Research and application of human gut bacteriophage
Author:
  • Article
  • | |
  • Metrics
  • |
  • Reference [91]
  • |
  • Related
  • | | |
  • Comments
    Abstract:

    The gut is the largest reservoir of human flora. In the last decade, with the increasing investigations on the relationships between gut microbiota and human health diseases, gut bacteriophage has also drawn more attention. However, the research of gut bacteriophage is still in its infancy, hampered by delayed progress in the experimental and bioinformatical technology for gut bacteriophage and virome. Thus, this review first summarizes the research methodology of gut bacteriophage in computation and experiments, including sequening analysis and phage isolation, etc. Then, phage taxonomy, phage-host interactions, and the clinical applications of gut bacteriophage are also discussed. Finally, this review looks forward to the challenges and opportunities for gut bacteriophage research in data and physical resources, bioinformatical and experimental technology, interactions with intestinal bacteria, interventions on human diseases, etc.

    Reference
    [1] Baquero F, Nombela C. The microbiome as a human organ[J]. Clinical Microbiology and Infection, 2012, 18:2-4
    [2] Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body[J]. PLoS Biology, 2016, 14(8):e1002533
    [3] Borderes M, Gasc C, Prestat E, Galvão Ferrarini M, Vinga S, Boucinha L, Sagot MF. A comprehensive evaluation of binning methods to recover human gut microbial species from a non-redundant reference gene catalog[J]. NAR Genomics and Bioinformatics, 2021, 3(1):lqab009
    [4] Liu RX, Hong J, Xu XQ, Feng Q, Zhang DY, Gu YY, Shi J, Zhao SQ, Liu W, Wang XK, et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention[J]. Nature Medicine, 2017, 23(7):859-868
    [5] Forslund K, Hildebrand F, Nielsen T, Falony G, Le Chatelier E, Sunagawa S, Prifti E, Vieira-Silva S, Gudmundsdottir V, Pedersen HK, et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota[J]. Nature, 2015, 528(7581):262-266
    [6] Jie ZY, Xia HH, Zhong SL, Feng Q, Li SH, Liang SS, Zhong HZ, Liu ZP, Gao Y, Zhao H, et al. The gut microbiome in atherosclerotic cardiovascular disease[J]. Nature Communications, 2017, 8:845
    [7] Yu J, Feng Q, Wong SH, Zhang DY, Liang QY, Qin YW, Tang LQ, Zhao H, Stenvang J, Li YL, et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer[J]. Gut, 2017, 66(1):70-78
    [8] Feng Q, Liang SS, Jia HJ, Stadlmayr A, Tang LQ, Lan Z, Zhang DY, Xia HH, Xu XY, Jie ZY, et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence[J]. Nature Communications, 2015, 6:6528
    [9] Zhang X, Zhang DY, Jia HJ, Feng Q, Wang DH, Liang D, Wu XN, Li JH, Tang LQ, Li Y, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment[J]. Nature Medicine, 2015, 21(8):895-905
    [10] Zhang YF, Gu YY, Ren HH, Wang SJ, Zhong HZ, Zhao XJ, Ma J, Gu XJ, Xue YM, Huang S, et al. Gut microbiome-related effects of berberine and probiotics on type 2 diabetes (the PREMOTE study)[J]. Nature Communications, 2020, 11:5015
    [11] Shkoporov AN, Hill C. Bacteriophages of the human gut:the "known unknown" of the microbiome[J]. Cell Host & Microbe, 2019, 25(2):195-209
    [12] Tao WY, Zhu S. Gut virome in health and disease[J]. Journal of Biology, 2019, 36(6):1-5(in Chinese)陶万银, 朱书. 肠道病毒组与人体健康研究进展[J]. 生物学杂志, 2019, 36(6):1-5
    [13] Zhou B, Lin Y, Zhu WY. Advances in the interaction among gut phage, bacteria and host and its impacts on the animal host health[J]. Chinese Journal of Animal and Veterinary Sciences, 2019, 50(1):14-20(in Chinese)周贝, 林焱, 朱伟云. 肠道噬菌体与细菌和宿主互作及其对动物机体健康影响的研究进展[J]. 畜牧兽医学报, 2019, 50(1):14-20
    [14] Wang Y, Chen Q. Intestinal phageome and human health[J]. Journal of Microbes and Infections, 2019, 14(5):317-322(in Chinese)王悦, 陈倩. 肠道噬菌体组与人体健康[J]. 微生物与感染, 2019, 14(5):317-322
    [15] Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J, Salamon P, Rohwer F. Metagenomic analyses of an uncultured viral community from human feces[J]. Journal of Bacteriology, 2003, 185(20):6220-6223
    [16] Roux S, Enault F, Hurwitz BL, Sullivan MB. VirSorter:mining viral signal from microbial genomic data[J]. PeerJ, 2015, 3:e985
    [17] Ren J, Ahlgren NA, Lu YY, Fuhrman JA, Sun FZ. VirFinder:a novel k-mer based tool for identifying viral sequences from assembled metagenomic data[J]. Microbiome, 2017, 5(1):69
    [18] Zou YQ, Xue WB, Luo GW, Deng ZQ, Qin PP, Guo RJ, Sun HP, Xia Y, Liang SS, Dai Y, et al. 1, 520 reference genomes from cultivated human gut bacteria enable functional microbiome analyses[J]. Nature Biotechnology, 2019, 37(2):179-185
    [19] Forster SC, Kumar N, Anonye BO, Almeida A, Viciani E, Stares MD, Dunn M, Mkandawire TT, Zhu A, Shao Y, et al. A human gut bacterial genome and culture collection for improved metagenomic analyses[J]. Nature Biotechnology, 2019, 37(2):186-192
    [20] Liu C, Du MX, Abuduaini R, Yu HY, Li DH, Wang YJ, Zhou N, Jiang MZ, Niu PX, Han SS, et al. Enlightening the taxonomy darkness of human gut microbiomes with a cultured biobank[J]. Microbiome, 2021, 9(1):119
    [21] Hryckowian AJ, Merrill BD, Porter NT, Van Treuren W, Nelson EJ, Garlena RA, Russell DA, Martens EC, Sonnenburg JL. Bacteroides thetaiotaomicron-infecting bacteriophage isolates inform sequence-based host range predictions[J]. Cell Host & Microbe, 2020, 28(3):371-379
    [22] Porter NT, Hryckowian AJ, Merrill BD, Fuentes JJ, Gardner JO, Glowacki RWP, Singh S, Crawford RD, Snitkin ES, Sonnenburg JL, et al. Phase-variable capsular polysaccharides and lipoproteins modify bacteriophage susceptibility in Bacteroides thetaiotaomicron[J]. Nature Microbiology, 2020, 5(9):1170-1181
    [23] Shkoporov AN, Khokhlova EV, Fitzgerald CB, Stockdale SR, Draper LA, Ross RP, Hill C. ΦCrAss001 represents the most abundant bacteriophage family in the human gut and infects Bacteroides intestinalis[J]. Nature Communications, 2018, 9:4781
    [24] Guerin E, Shkoporov AN, Stockdale SR, Comas JC, Khokhlova EV, Clooney AG, Daly KM, Draper LA, Stephens N, Scholz D, et al. Isolation and characterisation of ΦcrAss002, a crAss-like phage from the human gut that infects Bacteroides xylanisolvens[J]. Microbiome, 2021, 9(1):89
    [25] Shkoporov AN, Clooney AG, Sutton TDS, Ryan FJ, Daly KM, Nolan JA, McDonnell SA, Khokhlova EV, Draper LA, Forde A, et al. The human gut virome is highly diverse, stable, and individual specific[J]. Cell Host & Microbe, 2019, 26(4):527-541
    [26] Gregory AC, Zablocki O, Zayed AA, Howell A, Bolduc B, Sullivan MB. The gut virome database reveals age-dependent patterns of virome diversity in the human gut[J]. Cell Host & Microbe, 2020, 28(5):724-740
    [27] Ma YF, You XY, Mai GQ, Tokuyasu T, Liu CL. A human gut phage catalog correlates the gut phageome with type 2 diabetes[J]. Microbiome, 2018, 6(1):24
    [28] Minot S, Sinha R, Chen J, Li HZ, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD. The human gut virome:inter-individual variation and dynamic response to diet[J]. Genome Research, 2011, 21(10):1616-1625
    [29] Zuo T, Sun Y, Wan YT, Yeoh YK, Zhang F, Cheung CP, Chen N, Luo J, Wang W, Sung JJY, et al. Human-gut-DNA virome variations across geography, ethnicity, and urbanization[J]. Cell Host & Microbe, 2020, 28(5):741-751
    [30] Seo SU, Kweon MN. Virome-host interactions in intestinal health and disease[J]. Current Opinion in Virology, 2019, 37:63-71
    [31] Liang GX, Zhao CY, Zhang HJ, Mattei L, Sherrill-Mix S, Bittinger K, Kessler LR, Wu GD, Baldassano RN, DeRusso P, et al. The stepwise assembly of the neonatal virome is modulated by breastfeeding[J]. Nature, 2020, 581(7809):470-474
    [32] Bäckhed F, Roswall J, Peng YQ, Feng Q, Jia HJ, Kovatcheva-Datchary P, Li Y, Xia Y, Xie HL, Zhong HZ, et al. Dynamics and stabilization of the human gut microbiome during the first year of life[J]. Cell Host & Microbe, 2015, 17(5):690-703
    [33] Clooney AG, Sutton TDS, Shkoporov AN, Holohan RK, Daly KM, O'Regan O, Ryan FJ, Draper LA, Plevy SE, Ross RP, et al. Whole-virome analysis sheds light on viral dark matter in inflammatory bowel disease[J]. Cell Host & Microbe, 2019, 26(6):764-778
    [34] Camarillo-Guerrero LF, Almeida A, Rangel-Pineros G, Finn RD, Lawley TD. Massive expansion of human gut bacteriophage diversity[J]. Cell, 2021, 184(4):1098-1109.e9
    [35] Benler S, Yutin N, Antipov D, Rayko M, Shmakov S, Gussow AB, Pevzner P, Koonin EV. Thousands of previously unknown phages discovered in whole-community human gut metagenomes[J]. Microbiome, 2021, 9(1):78
    [36] Chen SF, Zhou YQ, Chen YR, Gu J. Fastp:an ultra-fast all-in-one FASTQ preprocessor[J]. Bioinformatics, 2018, 34(17):i884-i890
    [37] Bolger AM, Lohse M, Usadel B. Trimmomatic:a flexible trimmer for Illumina sequence data[J]. Bioinformatics, 2014, 30(15):2114-2120
    [38] Chen YX, Chen YS, Shi CM, Huang ZB, Zhang Y, Li SK, Li Y, Ye J, Yu C, Li Z, et al. SOAPnuke:a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data[J]. GigaScience, 2018, 7(1):gix120
    [39] Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes:a new versatile metagenomic assembler[J]. Genome Research, 2017, 27(5):824-834
    [40] Li DH, Luo RB, Liu CM, Leung CM, Ting HF, Sadakane K, Yamashita H, Lam TW. MEGAHIT v1.0:a fast and scalable metagenome assembler driven by advanced methodologies and community practices[J]. Methods, 2016, 102:3-11
    [41] Fu LM, Niu BF, Zhu ZW, Wu ST, Li WZ. CD-HIT:accelerated for clustering the next-generation sequencing data[J]. Bioinformatics, 2012, 28(23):3150-3152
    [42] Truong DT, Franzosa EA, Tickle TL, Scholz M, Weingart G, Pasolli E, Tett A, Huttenhower C, Segata N. MetaPhlAn2 for enhanced metagenomic taxonomic profiling[J]. Nature Methods, 2015, 12(10):902-903
    [43] Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2[J]. Genome Biology, 2019, 20(1):257
    [44] Guo JR, Bolduc B, Zayed AA, Varsani A, Dominguez-Huerta G, Delmont TO, Pratama AA, Gazitúa MC, Vik D, Sullivan MB, et al. VirSorter2:a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses[J]. Microbiome, 2021, 9(1):37
    [45] Zheng TT, Li J, Ni YQ, Kang K, Misiakou MA, Imamovic L, Chow BKC, Rode AA, Bytzer P, Sommer M, et al. Mining, analyzing, and integrating viral signals from metagenomic data[J]. Microbiome, 2019, 7(1):42
    [46] Zhao GY, Wu G, Lim ES, Droit L, Krishnamurthy S, Barouch DH, Virgin HW, Wang D. VirusSeeker, a computational pipeline for virus discovery and virome composition analysis[J]. Virology, 2017, 503:21-30
    [47] Roux S, Tournayre J, Mahul A, Debroas D, Enault F. Metavir 2:new tools for viral metagenome comparison and assembled virome analysis[J]. BMC Bioinformatics, 2014, 15:76
    [48] Song WC, Sun HX, Zhang C, Cheng L, Peng Y, Deng ZQ, Wang D, Wang Y, Hu M, Liu W, et al. Prophage Hunter:An integrative hunting tool for active prophages[J]. Nucleic Acids Research, 2019, 47(W1):W74-W80
    [49] Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang YJ, Wishart DS. PHASTER:a better, faster version of the PHAST phage search tool[J]. Nucleic Acids Research, 2016, 44(W1):W16-W21
    [50] Nayfach S, Camargo AP, Schulz F, Eloe-Fadrosh E, Roux S, Kyrpides NC. CheckV assesses the quality and completeness of metagenome-assembled viral genomes[J]. Nature Biotechnology, 2021, 39(5):578-585
    [51] Bolduc B, Jang HB, Doulcier G, You ZQ, Roux S, Sullivan MB. vConTACT:an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria[J]. PeerJ, 2017, 5:e3243
    [52] Jang HB, Bolduc B, Zablocki O, Kuhn JH, Roux S, Adriaenssens EM, Brister JR, Kropinski AM, Krupovic M, Lavigne R, et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks[J]. Nature Biotechnology, 2019, 37(6):632-639
    [53] Couvin D, Bernheim A, Toffano-Nioche C, Touchon M, Michalik J, Néron B, Rocha EPC, Vergnaud G, Gautheret D, Pourcel C. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins[J]. Nucleic Acids Research, 2018, 46(W1):W246-W251
    [54] Zhang F, 17-728
    [91] Kabwe M, Dashper S, Bachrach G, Tucci J. Bacteriophage manipulation of the microbiome associated with tumour microenvironments-can this improve cancer therapeutic response?[J]. FEMS Microbiology Reviews, 2021. DOI:doi.org/10.1093/femsre/fuab017
    [92] Dong X, Pan P, Zheng DW, Bao P, Zeng X, Zhang XZ. Bioinorganic hybrid bacteriophage for modulation of intestinal microbiota to remodel tumor-immune microenvironment against colorectal cancer[J]. Science Advances, 2020, 6(20):eaba1590
    [93] Wong SH, Yu J. Gut microbiota in colorectal cancer:mechanisms of action and clinical applications[J]. Nature Reviews Gastroenterology & Hepatology, 2019, 16(11):690-704
    [94] Zhu F, Ju YM, Wang W, Wang Q, Guo RJ, Ma QY, Sun Q, Fan YJ, Xie YY, Yang Z, et al. Metagenome-wide association of gut microbiome features for schizophrenia[J]. Nature Communications, 2020, 11(1):1612
    [95] Atarashi K, Suda W, Luo CW, Kawaguchi T, Motoo I, Narushima S, Kiguchi Y, Yasuma K, Watanabe E, Tanoue T, et al. Ectopic colonization of oral bacteria in the intestine drives TH1 cell induction and inflammation[J]. Science, 2017, 358(6361):359-365
    [96] Yang FM, Sun JH, Luo HN, Ren HH, Zhou HC, Lin YX, Han M, Chen B, Liao HL, Brix S, et al. Assessment of fecal DNA extraction protocols for metagenomic studies[J]. GigaScience, 2020, 9(7):giaa071v, 2018. DOI:10.1101/479105
    [60] Roux S, Páez-Espino D, Chen IMA, Palaniappan K, Ratner A, Chu K, Reddy TBK, Nayfach S, Schulz F, Call L, et al. IMG/VR v3:an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses[J]. Nucleic Acids Research, 2021, 49(D1):D764-D775
    [61] O'Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, Rajput B, Robbertse B, Smith-White B, Ako-Adjei D, et al. Reference sequence (RefSeq) database at NCBI:current status, taxonomic expansion, and functional annotation[J]. Nucleic Acids Research, 2016, 44(D1):D733-D745
    [62] Marbouty M, Thierry A, Koszul R. Phages-bacteria interactions network of the healthy human gut[J]. bioRxiv, 2020. DOI:10.1101/2020.05.13.093716
    [63] Alawi M, Burkhardt L, Indenbirken D, Reumann K, Christopeit M, Kröger N, Lütgehetmann M, Aepfelbacher M, Fischer N, Grundhoff A. DAMIAN:an open source bioinformatics tool for fast, systematic and cohort based analysis of microorganisms in diagnostic samples[J]. Scientific Reports, 2019, 9:16841
    [64] Guerin E, Hill C. Shining light on human gut bacteriophages[J]. Frontiers in Cellular and Infection Microbiology, 2020, 10:481
    [65] Qin XY, Yang HJ. Research progress on techniques for separation, purification of bacteriophages[J]. China Biotechnology, 2020, 40(5):78-83(in Chinese)秦旭颖, 杨洪江. 噬菌体分离纯化技术研究进展[J]. 中国生物工程杂志, 2020, 40(5):78-83
    [66] Soleimani-Delfan A, Bouzari M, Wang R. A rapid competitive method for bacteriophage genomic DNA extraction[J]. Journal of Virological Methods, 2021, 293:114148
    [67] 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[J]. Research in Microbiology, 2014, 165(10):803-812
    [68] Sutton TDS, Hill C. Gut bacteriophage:current understanding and challenges[J]. Frontiers in Endocrinology, 2019, 10:784
    [69] Roux S, Adriaenssens EM, Dutilh BE, Koonin EV, Kropinski AM, Krupovic M, Kuhn JH, Lavigne R, Brister JR, Varsani A, et al. Minimum information about an uncultivated virus genome (MIUViG)[J]. Nature Biotechnology, 2019, 37(1):29-37
    [70] Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GGZ, Boling LC, Barr JJ, Speth DR, Seguritan V, Aziz RK, et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes[J]. Nature Communications, 2014, 5:4498
    [71] Devoto AE, Santini JM, Olm MR, Anantharaman K, Munk P, Tung J, Archie EA, Turnbaugh PJ, Seed KD, Blekhman R, et al. Megaphages infect Prevotella and variants are widespread in gut microbiomes[J]. Nature Microbiology, 2019, 4(4):693-700
    [72] Hobbs Z, Abedon ST. Diversity of phage infection types and associated terminology:the problem with ‘Lytic or lysogenic’[J]. FEMS Microbiology Letters, 2016, 363(7):fnw047
    [73] Mirzaei MK, Maurice CF. Ménage à trois in the human gut:interactions between host, bacteria and phages[J]. Nature Reviews Microbiology, 2017, 15(7):397-408
    [74] Silveira CB, Rohwer FL. Piggyback-the-Winner in host-associated microbial communities[J]. NPJ Biofilms and Microbiomes, 2016, 2:16010
    [75] Knowles B, Silveira CB, Bailey BA, Barott K, Cantu VA, Cobián-Güemes AG, Coutinho FH, Dinsdale EA, Felts B, Furby KA, et al. Lytic to temperate switching of viral communities[J]. Nature, 2016, 531(7595):466-470
    [76] Breitbart M, Bonnain C, Malki K, Sawaya NA. Phage puppet Masters of the marine microbial realm[J]. Nature Microbiology, 2018, 3(7):754-766
    [77] Lourenço M, Chaffringeon L, Lamy-Besnier Q, Pédron T, Campagne P, Eberl C, Bérard M, Stecher B, Debarbieux L, De Sordi L. The spatial heterogeneity of the gut limits predation and fosters coexistence of bacteria and bacteriophages[J]. Cell Host & Microbe, 2020, 28(3):390-401.e5
    [78] Jiang XF, Hall AB, Arthur TD, Plichta DR, Covington CT, Poyet M, Crothers J, Moses PL, Tolonen AC, Vlamakis H, et al. Invertible promoters mediate bacterial phase variation, antibiotic resistance, and host adaptation in the gut[J]. Science, 2019, 363(6423):181-187
    [79] Oh JH, Lin XB, Zhang SW, Tollenaar SL, Özçam M, Dunphy C, Walter J, Van Pijkeren JP. Prophages in Lactobacillus reuteri are associated with fitness trade-offs but can increase competitiveness in the gut ecosystem[J]. Applied and Environmental Microbiology, 2019. DOI:10.1128/aem.01922-19
    [80] Kreuzer KN. DNA damage responses in prokaryotes:Regulating gene expression, modulating growth patterns, and manipulating replication forks[J]. Cold Spring Harbor Perspectives in Biology, 2013, 5(11):a012674
    [81] Manrique P, Dills M, Young M. The human gut phage community and its implications for health and disease[J]. Viruses, 2017, 9(6):141
    [82] Hu Q, Liu C, Zhang D, Wang R, Qin LL, Xu Q, Che LQ, Gao F. Effects of low-dose antibiotics on gut immunity and antibiotic resistomes in weaned piglets[J]. Frontiers in Immunology, 2020, 11:903
    [83] 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[J]. Cell Host & Microbe, 2019, 25(6):803-814
    [84] Campbell DE, Ly LK, Ridlon JM, Hsiao A, Whitaker RJ, Degnan PH. Infection with Bacteroides phage BV01 alters the host transcriptome and bile acid metabolism in a common human gut microbe[J]. Cell Reports, 2020, 32(11):108142
    [85] Wahida A, Tang F, Barr JJ. Rethinking phage-bacteria- eukaryotic relationships and their influence on human health[J]. Cell Host & Microbe, 2021, 29(5):681-688
    [86] Galtier M, Sordi LD, Sivignon A, De Vallée A, Maura D, Neut C, Rahmouni O, Wannerberger K, Darfeuille-Michaud A, Desreumaux P, et al. Bacteriophages targeting adherent invasive Escherichia coli strains as a promising new treatment for Crohn's disease[J]. Journal of Crohn's and Colitis, 2017, 11(7):840-847
    [87] Small CLN, Reid-Yu SA, McPhee JB, Coombes BK. Persistent infection with Crohn's disease-associated adherent-invasive Escherichia coli leads to chronic inflammation and intestinal fibrosis[J]. Nature Communications, 2013, 4:1957
    [88] Duan Y, Llorente C, Lang S, Brandl K, Chu HK, Jiang L, White RC, Clarke TH, Nguyen K, Torralba M, et al. Bacteriophage targeting of gut bacterium attenuates alcoholic liver disease[J]. Nature, 2019, 575(7783):505-511
    [89] Yuan J, Chen C, Cui JH, Lu J, Yan C, Wei X, Zhao XN, Li NN, Li SL, Xue GH, et al. Fatty liver disease caused by high-alcohol-producing Klebsiella pneumoniae[J]. Cell Metabolism, 2019, 30(4):675-688.e7
    [90] Zheng DW, Dong X, Pan P, Chen KW, Fan JX, Cheng SX, Zhang XZ. Phage-guided modulation of the gut microbiota of mouse models of colorectal cancer augments their responses to chemotherapy[J]. Nature Biomedical Engineering, 2019, 3(9):7
    Related
    Cited by
    Comments
    Comments
    分享到微博
    Submit
Get Citation

LIU Cong, XING Bo, CHEN Wantong, LI Junhua, XIAO Minfeng. Research and application of human gut bacteriophage[J]. Microbiology China, 2021, 48(9): 3314-3329

Copy
Share
Article Metrics
  • Abstract:
  • PDF:
  • HTML:
  • Cited by:
History
  • Received:May 29,2021
  • Adopted:August 04,2021
  • Online: September 08,2021
Article QR Code