TY - JOUR

T1 - Opisthorchis viverrini, Clonorchis sinensis and Opisthorchis felineus liver flukes affect mammalian host microbiome in a species-specific manner

AU - Pakharukova, Maria Y

AU - Lishai, Ekaterina A

AU - Zaparina, Oxana

AU - Baginskaya, Nina V

AU - Hong, Sung-Jong

AU - Sripa, Banchob

AU - Mordvinov, Viatcheslav A

N1 - Funding: Library preparation, sequencing, and data analysis was financially supported by the Russian Science Foundation and Novosibirsk Oblast (https://rscf.ru/en/) (grant number 22-24-20010 to M.Y.P.). The microscopic analysis was conducted at the Microscopy Center of the ICG SB RAS and was supported by the Siberian Branch of the Russian Academy of Science (grant number FWNR-2022-0021 to V.A.M.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Copyright: © 2023 Pakharukova et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2023/2/13

Y1 - 2023/2/13

N2 - BACKGROUND: Opisthorchis felineus, Opisthorchis viverrini and Clonorchis sinensis are epidemiologically significant food-borne trematodes endemic to diverse climatic areas. O. viverrini and C. sinensis are both recognized to be 1A group of biological carcinogens to human, whereas O. felineus is not. The mechanisms of carcinogenesis by the liver flukes are studied fragmentarily, the role of host and parasite microbiome is an unexplored aspect.METHODOLOGY/PRINCIPAL FINDINGS: Specific pathogen free Mesocricetus auratus hamsters were infected with C. sinensis, O. viverrini and O. felineus. The microbiota of the adult worms, colon feces and bile from the hamsters was investigated using Illumina-based sequencing targeting the prokaryotic 16S rRNA gene. The analysis of 43 libraries revealed 18,830,015 sequences, the bacterial super-kingdom, 16 different phyla, 39 classes, 63 orders, 107 families, 187 genera-level phylotypes. O. viverrini, a fluke with the most pronounced carcinogenic potential, has the strongest impact on the host bile microbiome, changing the abundance of 92 features, including Bifidobacteriaceae, Erysipelotrichaceae, [Paraprevotellaceae], Acetobacteraceae, Coriobacteraceae and Corynebacteriaceae bacterial species. All three infections significantly increased Enterobacteriaceae abundance in host bile, reduced the level of commensal bacteria in the gut microbiome (Parabacteroides, Roseburia, and AF12).CONCLUSIONS/SIGNIFICANCE: O. felineus, O. viverrini, and C. sinensis infections cause both general and species-specific qualitative and quantitative changes in the composition of microbiota of bile and colon feces of experimental animals infected with these trematodes. The alterations primarily concern the abundance of individual features and the phylogenetic diversity of microbiomes of infected hamsters.

AB - BACKGROUND: Opisthorchis felineus, Opisthorchis viverrini and Clonorchis sinensis are epidemiologically significant food-borne trematodes endemic to diverse climatic areas. O. viverrini and C. sinensis are both recognized to be 1A group of biological carcinogens to human, whereas O. felineus is not. The mechanisms of carcinogenesis by the liver flukes are studied fragmentarily, the role of host and parasite microbiome is an unexplored aspect.METHODOLOGY/PRINCIPAL FINDINGS: Specific pathogen free Mesocricetus auratus hamsters were infected with C. sinensis, O. viverrini and O. felineus. The microbiota of the adult worms, colon feces and bile from the hamsters was investigated using Illumina-based sequencing targeting the prokaryotic 16S rRNA gene. The analysis of 43 libraries revealed 18,830,015 sequences, the bacterial super-kingdom, 16 different phyla, 39 classes, 63 orders, 107 families, 187 genera-level phylotypes. O. viverrini, a fluke with the most pronounced carcinogenic potential, has the strongest impact on the host bile microbiome, changing the abundance of 92 features, including Bifidobacteriaceae, Erysipelotrichaceae, [Paraprevotellaceae], Acetobacteraceae, Coriobacteraceae and Corynebacteriaceae bacterial species. All three infections significantly increased Enterobacteriaceae abundance in host bile, reduced the level of commensal bacteria in the gut microbiome (Parabacteroides, Roseburia, and AF12).CONCLUSIONS/SIGNIFICANCE: O. felineus, O. viverrini, and C. sinensis infections cause both general and species-specific qualitative and quantitative changes in the composition of microbiota of bile and colon feces of experimental animals infected with these trematodes. The alterations primarily concern the abundance of individual features and the phylogenetic diversity of microbiomes of infected hamsters.

UR - https://www.scopus.com/record/display.uri?eid=2-s2.0-85148963593&origin=inward&txGid=121c07c5af6219193ad12ba15c3ff312

UR - https://www.mendeley.com/catalogue/ee6c4089-969f-34a0-bec1-f7c6bbd22f5c/

U2 - 10.1371/journal.pntd.0011111

DO - 10.1371/journal.pntd.0011111

M3 - Article

C2 - 36780567

VL - 17

JO - PLoS neglected tropical diseases

JF - PLoS neglected tropical diseases

SN - 1935-2727

IS - 2

M1 - e0011111

ER -