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Interactions between parasitic helminths and gut microbiota in wild tropical primates from intact and fragmented habitats

  • 1.

    Zaiss, M. M. & Harris, N. L. Interactions between the intestinal microbiome and helminth parasites. Parasite Immunol. 38, 5–11 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 2.

    Cortés, A., Peachey, L. E., Jenkins, T. P., Scotti, R. & Cantacessi, C. Helminths and microbes within the vertebrate gut—not all studies are created equal. Parasitology 146, 1371–1378 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 3.

    Sender, R., Fuchs, S. & Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 14, e1002533 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 4.

    Claesson, M. J. et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 488, 178–184 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 5.

    Clemente, J. C., Ursell, L. K., Parfrey, L. W. & Knight, R. The impact of the gut microbiota on human health: An integrative view. Cell 148, 1258–1270 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 6.

    McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Nat. Acad. Sci. 110, 3229–3236 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 7.

    Hooper, L. V., Littman, D. R. & Macpherson, A. J. Interactions between the microbiota and the immune system. Science 336, 1268–1273 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 8.

    Tremaroli, V. & Bäckhed, F. Functional interactions between the gut microbiota and host metabolism. Nature 489, 242–249 (2012).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 9.

    Brown, E. M., Sadarangani, M. & Finlay, B. B. The role of the immune system in governing host-microbe interactions in the intestine. Nat. Immunol. 14, 660–667 (2013).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 10.

    Kim, S., Covington, A. & Pamer, E. G. The intestinal microbiota: Antibiotics, colonization resistance, and enteric pathogens. Immunol. Rev. 279, 90–105 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 11.

    Ducarmon, Q. R. et al. Gut microbiota and colonization resistance against bacterial enteric infection. Microbiol. Mol. Biol. Rev. 83, e00007-19 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 12.

    Sorbara, M. T. & Pamer, E. G. Interbacterial mechanisms of colonization resistance and the strategies pathogens use to overcome them. Mucosal Immunol. 12, 1–9 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 13.

    Jourdan, P. M., Lamberton, P. H. L., Fenwick, A. & Addiss, D. G. Soil-transmitted helminth infections. Lancet 391, 252–265 (2018).

    PubMed 
    Article 

    Google Scholar 

  • 14.

    Wammes, L. J., Mpairwe, H., Elliott, A. M. & Yazdanbakhsh, M. Helminth therapy or elimination: Epidemiological, immunological, and clinical considerations. Lancet Infect. Dis. 14, 1150–1162 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 15.

    Jenkins, T. P. et al. Experimental infection with the hookworm, Necator americanus, is associated with stable gut microbial diversity in human volunteers with relapsing multiple sclerosis. BMC Biol. 19, 1–17 (2021).

    Article 
    CAS 

    Google Scholar 

  • 16.

    Holm, J. B. et al. Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of Lactobacilli. PLoS ONE 10, e0125495 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 17.

    Ducarmon, Q. R. et al. Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae. Gut Microbes 12, 1840764 (2020).

    PubMed Central 
    Article 
    CAS 
    PubMed 

    Google Scholar 

  • 18.

    Broadhurst, M. J. et al. Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog. 8, e1003000 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 19.

    Kreisinger, J., Bastien, G., Hauffe, H. C., Marchesi, J. & Perkins, S. E. Interactions between multiple helminths and the gut microbiota in wild rodents. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20140295 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 20.

    Filyk, H. A. & Osborne, L. C. The multibiome: The intestinal ecosystem’s influence on immune homeostasis, health, and disease. EBioMedicine 13, 46–54 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 21.

    Cantacessi, C. et al. Impact of experimental hookworm infection on the human gut microbiota. J. Infect. Dis. 210, 1431–1434 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 22.

    Li, R. W. et al. Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis. Infect. Immun. 80, 2150–2157 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 23.

    Reynolds, L. A., Brett Finlay, B. & Maizels, R. M. Cohabitation in the intestine: Interactions among helminth parasites, bacterial microbiota, and host immunity. J. Immunol. 195, 4059–4066 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 24.

    Lee, S. C. et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl. Trop. Dis. 8, e2880 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 25.

    Rosa, B. A. et al. Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia. Microbiome 6, 33 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 26.

    Newbold, L. K. et al. Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota. ISME J. 11, 663–675 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 27.

    Baxter, N. T. et al. Intra- and interindividual variations mask interspecies variation in the microbiota of sympatric Peromyscus populations. Appl. Environ. Microbiol. 81, 396–404 (2015).

    ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 28.

    Cooper, P. et al. Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLoS ONE 8, e76573 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 29.

    Rapin, A. & Harris, N. L. Helminth-bacterial interactions: Cause and consequence. Trends Immunol. 39, 724–733 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 30.

    Cowlishaw, G. & Dunbar, R. I. Primate Conservation Biology (University of Chicago Press, 2000).

    Book 

    Google Scholar 

  • 31.

    Estrada, A. et al. Impending extinction crisis of the world’s primates: Why primates matter. Sci. Adv. 3, e1600946 (2017).

    ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 32.

    Barelli, C. et al. The gut microbiota communities of wild arboreal and ground-feeding tropical primates are affected differently by habitat disturbance. mSystems 5, 3 (2020).

    Article 

    Google Scholar 

  • 33.

    Barelli, C. et al. Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: Implications for conservation. Sci. Rep. 5, 14862 (2015).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 34.

    Barelli, C. et al. Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum. PLoS ONE 14, e0225142 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 35.

    Barelli, C. et al. Loss of protozoan and metazoan intestinal symbiont biodiversity in wild primates living in unprotected forests. Sci. Rep. 10, 1–12 (2020).

    Article 
    CAS 

    Google Scholar 

  • 36.

    Aivelo, T. & Norberg, A. Parasite-microbiota interactions potentially affect intestinal communities in wild mammals. J. Anim. Ecol. 87, 438–447 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 37.

    Vlčková, K. et al. Relationships between gastrointestinal parasite infections and the fecal microbiome in free-ranging western lowland gorillas. Front. Microbiol. 9, 1202 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 38.

    Mann, A. E. et al. Biodiversity of protists and nematodes in the wild nonhuman primate gut. ISME J. 14, 609–622 (2020).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 39.

    de Winter, I. I. et al. Effects of seasonality and previous logging on faecal helminth-microbiota associations in wild lemurs. Sci. Rep. 10, 16818 (2020).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 40.

    Ghai, R. R. et al. Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda. PLoS Negl. Trop. Dis. 8, e3256 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 41.

    Nutman, T. B. Human infection with Strongyloides stercoralis and other related Strongyloides species. Parasitology 144, 263–273 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    Stephenson, L. S., Holland, C. V. & Cooper, E. S. The public health significance of Trichuris trichiura. Parasitology 121, S73–S95 (2000).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 43.

    Viney, M. E. The biology of Strongyloides spp. WormBook https://doi.org/10.1895/wormbook.1.141.2 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 44.

    Renelies-Hamilton, J. et al. Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal. Infect. Genet. Evol. 74, 104010 (2019).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 45.

    Afrin, T. et al. Sequential changes in the host gut microbiota during infection with the intestinal parasitic nematode. Front. Cell Infect. Microbiol. 9, 217 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 46.

    Rubel, M. A. et al. Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians. Genome Biol. 21, 122 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 47.

    Jenkins, T. P. et al. Author Correction: A comprehensive analysis of the faecal microbiome and metabolome of Strongyloides stercoralis infected volunteers from a non-endemic area. Sci. Rep. 9, 8571 (2019).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 48.

    Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 49.

    van der Zande, H. J. P., Zawistowska-Deniziak, A. & Guigas, B. Immune regulation of metabolic homeostasis by helminths and their molecules. Trends Parasitol. 35, 795–808 (2019).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 50.

    Maeda, Y. & Takeda, K. Host–microbiota interactions in rheumatoid arthritis. Exp. Mol. Med. 51, 1–6 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 51.

    Biddle, A., Stewart, L., Blanchard, J. & Leschine, S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity 5, 627–640 (2013).

    Article 

    Google Scholar 

  • 52.

    Brulc, J. M. et al. Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc. Natl. Acad. Sci. USA 106, 1948–1953 (2009).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 53.

    Hale, V. L. et al. Diet versus phylogeny: A comparison of gut microbiota in captive Colobine monkey species. Microb. Ecol. 75, 515–527 (2018).

    PubMed 
    Article 

    Google Scholar 

  • 54.

    Trosvik, P. et al. Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate. Microbiome 6, 84 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 55.

    Liu, B. et al. Western diet feeding influences gut microbiota profiles in apoE knockout mice. Lipids Health Dis. 17, 159 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 56.

    Bhute, S. S. et al. Gut microbial diversity assessment of Indian Type-2-diabetics reveals alterations in Eubacteria, Archaea, and Eukaryotes. Front. Microbiol. 8, 214 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 57.

    Wang, Y. et al. Phocea, Pseudoflavonifractor and Lactobacillus intestinalis: Three potential biomarkers of gut microbiota that affect progression and complications of obesity-induced Type 2 diabetes Mellitus. Diabetes Metab. Syndr. Obes. 13, 835–850 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 58.

    Yarahmadi, M. et al. The anti-giardial effectiveness of fungal and commercial chitosan against Giardia intestinalis cysts in vitro. J. Parasit. Dis. 40, 75–80 (2016).

    PubMed 
    Article 

    Google Scholar 

  • 59.

    Dinleyici, E. C. et al. Clinical efficacy of Saccharomyces boulardii or metronidazole in symptomatic children with Blastocystis hominis infection. Parasitol. Res. 108, 541–545 (2011).

    PubMed 
    Article 

    Google Scholar 

  • 60.

    Lepczyńska, M. & Dzika, E. The influence of probiotic bacteria and human gut microorganisms causing opportunistic infections on ST3. Gut Pathog. 11, 6 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 61.

    Huseyin, C. E., O’Toole, P. W., Cotter, P. D. & Scanlan, P. D. Forgotten fungi—the gut mycobiome in human health and disease. FEMS Microbiol. Rev. 41, 479–511 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 62.

    Mittermeier, R. A., Myers, N., Gill, P. C. & Mittermeier, C. G. Hotspots: Earth’s Richest and Most Endangered Terrestrial Ecoregions (CEMEX, 2000).

    Google Scholar 

  • 63.

    Platts, P. J. et al. Delimiting tropical mountain ecoregions for conservation. Environ. Conserv. 38, 312–324 (2011).

    Article 

    Google Scholar 

  • 64.

    Ruiz-Lopez, M. J. et al. A novel landscape genetic approach demonstrates the effects of human disturbance on the Udzungwa red colobus monkey (Procolobus gordonorum). Heredity 116, 167–176 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 65.

    Cavada, N., Tenan, S., Barelli, C. & Rovero, F. Effects of anthropogenic disturbance on primate density at the landscape scale. Conserv. Biol. 33, 873–882 (2019).

    PubMed 
    Article 

    Google Scholar 

  • 66.

    Laurance, W. F. et al. Averting biodiversity collapse in tropical forest protected areas. Nature 489, 290–294 (2012).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 67.

    Rovero, F. et al. Primates decline rapidly in unprotected forests: Evidence from a monitoring program with data constraints. PLoS ONE 10, e0118330 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 68.

    International Union for the Conservation of Nature and Natural Resources (IUCN). 2021. IUCN red list of threatened species version 2020-2. International Union for the Conservation of Nature and Natural Resources http://www.iucnredlist.org. (Accessed 21 Apr 2021).

  • 69.

    Modrý, D., Pafčo, B., Petrželková, K. J. & Hasegawa, H. Parasites of Apes: An Atlas of Coproscopic Diagnostics (2018).

  • 70.

    Gillespie, T. R. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. Int. J. Primatol. 27, 1129–1143 (2006).

    Article 

    Google Scholar 

  • 71.

    Hasegawa, H. Methods of collection and identification of minute nematodes from the feces of primates, with special application to coevolutionary study of pinworms. In Primate Parasite Ecology: The Dynamics of Host-parasite Relationships (eds Huffman, M. A. & Chapman, C. A.) 29–46 (Cambridge University Press, 2009).

    Google Scholar 

  • 72.

    Mallott, E. K., Malhi, R. S. & Garber, P. A. High-throughput sequencing of fecal DNA to identify insects consumed by wild Weddell’s saddleback tamarins (Saguinus weddelli, Cebidae, Primates) in Bolivia. Am. J. Phys. Anthropol. 156, 474–481 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 73.

    Mallott, E. K., Garber, P. A. & Malhi, R. S. Integrating feeding behavior, ecological data, and DNA barcoding to identify developmental differences in invertebrate foraging strategies in wild white-faced capuchins (Cebus capucinus). Am. J. Phys. Anthropol. 162, 241–254 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 74.

    Albanese, D., Fontana, P., De Filippo, C., Cavalieri, D. & Donati, C. MICCA: A complete and accurate software for taxonomic profiling of metagenomic data. Sci. Rep. 5, 9743 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 75.

    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2021) https://www.R-project.org.

  • 76.

    Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. Emmeans: Estimated marginal means, aka least-squares means. R package version, Vol. 1, 3 (2018) https://CRAN.R-project.org/package=emmeans.


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