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Published in: Gut Pathogens 1/2022

01-12-2022 | Liver Cirrhosis | Research

Investigation and characterization of human gut phageome in advanced liver cirrhosis of defined etiologies

Authors: Mohadeseh Naseri, Fahimeh Palizban, Abbas Yadegar, Mohsen Khodarahmi, Hamid Asadzadeh Aghdaei, Hamidreza Houri, Javad Zahiri

Published in: Gut Pathogens | Issue 1/2022

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Abstract

Background

Liver cirrhosis is a major public health problem, accounting for high rates of morbidity and mortality worldwide. The cirrhosis etiology is a broad and essential step in planning a treatment strategy. Many recent studies have documented that gut microbiome alterations play a vital role in the development and progression of cirrhosis and its complications. Nevertheless, there is insufficient data on the correlation between liver cirrhosis and gut phageome alterations in patients with advanced liver diseases. This study aimed to analyze the taxonomic structure and functional attributes of the gut phageome in six different etiologies of advanced liver cirrhosis.

Methods

We first retrieved metagenomic sequencing data from three datasets of fecal samples taken from cirrhotic patients with various etiologies. Subsequently, several bioinformatics pipelines were used to analyze bacteriophage composition and determine their functionality.

Results

A gene catalog of 479,425 non-redundant genes was developed as a reference to measure gene prevalence. The results of the analysis revealed a few significant differences among the cohorts at the phage species level. However, the alternations were more evident as there were more in-depth analyses of the functional resolution of the gut phageome.

Conclusions

Our findings suggest that the functional analysis of the gut phageome would provide meaningful markers to predict the progression of liver cirrhosis and facilitate the development of novel treatment approaches.
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Literature
1.
go back to reference Cani PD. Human gut microbiome: hopes, threats and promises. Gut. 2018;67(9):1716–25.PubMed Cani PD. Human gut microbiome: hopes, threats and promises. Gut. 2018;67(9):1716–25.PubMed
2.
go back to reference Lapidot Y, Amir A, Nosenko R, Uzan-Yulzari A, Veitsman E, Cohen-Ezra O, Davidov Y, Weiss P, Bradichevski T, Segev S, et al. Alterations in the gut microbiome in the progression of cirrhosis to hepatocellular carcinoma. mSystems. 2020;5(3):e00153-e1120.PubMedPubMedCentral Lapidot Y, Amir A, Nosenko R, Uzan-Yulzari A, Veitsman E, Cohen-Ezra O, Davidov Y, Weiss P, Bradichevski T, Segev S, et al. Alterations in the gut microbiome in the progression of cirrhosis to hepatocellular carcinoma. mSystems. 2020;5(3):e00153-e1120.PubMedPubMedCentral
3.
go back to reference Anand G, Zarrinpar A, Loomba R. Targeting dysbiosis for the treatment of liver disease. Semin Liver Dis. 2016;36(1):37–47.PubMedPubMedCentral Anand G, Zarrinpar A, Loomba R. Targeting dysbiosis for the treatment of liver disease. Semin Liver Dis. 2016;36(1):37–47.PubMedPubMedCentral
4.
go back to reference Pasolli E, Truong DT, Malik F, Waldron L, Segata N. Machine learning meta-analysis of large metagenomic datasets: tools and biological insights. PLoS Comput Biol. 2016;12(7):e1004977.PubMedPubMedCentral Pasolli E, Truong DT, Malik F, Waldron L, Segata N. Machine learning meta-analysis of large metagenomic datasets: tools and biological insights. PLoS Comput Biol. 2016;12(7):e1004977.PubMedPubMedCentral
5.
go back to reference Asrani SK, Devarbhavi H, Eaton J, Kamath PS. Burden of liver diseases in the world. J Hepatol. 2019;70(1):151–71.PubMed Asrani SK, Devarbhavi H, Eaton J, Kamath PS. Burden of liver diseases in the world. J Hepatol. 2019;70(1):151–71.PubMed
6.
go back to reference Sarin SK, Choudhury A. Acute-on-chronic liver failure: terminology, mechanisms and management. Nat Rev Gastroenterol Hepatol. 2016;13(3):131–49.CrossRefPubMed Sarin SK, Choudhury A. Acute-on-chronic liver failure: terminology, mechanisms and management. Nat Rev Gastroenterol Hepatol. 2016;13(3):131–49.CrossRefPubMed
7.
go back to reference Pinzani M, Rosselli M, Zuckermann M. Liver cirrhosis. Best Pract Res Clin Gastroenterol. 2011;25(2):281–90.PubMed Pinzani M, Rosselli M, Zuckermann M. Liver cirrhosis. Best Pract Res Clin Gastroenterol. 2011;25(2):281–90.PubMed
8.
go back to reference Acharya C, Bajaj JS. Altered microbiome in patients with cirrhosis and complications. Clin Gastroenterol Hepatol. 2019;17(2):307–21.PubMed Acharya C, Bajaj JS. Altered microbiome in patients with cirrhosis and complications. Clin Gastroenterol Hepatol. 2019;17(2):307–21.PubMed
9.
go back to reference Oikonomou T, Papatheodoridis G, Samarkos M, Goulis I, Cholongitas E. Clinical impact of microbiome in patients with decompensated cirrhosis. World J Gastroenterol. 2018;24:3813–20.PubMedPubMedCentral Oikonomou T, Papatheodoridis G, Samarkos M, Goulis I, Cholongitas E. Clinical impact of microbiome in patients with decompensated cirrhosis. World J Gastroenterol. 2018;24:3813–20.PubMedPubMedCentral
10.
go back to reference Loomba R, Seguritan V, Li W, Long T, Klitgord N, Bhatt A, Dulai PS, Caussy C, Bettencourt R, Highlander SK, et al. Gut microbiome-based metagenomic signature for non-invasive detection of advanced fibrosis in human nonalcoholic fatty liver disease. Cell Metab. 2017;25(5):1054-1062.e1055.PubMedPubMedCentral Loomba R, Seguritan V, Li W, Long T, Klitgord N, Bhatt A, Dulai PS, Caussy C, Bettencourt R, Highlander SK, et al. Gut microbiome-based metagenomic signature for non-invasive detection of advanced fibrosis in human nonalcoholic fatty liver disease. Cell Metab. 2017;25(5):1054-1062.e1055.PubMedPubMedCentral
11.
go back to reference Zhao Y, Zhou J, Liu J, Wang Z, Chen M, Zhou S. Metagenome of gut microbiota of children with nonalcoholic fatty liver disease. Front Pediatr. 2019;7:518–518.PubMedPubMedCentral Zhao Y, Zhou J, Liu J, Wang Z, Chen M, Zhou S. Metagenome of gut microbiota of children with nonalcoholic fatty liver disease. Front Pediatr. 2019;7:518–518.PubMedPubMedCentral
12.
go back to reference Wylie KM, Weinstock GM, Storch GA. Emerging view of the human virome. Transl Res J Lab Clin Med. 2012;160(4):283–90. Wylie KM, Weinstock GM, Storch GA. Emerging view of the human virome. Transl Res J Lab Clin Med. 2012;160(4):283–90.
13.
go back to reference Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, Rubin E, Ivanova NN, Kyrpides NC. Uncovering earth’s virome. Nature. 2016;536(7617):425–30.PubMed Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, Rubin E, Ivanova NN, Kyrpides NC. Uncovering earth’s virome. Nature. 2016;536(7617):425–30.PubMed
14.
go back to reference Norman Jason M, Handley Scott A, Baldridge Megan T, Droit L, Liu Catherine Y, Keller Brian C, Kambal A, Monaco Cynthia L, Zhao G, Fleshner P, et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell. 2015;160(3):447–60.PubMedPubMedCentral Norman Jason M, Handley Scott A, Baldridge Megan T, Droit L, Liu Catherine Y, Keller Brian C, Kambal A, Monaco Cynthia L, Zhao G, Fleshner P, et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell. 2015;160(3):447–60.PubMedPubMedCentral
15.
go back to reference Shkoporov AN, Hill C. Bacteriophages of the human gut: the “known unknown” of the microbiome. Cell Host Microbe. 2019;25(2):195–209.PubMed Shkoporov AN, Hill C. Bacteriophages of the human gut: the “known unknown” of the microbiome. Cell Host Microbe. 2019;25(2):195–209.PubMed
16.
go back to reference d’Humières C, Touchon M, Dion S, Cury J, Ghozlane A, Garcia-Garcera M, Bouchier C, Ma L, Denamur E, Rocha EPC. A simple, reproducible and cost-effective procedure to analyse gut phageome: from phage isolation to bioinformatic approach. Sci Rep. 2019;9(1):11331.PubMedPubMedCentral d’Humières C, Touchon M, Dion S, Cury J, Ghozlane A, Garcia-Garcera M, Bouchier C, Ma L, Denamur E, Rocha EPC. A simple, reproducible and cost-effective procedure to analyse gut phageome: from phage isolation to bioinformatic approach. Sci Rep. 2019;9(1):11331.PubMedPubMedCentral
17.
go back to reference Manrique P, Bolduc B, Walk ST, van der Oost J, de Vos WM, Young MJ. Healthy human gut phageome. Proc Natl Acad Sci USA. 2016;113(37):10400–5.PubMedPubMedCentral Manrique P, Bolduc B, Walk ST, van der Oost J, de Vos WM, Young MJ. Healthy human gut phageome. Proc Natl Acad Sci USA. 2016;113(37):10400–5.PubMedPubMedCentral
18.
go back to reference Hoyles L, McCartney AL, Neve H, Gibson GR, Sanderson JD, Heller KJ, van Sinderen D. Characterization of virus-like particles associated with the human faecal and caecal microbiota. Res Microbiol. 2014;165(10):803–12.PubMed Hoyles L, McCartney AL, Neve H, Gibson GR, Sanderson JD, Heller KJ, van Sinderen D. Characterization of virus-like particles associated with the human faecal and caecal microbiota. Res Microbiol. 2014;165(10):803–12.PubMed
19.
go back to reference Sausset R, Petit MA, Gaboriau-Routhiau V, De Paepe M. New insights into intestinal phages. Mucosal Immunol. 2020;13(2):205–15.PubMedPubMedCentral Sausset R, Petit MA, Gaboriau-Routhiau V, De Paepe M. New insights into intestinal phages. Mucosal Immunol. 2020;13(2):205–15.PubMedPubMedCentral
20.
go back to reference Monaco Cynthia L, Gootenberg David B, Zhao G, Handley Scott A, Ghebremichael Musie S, Lim Efrem S, Lankowski A, Baldridge Megan T, Wilen Craig B, Flagg M, et al. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome. Cell Host Microbe. 2016;19(3):311–22.PubMedPubMedCentral Monaco Cynthia L, Gootenberg David B, Zhao G, Handley Scott A, Ghebremichael Musie S, Lim Efrem S, Lankowski A, Baldridge Megan T, Wilen Craig B, Flagg M, et al. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome. Cell Host Microbe. 2016;19(3):311–22.PubMedPubMedCentral
21.
go back to reference Reyes A, Blanton LV, Cao S, Zhao G, Manary M, Trehan I, Smith MI, Wang D, Virgin HW, Rohwer F, et al. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc Natl Acad Sci USA. 2015;112(38):11941–6.PubMedPubMedCentral Reyes A, Blanton LV, Cao S, Zhao G, Manary M, Trehan I, Smith MI, Wang D, Virgin HW, Rohwer F, et al. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc Natl Acad Sci USA. 2015;112(38):11941–6.PubMedPubMedCentral
22.
go back to reference Ma Y, You X, Mai G, Tokuyasu T, Liu C. A human gut phage catalog correlates the gut phageome with type 2 diabetes. Microbiome. 2018;6(1):24.PubMedPubMedCentral Ma Y, You X, Mai G, Tokuyasu T, Liu C. A human gut phage catalog correlates the gut phageome with type 2 diabetes. Microbiome. 2018;6(1):24.PubMedPubMedCentral
23.
go back to reference Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, Arumugam M, Kultima JR, Prifti E, Nielsen T, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32(8):834–41.PubMed Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, Arumugam M, Kultima JR, Prifti E, Nielsen T, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32(8):834–41.PubMed
24.
go back to reference Qin N, Yang F, Li A, Prifti E, Chen Y, Shao L, Guo J, Le Chatelier E, Yao J, Wu L, et al. Alterations of the human gut microbiome in liver cirrhosis. Nature. 2014;513(7516):59–64.PubMed Qin N, Yang F, Li A, Prifti E, Chen Y, Shao L, Guo J, Le Chatelier E, Yao J, Wu L, et al. Alterations of the human gut microbiome in liver cirrhosis. Nature. 2014;513(7516):59–64.PubMed
25.
go back to reference Tyakht AV, Dubinkina VB, Odintsova VY, Yarygin KS, Kovarsky BA, Pavlenko AV, Ischenko DS, Popenko AS, Alexeev DG, Taraskina AY, et al. Data on gut metagenomes of the patients with alcoholic dependence syndrome and alcoholic liver cirrhosis. Data Brief. 2017;11:98–102.PubMedPubMedCentral Tyakht AV, Dubinkina VB, Odintsova VY, Yarygin KS, Kovarsky BA, Pavlenko AV, Ischenko DS, Popenko AS, Alexeev DG, Taraskina AY, et al. Data on gut metagenomes of the patients with alcoholic dependence syndrome and alcoholic liver cirrhosis. Data Brief. 2017;11:98–102.PubMedPubMedCentral
26.
go back to reference Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40.PubMed Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40.PubMed
28.
go back to reference Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47–e47.PubMedPubMedCentral Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47–e47.PubMedPubMedCentral
29.
go back to reference Tithi SS, Aylward FO, Jensen RV, Zhang L. FastViromeExplorer: a pipeline for virus and phage identification and abundance profiling in metagenomics data. PeerJ. 2018;6:e4227.PubMedPubMedCentral Tithi SS, Aylward FO, Jensen RV, Zhang L. FastViromeExplorer: a pipeline for virus and phage identification and abundance profiling in metagenomics data. PeerJ. 2018;6:e4227.PubMedPubMedCentral
30.
go back to reference Li D, Liu C-M, Luo R, Sadakane K, Lam T-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31(10):1674–6.PubMed Li D, Liu C-M, Luo R, Sadakane K, Lam T-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31(10):1674–6.PubMed
31.
go back to reference Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007;35(suppl_2):W52–7.PubMedPubMedCentral Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007;35(suppl_2):W52–7.PubMedPubMedCentral
32.
go back to reference Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12(1):59–60.PubMed Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12(1):59–60.PubMed
33.
go back to reference Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics (Oxford, England). 2012;28(23):3150–2. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics (Oxford, England). 2012;28(23):3150–2.
34.
go back to reference Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci. 2003;14(6):927–30. Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci. 2003;14(6):927–30.
35.
go back to reference McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8(4):e61217.PubMedPubMedCentral McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8(4):e61217.PubMedPubMedCentral
36.
go back to reference Wickham H. ggplot2. Wiley Interdiscip Rev Comput Stat. 2011;3(2):180–5. Wickham H. ggplot2. Wiley Interdiscip Rev Comput Stat. 2011;3(2):180–5.
37.
go back to reference Lee W-P, Stromberg MP, Ward A, Stewart C, Garrison EP, Marth GT. MOSAIK: a hash-based algorithm for accurate next-generation sequencing short-read mapping. PLoS ONE. 2014;9(3):e90581.PubMedPubMedCentral Lee W-P, Stromberg MP, Ward A, Stewart C, Garrison EP, Marth GT. MOSAIK: a hash-based algorithm for accurate next-generation sequencing short-read mapping. PLoS ONE. 2014;9(3):e90581.PubMedPubMedCentral
38.
go back to reference Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078–9.PubMedPubMedCentral Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078–9.PubMedPubMedCentral
39.
go back to reference Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016;428(4):726–31.PubMed Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016;428(4):726–31.PubMed
40.
go back to reference Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, et al. The COG database: an updated version includes eukaryotes. BMC Bioinform. 2003;4:41. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, et al. The COG database: an updated version includes eukaryotes. BMC Bioinform. 2003;4:41.
41.
go back to reference Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, et al. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 2016;44(D1):D286–93.PubMed Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, et al. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 2016;44(D1):D286–93.PubMed
42.
go back to reference Sonnhammer ELL, Eddy SR, Birney E, Bateman A, Durbin R. Pfam: Multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res. 1998;26(1):320–2.PubMedPubMedCentral Sonnhammer ELL, Eddy SR, Birney E, Bateman A, Durbin R. Pfam: Multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res. 1998;26(1):320–2.PubMedPubMedCentral
43.
go back to reference Marchler-Bauer A, Panchenko AR, Shoemaker BA, Thiessen PA, Geer LY, Bryant SH. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res. 2002;30(1):281–3.PubMedPubMedCentral Marchler-Bauer A, Panchenko AR, Shoemaker BA, Thiessen PA, Geer LY, Bryant SH. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res. 2002;30(1):281–3.PubMedPubMedCentral
44.
go back to reference Uchiyama T, Irie M, Mori H, Kurokawa K, Yamada T. FuncTree: functional analysis and visualization for large-scale omics data. PLoS ONE. 2015;10(5):e0126967.PubMedPubMedCentral Uchiyama T, Irie M, Mori H, Kurokawa K, Yamada T. FuncTree: functional analysis and visualization for large-scale omics data. PLoS ONE. 2015;10(5):e0126967.PubMedPubMedCentral
45.
go back to reference Tetz G, Brown SM, Hao Y, Tetz V. Parkinson’s disease and bacteriophages as its overlooked contributors. Sci Rep. 2018;8(1):10812.PubMedPubMedCentral Tetz G, Brown SM, Hao Y, Tetz V. Parkinson’s disease and bacteriophages as its overlooked contributors. Sci Rep. 2018;8(1):10812.PubMedPubMedCentral
46.
go back to reference Pérez-Brocal V, García-López R, Nos P, Beltrán B, Moret I, Moya A. Metagenomic analysis of crohn’s disease patients identifies changes in the virome and microbiome related to disease status and therapy, and detects potential interactions and biomarkers. Inflamm Bowel Dis. 2015;21(11):2515–32.PubMed Pérez-Brocal V, García-López R, Nos P, Beltrán B, Moret I, Moya A. Metagenomic analysis of crohn’s disease patients identifies changes in the virome and microbiome related to disease status and therapy, and detects potential interactions and biomarkers. Inflamm Bowel Dis. 2015;21(11):2515–32.PubMed
47.
go back to reference Knezevic P, Voet M, Lavigne R. Prevalence of Pf1-like (pro)phage genetic elements among Pseudomonas aeruginosa isolates. Virology. 2015;483:64–71.PubMed Knezevic P, Voet M, Lavigne R. Prevalence of Pf1-like (pro)phage genetic elements among Pseudomonas aeruginosa isolates. Virology. 2015;483:64–71.PubMed
48.
go back to reference Mirzaei MK, Maurice CF. Ménage à trois in the human gut: interactions between host, bacteria and phages. Nat Rev Microbiol. 2017;15(7):397–408.PubMed Mirzaei MK, Maurice CF. Ménage à trois in the human gut: interactions between host, bacteria and phages. Nat Rev Microbiol. 2017;15(7):397–408.PubMed
49.
go back to reference Manrique P, Dills M, Young MJ. The human gut phage community and its implications for health and disease. Viruses. 2017;9(6):141.PubMedCentral Manrique P, Dills M, Young MJ. The human gut phage community and its implications for health and disease. Viruses. 2017;9(6):141.PubMedCentral
50.
go back to reference Hsu BB, Gibson TE, Yeliseyev V, Liu Q, Lyon L, Bry L, Silver PA, Gerber GK. Dynamic modulation of the gut microbiota and metabolome by bacteriophages in a mouse model. Cell Host Microbe. 2019;25(6):803-814.e805.PubMedPubMedCentral Hsu BB, Gibson TE, Yeliseyev V, Liu Q, Lyon L, Bry L, Silver PA, Gerber GK. Dynamic modulation of the gut microbiota and metabolome by bacteriophages in a mouse model. Cell Host Microbe. 2019;25(6):803-814.e805.PubMedPubMedCentral
51.
go back to reference Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature. 2010;466(7304):334–8.PubMedPubMedCentral Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature. 2010;466(7304):334–8.PubMedPubMedCentral
52.
go back to reference Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GG, Boling L, Barr JJ, Speth DR, Seguritan V, Aziz RK, et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat Commun. 2014;5:4498.PubMed Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GG, Boling L, Barr JJ, Speth DR, Seguritan V, Aziz RK, et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat Commun. 2014;5:4498.PubMed
53.
go back to reference Duan Y, Llorente C, Lang S, Brandl K, Chu H, Jiang L, White RC. Bacteriophage targeting of gut bacterium attenuates alcoholic liver disease. Nature. 2019;575(7783):505–11.PubMedPubMedCentral Duan Y, Llorente C, Lang S, Brandl K, Chu H, Jiang L, White RC. Bacteriophage targeting of gut bacterium attenuates alcoholic liver disease. Nature. 2019;575(7783):505–11.PubMedPubMedCentral
Metadata
Title
Investigation and characterization of human gut phageome in advanced liver cirrhosis of defined etiologies
Authors
Mohadeseh Naseri
Fahimeh Palizban
Abbas Yadegar
Mohsen Khodarahmi
Hamid Asadzadeh Aghdaei
Hamidreza Houri
Javad Zahiri
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2022
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-022-00482-4

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