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

. 2021 Nov 03 ; 11 (1) : 21569. [epub] 20211103

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34732823

Grantová podpora
752399 European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie

Odkazy

PubMed 34732823
PubMed Central PMC8566450
DOI 10.1038/s41598-021-01145-1
PII: 10.1038/s41598-021-01145-1
Knihovny.cz E-zdroje

The mammalian gastrointestinal tract harbours a highly complex ecosystem composed of a variety of micro- (bacteria, fungi, viruses, protozoans) and macro-organisms (helminths). Although most microbiota research focuses on the variation of single gut components, the crosstalk between components is still poorly characterized, especially in hosts living under natural conditions. We investigated the gut micro-biodiversity (bacteria, fungi and helminths) of 158 individuals of two wild non-human primates, the Udzungwa red colobus (Procolobus gordonorum) and the yellow baboon (Papio cynocephalus). These species have contrasting diets and lifestyles, but live sympatrically in both human-impacted and pristine forests in the Udzungwa Mountains of Tanzania. Using non-invasive faecal pellets, helminths were identified using standard microscopy while bacteria and fungi were characterized by sequencing the V1-V3 variable region of the 16S rRNA gene for bacteria and the ITS1-ITS2 fragment for fungi. Our results show that both diversity and composition of bacteria and fungi are associated with variation in helminth presence. Although interactions differed by habitat type, in both primates we found that Strongyloides was negatively associated and Trichuris was positively associated with bacterial and fungal richness. To our knowledge, this is one of the few studies demonstrating an interaction between helminth and gut microbiota communities in wild non-human primates.

Zobrazit více v PubMed

Zaiss MM, Harris NL. Interactions between the intestinal microbiome and helminth parasites. Parasite Immunol. 2016;38:5–11. doi: 10.1111/pim.12274. PubMed DOI PMC

Cortés A, Peachey LE, Jenkins TP, Scotti R, Cantacessi C. Helminths and microbes within the vertebrate gut—not all studies are created equal. Parasitology. 2019;146:1371–1378. doi: 10.1017/S003118201900088X. PubMed DOI

Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14:e1002533. doi: 10.1371/journal.pbio.1002533. PubMed DOI PMC

Claesson MJ, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012;488:178–184. doi: 10.1038/nature11319. PubMed DOI

Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: An integrative view. Cell. 2012;148:1258–1270. doi: 10.1016/j.cell.2012.01.035. PubMed DOI PMC

McFall-Ngai M, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Nat. Acad. Sci. 2013;110:3229–3236. doi: 10.1073/pnas.1218525110. PubMed DOI PMC

Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336:1268–1273. doi: 10.1126/science.1223490. PubMed DOI PMC

Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:242–249. doi: 10.1038/nature11552. PubMed DOI

Brown EM, Sadarangani M, Finlay BB. The role of the immune system in governing host-microbe interactions in the intestine. Nat. Immunol. 2013;14:660–667. doi: 10.1038/ni.2611. PubMed DOI

Kim S, Covington A, Pamer EG. The intestinal microbiota: Antibiotics, colonization resistance, and enteric pathogens. Immunol. Rev. 2017;279:90–105. doi: 10.1111/imr.12563. PubMed DOI PMC

Ducarmon QR, Zwittink RD, Hornung BVH, Van Schaik W, Young VB, Kuijper EJ. Gut microbiota and colonization resistance against bacterial enteric infection. Microbiol. Mol. Biol. Rev. 2019;83:e00007-19. doi: 10.1128/MMBR.00007-19. PubMed DOI PMC

Sorbara MT, Pamer EG. Interbacterial mechanisms of colonization resistance and the strategies pathogens use to overcome them. Mucosal Immunol. 2019;12:1–9. doi: 10.1038/s41385-018-0053-0. PubMed DOI PMC

Jourdan PM, Lamberton PHL, Fenwick A, Addiss DG. Soil-transmitted helminth infections. Lancet. 2018;391:252–265. doi: 10.1016/S0140-6736(17)31930-X. PubMed DOI

Wammes LJ, Mpairwe H, Elliott AM, Yazdanbakhsh M. Helminth therapy or elimination: Epidemiological, immunological, and clinical considerations. Lancet Infect. Dis. 2014;14:1150–1162. doi: 10.1016/S1473-3099(14)70771-6. PubMed DOI

Jenkins TP, 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. 2021;19:1–17. doi: 10.1186/s12915-021-01003-6. PubMed DOI PMC

Holm JB, et al. Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of Lactobacilli. PLoS ONE. 2015;10:e0125495. doi: 10.1371/journal.pone.0125495. PubMed DOI PMC

Ducarmon QR, et al. Dynamics of the bacterial gut microbiota during controlled human infection with Necator americanus larvae. Gut Microbes. 2020;12:1840764. doi: 10.1080/19490976.2020.1840764. PubMed DOI PMC

Broadhurst MJ, et al. Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog. 2012;8:e1003000. doi: 10.1371/journal.ppat.1003000. PubMed DOI PMC

Kreisinger J, Bastien G, Hauffe HC, Marchesi J, Perkins SE. Interactions between multiple helminths and the gut microbiota in wild rodents. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2015;370:20140295. doi: 10.1098/rstb.2014.0295. PubMed DOI PMC

Filyk HA, Osborne LC. The multibiome: The intestinal ecosystem’s influence on immune homeostasis, health, and disease. EBioMedicine. 2016;13:46–54. doi: 10.1016/j.ebiom.2016.10.007. PubMed DOI PMC

Cantacessi C, et al. Impact of experimental hookworm infection on the human gut microbiota. J. Infect. Dis. 2014;210:1431–1434. doi: 10.1093/infdis/jiu256. PubMed DOI PMC

Li RW, et al. Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis. Infect. Immun. 2012;80:2150–2157. doi: 10.1128/IAI.00141-12. PubMed DOI PMC

Reynolds LA, Brett Finlay B, Maizels RM. Cohabitation in the intestine: Interactions among helminth parasites, bacterial microbiota, and host immunity. J. Immunol. 2015;195:4059–4066. doi: 10.4049/jimmunol.1501432. PubMed DOI PMC

Lee SC, et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl. Trop. Dis. 2014;8:e2880. doi: 10.1371/journal.pntd.0002880. PubMed DOI PMC

Rosa BA, et al. Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia. Microbiome. 2018;6:33. doi: 10.1186/s40168-018-0416-5. PubMed DOI PMC

Newbold LK, et al. Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota. ISME J. 2017;11:663–675. doi: 10.1038/ismej.2016.153. PubMed DOI PMC

Baxter NT, et al. Intra- and interindividual variations mask interspecies variation in the microbiota of sympatric Peromyscus populations. Appl. Environ. Microbiol. 2015;81:396–404. doi: 10.1128/AEM.02303-14. PubMed DOI PMC

Cooper P, et al. Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLoS ONE. 2013;8:e76573. doi: 10.1371/journal.pone.0076573. PubMed DOI PMC

Rapin A, Harris NL. Helminth-bacterial interactions: Cause and consequence. Trends Immunol. 2018;39:724–733. doi: 10.1016/j.it.2018.06.002. PubMed DOI

Cowlishaw G, Dunbar RI. Primate Conservation Biology. University of Chicago Press; 2000.

Estrada A, et al. Impending extinction crisis of the world’s primates: Why primates matter. Sci. Adv. 2017;3:e1600946. doi: 10.1126/sciadv.1600946. PubMed DOI PMC

Barelli C, et al. The gut microbiota communities of wild arboreal and ground-feeding tropical primates are affected differently by habitat disturbance. mSystems. 2020;5:3. doi: 10.1128/mSystems.00061-20. PubMed DOI PMC

Barelli C, et al. Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: Implications for conservation. Sci. Rep. 2015;5:14862. doi: 10.1038/srep14862. PubMed DOI PMC

Barelli C, et al. Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum. PLoS ONE. 2019;14:e0225142. doi: 10.1371/journal.pone.0225142. PubMed DOI PMC

Barelli C, et al. Loss of protozoan and metazoan intestinal symbiont biodiversity in wild primates living in unprotected forests. Sci. Rep. 2020;10:1–12. doi: 10.1038/s41598-020-67959-7. PubMed DOI PMC

Aivelo T, Norberg A. Parasite-microbiota interactions potentially affect intestinal communities in wild mammals. J. Anim. Ecol. 2018;87:438–447. doi: 10.1111/1365-2656.12708. PubMed DOI

Vlčková K, et al. Relationships between gastrointestinal parasite infections and the fecal microbiome in free-ranging western lowland gorillas. Front. Microbiol. 2018;9:1202. doi: 10.3389/fmicb.2018.01202. PubMed DOI PMC

Mann AE, et al. Biodiversity of protists and nematodes in the wild nonhuman primate gut. ISME J. 2020;14:609–622. doi: 10.1038/s41396-019-0551-4. PubMed DOI PMC

de Winter II, et al. Effects of seasonality and previous logging on faecal helminth-microbiota associations in wild lemurs. Sci. Rep. 2020;10:16818. doi: 10.1038/s41598-020-73827-1. PubMed DOI PMC

Ghai RR, 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. 2014;8:e3256. doi: 10.1371/journal.pntd.0003256. PubMed DOI PMC

Nutman TB. Human infection with Strongyloides stercoralis and other related Strongyloides species. Parasitology. 2017;144:263–273. doi: 10.1017/S0031182016000834. PubMed DOI PMC

Stephenson LS, Holland CV, Cooper ES. The public health significance of Trichuris trichiura. Parasitology. 2000;121:S73–S95. doi: 10.1017/S0031182000006867. PubMed DOI

Viney ME. The biology of Strongyloides spp. WormBook. 2015 doi: 10.1895/wormbook.1.141.2. PubMed DOI PMC

Renelies-Hamilton J, et al. Exploring interactions between Blastocystis sp., Strongyloides spp. and the gut microbiomes of wild chimpanzees in Senegal. Infect. Genet. Evol. 2019;74:104010. doi: 10.1016/j.meegid.2019.104010. PubMed DOI

Afrin T, et al. Sequential changes in the host gut microbiota during infection with the intestinal parasitic nematode. Front. Cell Infect. Microbiol. 2019;9:217. doi: 10.3389/fcimb.2019.00217. PubMed DOI PMC

Rubel MA, et al. Lifestyle and the presence of helminths is associated with gut microbiome composition in Cameroonians. Genome Biol. 2020;21:122. doi: 10.1186/s13059-020-02020-4. PubMed DOI PMC

Jenkins TP, 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. 2019;9:8571. doi: 10.1038/s41598-019-43508-9. PubMed DOI PMC

Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489:220–230. doi: 10.1038/nature11550. PubMed DOI PMC

van der Zande HJP, Zawistowska-Deniziak A, Guigas B. Immune regulation of metabolic homeostasis by helminths and their molecules. Trends Parasitol. 2019;35:795–808. doi: 10.1016/j.pt.2019.07.014. PubMed DOI

Maeda Y, Takeda K. Host–microbiota interactions in rheumatoid arthritis. Exp. Mol. Med. 2019;51:1–6. doi: 10.1038/s12276-019-0283-6. PubMed DOI PMC

Biddle A, Stewart L, Blanchard J, Leschine S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity. 2013;5:627–640. doi: 10.3390/d5030627. DOI

Brulc JM, et al. Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc. Natl. Acad. Sci. USA. 2009;106:1948–1953. doi: 10.1073/pnas.0806191105. PubMed DOI PMC

Hale VL, et al. Diet versus phylogeny: A comparison of gut microbiota in captive Colobine monkey species. Microb. Ecol. 2018;75:515–527. doi: 10.1007/s00248-017-1041-8. PubMed DOI

Trosvik P, et al. Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate. Microbiome. 2018;6:84. doi: 10.1186/s40168-018-0468-6. PubMed DOI PMC

Liu B, et al. Western diet feeding influences gut microbiota profiles in apoE knockout mice. Lipids Health Dis. 2018;17:159. doi: 10.1186/s12944-018-0811-8. PubMed DOI PMC

Bhute SS, et al. Gut microbial diversity assessment of Indian Type-2-diabetics reveals alterations in Eubacteria, Archaea, and Eukaryotes. Front. Microbiol. 2017;8:214. doi: 10.3389/fmicb.2017.00214. PubMed DOI PMC

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. 2020;13:835–850. doi: 10.2147/DMSO.S240728. PubMed DOI PMC

Yarahmadi M, et al. The anti-giardial effectiveness of fungal and commercial chitosan against Giardia intestinalis cysts in vitro. J. Parasit. Dis. 2016;40:75–80. doi: 10.1007/s12639-014-0449-z. PubMed DOI PMC

Dinleyici EC, et al. Clinical efficacy of Saccharomyces boulardii or metronidazole in symptomatic children with Blastocystis hominis infection. Parasitol. Res. 2011;108:541–545. doi: 10.1007/s00436-010-2095-4. PubMed DOI

Lepczyńska M, Dzika E. The influence of probiotic bacteria and human gut microorganisms causing opportunistic infections on ST3. Gut Pathog. 2019;11:6. doi: 10.1186/s13099-019-0287-8. PubMed DOI PMC

Huseyin CE, O’Toole PW, Cotter PD, Scanlan PD. Forgotten fungi—the gut mycobiome in human health and disease. FEMS Microbiol. Rev. 2017;41:479–511. doi: 10.1093/femsre/fuw047. PubMed DOI

Mittermeier RA, Myers N, Gill PC, Mittermeier CG. Hotspots: Earth’s Richest and Most Endangered Terrestrial Ecoregions. CEMEX; 2000.

Platts PJ, et al. Delimiting tropical mountain ecoregions for conservation. Environ. Conserv. 2011;38:312–324. doi: 10.1017/S0376892911000191. DOI

Ruiz-Lopez MJ, et al. A novel landscape genetic approach demonstrates the effects of human disturbance on the Udzungwa red colobus monkey (Procolobus gordonorum) Heredity. 2016;116:167–176. doi: 10.1038/hdy.2015.82. PubMed DOI PMC

Cavada N, Tenan S, Barelli C, Rovero F. Effects of anthropogenic disturbance on primate density at the landscape scale. Conserv. Biol. 2019;33:873–882. doi: 10.1111/cobi.13269. PubMed DOI

Laurance WF, et al. Averting biodiversity collapse in tropical forest protected areas. Nature. 2012;489:290–294. doi: 10.1038/nature11318. PubMed DOI

Rovero F, et al. Primates decline rapidly in unprotected forests: Evidence from a monitoring program with data constraints. PLoS ONE. 2015;10:e0118330. doi: 10.1371/journal.pone.0118330. PubMed DOI PMC

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).

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

Gillespie TR. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. Int. J. Primatol. 2006;27:1129–1143. doi: 10.1007/s10764-006-9064-x. DOI

Hasegawa H. Methods of collection and identification of minute nematodes from the feces of primates, with special application to coevolutionary study of pinworms. In: Huffman MA, Chapman CA, editors. Primate Parasite Ecology: The Dynamics of Host-parasite Relationships. Cambridge University Press; 2009. pp. 29–46.

Mallott EK, Malhi RS, Garber PA. 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. 2015;156:474–481. doi: 10.1002/ajpa.22654. PubMed DOI

Mallott EK, Garber PA, Malhi RS. 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. 2017;162:241–254. doi: 10.1002/ajpa.23113. PubMed DOI

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. 2015;5:9743. doi: 10.1038/srep09743. PubMed DOI PMC

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

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.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...