbiota, and changes to intestinal bacterial biofilm structure have all been demonstrated during the course of Giardia infection and have been implicated in Giardia pathogenesis. Conversely, the gut microbiota has been found to regulate parasite colonization and establishment and plays a critical role in immune modulation during mono and polymicrobial infections. These disruptions to the commensal microbiome may contribute to a number of acute, chronic, and post-infectious clinical manifestations of giardiasis and may account for variations in disease presentation within and between infected populations. This review discusses recent advances in characterizing Giardia-induced bacterial dysbiosis in the gut and the roles of dysbiosis in Giardia pathogenesis.

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“…During the acute phase of infection, Giardia actively interacts with the intestinal surface, causing epithelial damage, mucus layer disruptions, and gut microbiota dysbiosis [4,7,26,27,42]. These effects may occur at the site of infection and beyond, and result at least in part from the actions of Giardia excretory and secretory products and the host immune response ( [28,35], Gruettner p. 221 in [31]).…”

Section: Production Of Diseasementioning

confidence: 99%

“…These effects may occur at the site of infection and beyond, and result at least in part from the actions of Giardia excretory and secretory products and the host immune response ( [28,35], Gruettner p. 221 in [31]). Giardia cysteine proteases appear to play a critical role in the interactions between host intestinal epithelial cells and the parasite (Peirasmaki p. 89 in [31]; Gruettner p. 221 in [31]), as they do in the microbiota dysbiosis it induces [27]. Elegant studies A.G. Buret et al: Parasite 2020, 27, 49 using murine model systems confirmed that infection with Giardia disrupts intestinal microbiota and pave the way towards more research into microbiome-Giardia interactions (Starcevich p. 83 in [31]).…”

Section: Production Of Diseasementioning

confidence: 99%

Update on Giardia: Highlights from the seventh International Giardia and Cryptosporidium Conference

et al. 2020

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Although Giardia duodenalis is recognized as one of the leading causes of parasitic human diarrhea in the world, knowledge of the mechanisms of infection is limited, as the pathophysiological consequences of infection remain incompletely elucidated. Similarly, the reason for and consequences of the very specific genome-organization in this parasite with 2 active nuclei is only partially known. Consistent with its tradition, the 7th International Giardia and Cryptosporidium Conference (IGCC 2019) was held from June 23 to 26, 2019, at the Faculty of Medicine and Pharmacy of the University of Rouen-Normandie, France, to discuss current research perspectives in the field. This renowned event brought together an international delegation of researchers to present and debate recent advances and identify the main research themes and knowledge gaps. The program for this interdisciplinary conference included all aspects of host-parasite relationships, from basic research to applications in human and veterinary medicine, as well as the environmental issues raised by water-borne parasites and their epidemiological consequences. With regard to Giardia and giardiasis, the main areas of research for which new findings and the most impressive communications were presented and discussed included: parasite ecology and epidemiology of giardiasis, Giardia-host interactions, and cell biology of Giardia, genomes and genomic evolution. The high-quality presentations discussed at the Conference noted breakthroughs and identified new opportunities that will inspire researchers and funding agencies to stimulate future research in a “one health” approach to improve basic knowledge and clinical and public health management of zoonotic giardiasis.

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Impact of intestinal parasites on microbiota and cobalamin gene sequences: a pilot study

Cited by 35 publications

References 63 publications

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

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

Giardia spp. and the Gut Microbiota: Dangerous Liaisons

Update on Giardia: Highlights from the seventh International Giardia and Cryptosporidium Conference

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