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A practical guide to amplicon and metagenomic analysis of microbiome data |
Yong-Xin Liu1,2,3( ), Yuan Qin1,2,3,4, Tong Chen5, Meiping Lu6, Xubo Qian6, Xiaoxuan Guo1,2,3, Yang Bai1,2,3,4( ) |
1. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China 2. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China 3. CAS-JIC Centre of Excellence for Plant and Microbial Science, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China 4. College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100049, China 5. National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China 6. Department of Rheumatology Immunology & Allergy, Children’s Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang Province 310053, China |
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Abstract Advances in high-throughput sequencing (HTS) have fostered rapid developments in the field of microbiome research, and massive microbiome datasets are now being generated. However, the diversity of software tools and the complexity of analysis pipelines make it difficult to access this field. Here, we systematically summarize the advantages and limitations of microbiome methods. Then, we recommend specific pipelines for amplicon and metagenomic analyses, and describe commonly-used software and databases, to help researchers select the appropriate tools. Furthermore, we introduce statistical and visualization methods suitable for microbiome analysis, including alpha- and betadiversity, taxonomic composition, difference comparisons, correlation, networks, machine learning, evolution, source tracing, and common visualization styles to help researchers make informed choices. Finally, a stepby-step reproducible analysis guide is introduced. We hope this review will allow researchers to carry out data analysis more effectively and to quickly select the appropriate tools in order to efficiently mine the biological significance behind the data.
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Keywords
metagenome
marker genes
highthroughput sequencing
pipeline
reproducible analysis
visualization
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Corresponding Author(s):
Yong-Xin Liu,Yang Bai
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Online First Date: 14 September 2020
Issue Date: 08 June 2021
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|
1 |
J Alneberg, BS Bjarnason, I de Bruijn, M Schirmer, J Quick, UZ Ijaz, L Lahti, NJ Loman, AF Andersson, C Quince (2014) Binning metagenomic contigs by coverage and composition. Nat Methods 11:1144–1146
https://doi.org/10.1038/nmeth.3103
|
2 |
M Arumugam, J Raes, E Pelletier, D Le Paslier, T Yamada, DR Mende, GR Fernandes, J, Tap T Bruls, JM Battoet al. (2011) Enterotypes of the human gut microbiome. Nature 473:174–180
https://doi.org/10.1038/nature09944
|
3 |
F Asnicar, G Weingart, TL Tickle, C Huttenhower, N Segata (2015) Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ 3:e1029
https://doi.org/10.7717/peerj.1029
|
4 |
KP Asshauer, B Wemheuer, R Daniel, P Meinicke (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882–2884
https://doi.org/10.1093/bioinformatics/btv287
|
5 |
Y, Bai DB Müller, G, Srinivas R Garrido-Oter, E Potthoff, M Rott, N Dombrowski, PC Münch , S, Spaepen M Remus-Emsermannet al. (2015) Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364–369
https://doi.org/10.1038/nature16192
|
6 |
M Bastian, S Heymann, and M Jacomy (2009). Gephi: an open source software for exploring and manipulating networks. In: Third international AAAI conference on weblogs and social media.
|
7 |
B Beckers, M Op De Beeck, N Weyens, W Boerjan, J Vangronsveld (2017) Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees. Microbiome 5:25
https://doi.org/10.1186/s40168-017-0241-2
|
8 |
D Bertrand, J Shaw, M Kalathiyappan, AHQ Ng, MS Kumar, C Li, M Dvornicic, JP Soldo, JY Koh, C Tonget al. (2019) Hybrid metagenomic assembly enables high-resolution analysis of resistance determinants and mobile elements in human microbiomes. Nat Biotechnol 37:937–944
https://doi.org/10.1038/s41587-019-0191-2
|
9 |
A Bishara, EL Moss, M Kolmogorov, AE Parada, Z Weng, A, Sidow AE Dekas, S Batzoglou, AS Bhatt (2018) High-quality genome sequences of uncultured microbes by assembly of read clouds. Nat Biotechnol 36:1067–1075
https://doi.org/10.1038/nbt.4266
|
10 |
K Blin, T Weber, SY Lee, MH Medema, V Pascal Andreu, ELC de los Santos, F Del Carratore (2018) The antiSMASH database version 2: a comprehensive resource on secondary metabolite biosynthetic gene clusters. Nucleic Acids Res 47:D625–D630
https://doi.org/10.1093/nar/gky1060
|
11 |
AM Bolger, M Lohse, B Usadel (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
https://doi.org/10.1093/bioinformatics/btu170
|
12 |
E Bolyen, JR Rideout, MR Dillon, NA Bokulich, CC Abnet, GA Al-Ghalith, H Alexander, EJ Alm, M Arumugam, F Asnicaret al. (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857
https://doi.org/10.1038/s41587-019-0209-9
|
13 |
RM Bowers, NC Kyrpides, R Stepanauskas, M Harmon-Smith, D Doud, TBK Reddy, F Schulz, J, Jarett AR Rivers, EA Eloe-Fadroshet al. (2017) Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol 35:725–731
https://doi.org/10.1038/nbt.3893
|
14 |
BJ Callahan, PJ McMurdie, MJ Rosen, AW Han, AJA Johnson, SP Holmes (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583
https://doi.org/10.1038/nmeth.3869
|
15 |
JG Caporaso, J Kuczynski, J, Stombaugh K Bittinger, FD Bushman, EK Costello, N Fierer, AG Peña, JK Goodrich, JI Gordonet al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
https://doi.org/10.1038/nmeth.f.303
|
16 |
P Carini, PJ Marsden, JW Leff, EE Morgan, MS Strickland, N Fierer (2016) Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat Microbiol 2:16242
https://doi.org/10.1038/nmicrobiol.2016.242
|
17 |
VJ Carrión, J Perez-Jaramillo, V Cordovez, V Tracanna, M de Hollander, D Ruiz-Buck, LW Mendes, WFJ van Ijcken, R Gomez- Exposito, SS Elsayedet al. (2019) Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366:606–612
https://doi.org/10.1126/science.aaw9285
|
18 |
T Charalampous, GL Kay, H Richardson, A Aydin, R Baldan, C Jeanes, D Rae, S Grundy, DJ Turner, J Wainet al. (2019) Nanopore metagenomics enables rapid clinical diagnosis of bacterial lower respiratory infection. Nat Biotechnol 37:783–792
https://doi.org/10.1038/s41587-019-0156-5
|
19 |
Q Chen, T Jiang, Y-X Liu, H Liu, T Zhao, Z Liu, X Gan, A Hallab, X Wang, J Heet al. (2019) Recently duplicated sesterterpene (C25) gene clusters in Arabidopsis thaliana modulate root microbiota. Sci China Life Sci 62:947–958
https://doi.org/10.1007/s11427-019-9521-2
|
20 |
PI Costea, G Zeller, S Sunagawa, E Pelletier, A Alberti, F, Levenez M Tramontano, M Driessen, R Hercog, F-E Junget al. (2017) Towards standards for human fecal sample processing in metagenomic studies. Nat Biotechnol 35:1069–1076
https://doi.org/10.1038/nbt.3960
|
21 |
G Csardi, T Nepusz (2006) The igraph software package for complex network research. InterJ Complex Syst 1695:1–9
|
22 |
MC de Goffau, S Lager, U Sovio, F Gaccioli, E Cook, SJ Peacock, J Parkhill, DS Charnock-Jones, GCS Smith (2019) Human placenta has no microbiome but can contain potential pathogens. Nature 572:329–334
https://doi.org/10.1038/s41586-019-1451-5
|
23 |
EJ de Muinck, P Trosvik, GD Gilfillan, JR Hov, AYM Sundaram (2017) A novel ultra high-throughput 16S rRNA gene amplicon sequencing library preparation method for the Illumina HiSeq platform. Microbiome 5:68
https://doi.org/10.1186/s40168-017-0279-1
|
24 |
RC Edgar (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
https://doi.org/10.1093/bioinformatics/btq461
|
25 |
RC Edgar (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998
https://doi.org/10.1038/nmeth.2604
|
26 |
RC Edgar, H Flyvbjerg (2015) Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31:3476–3482
https://doi.org/10.1093/bioinformatics/btv401
|
27 |
J, Edwards C Johnson, C Santos-Medellín , E Lurie, NK Podishetty, S Bhatnagar, JA Eisen, V Sundaresan (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112:E911–E920
https://doi.org/10.1073/pnas.1414592112
|
28 |
JA Edwards, CM Santos-Medellín, ZS Liechty, B Nguyen, E Lurie, S Eason, G Phillips, V Sundaresan (2018) Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice. PLoS Biol 16:e2003862
https://doi.org/10.1371/journal.pbio.2003862
|
29 |
K Fan, M Delgado-Baquerizo, X Guo, D Wang, Y Wu, M Zhu, W Yu, H Yao, Y-g Zhu, H Chu (2019) Suppressed N fixation and diazotrophs after four decades of fertilization. Microbiome 7:143
https://doi.org/10.1186/s40168-019-0757-8
|
30 |
D, Field G, Garrity T Gray, N Morrison, J Selengut, P Sterk, T, Tatusova N Thomson, MJ Allen, SV Angiuoliet al. (2008) The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol 26:541–547
https://doi.org/10.1038/nbt1360
|
31 |
EA Franzosa, LJ McIver, G Rahnavard, LR Thompson, M Schirmer, G, Weingart KS Lipson, R Knight, JG Caporaso, N Segataet al. (2018) Species-level functional profiling of metagenomes and metatranscriptomes. Nat Methods 15:962–968
https://doi.org/10.1038/s41592-018-0176-y
|
32 |
P Fresia, V Antelo, C Salazar, M, Giménez B, D’Alessandro E, Afshinnekoo C, Mason GH Gonnet, G Iraola (2019) Urban metagenomics uncover antibiotic resistance reservoirs in coastal beach and sewage waters. Microbiome 7:35
https://doi.org/10.1186/s40168-019-0648-z
|
33 |
L Fu, B Niu, Z Zhu, S Wu, W Li (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152
https://doi.org/10.1093/bioinformatics/bts565
|
34 |
F Galkin, A Aliper, E Putin, I, Kuznetsov VN Gladyshev, A Zhavoronkov (2018) Human microbiome aging clocks based on deep learning and tandem of permutation feature importance and accumulated local effects. bioRxiv 507780
https://doi.org/10.1101/507780
|
35 |
L Gao, T Xu, G Huang, S Jiang, Y Gu, F Chen (2018) Oral microbiomes: more and more importance in oral cavity and whole body. Protein Cell 9:488–500
https://doi.org/10.1007/s13238-018-0548-1
|
36 |
A Gonzalez, JA Navas-Molina , T Kosciolek, D McDonald, Y Vázquez-Baeza, G Ackermann, J DeReus, S Janssen, AD Swafford, SB Orchanianet al. (2018) Qiita: rapid, web-enabled microbiome meta-analysis. Nat Methods 15:796–798
https://doi.org/10.1038/s41592-018-0141-9
|
37 |
AL Goodman, G Kallstrom, JJ Faith, A Reyes, A Moore, G Dantas, JI Gordon (2011) Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc Natl Acad Sci USA 108:6252–6257
https://doi.org/10.1073/pnas.1102938108
|
38 |
B Grüning, R Dale, A Sjödin, BA Chapman, J Rowe, CH Tomkins-Tinch, R Valieris, J Köster, T The Bioconda (2018) Bioconda: sustainable and comprehensive software distribution for the life sciences. Nat Methods 15:475–476
https://doi.org/10.1038/s41592-018-0046-7
|
39 |
X Guo, X Zhang, Y Qin, Y-X Liu, J Zhang, N Zhang, K Wu, B Qu, Z He, X Wanget al. (2020) Host-associated quantitative abundance profiling reveals the microbial load variation of root microbiome. Plant Commun 1:100003
https://doi.org/10.1016/j.xplc.2019.100003
|
40 |
AC Huang, T Jiang, Y-X Liu, Y-C Bai, J Reed, B Qu, A Goossens, H-W Nützmann, Y, Bai A Osbourn (2019) A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science 364:eaau6389
https://doi.org/10.1126/science.aau6389
|
41 |
P, Huang Y, Zhang K Xiao, F Jiang, H Wang, D Tang, D Liu, B Liu, Y Liu, X Heet al. (2018) The chicken gut metagenome and the modulatory effects of plant-derived benzylisoquinoline alkaloids. Microbiome 6:211
https://doi.org/10.1186/s40168-018-0590-5
|
42 |
DH Huson, S Beier, I Flade, A Górska, M El-Hadidi, S Mitra, H-J Ruscheweyh, R Tappu (2016) MEGAN community edition—interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Comput Biol 12:e1004957
https://doi.org/10.1371/journal.pcbi.1004957
|
43 |
D Hyatt, PF LoCascio, LJ Hauser, EC Uberbacher (2012) Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics 28:2223–2230
https://doi.org/10.1093/bioinformatics/bts429
|
44 |
P Ji, Y Zhang, J, Wang F Zhao (2017) MetaSort untangles metagenome assembly by reducing microbial community complexity. Nat Commun 8:14306
https://doi.org/10.1038/ncomms14306
|
45 |
X, Jiang X Li, L Yang, C Liu, Q Wang, W Chi, H Zhu (2019) How microbes shape their communities? A microbial community model based on functional genes. Genom Proteom Bioinf 17:91–105
https://doi.org/10.1016/j.gpb.2018.09.003
|
46 |
S Jiao, Z Liu, Y Lin, J Yang, W Chen, G Wei (2016) Bacterial communities in oil contaminated soils: biogeography and cooccurrence patterns. Soil Biol Biochem 98:64–73
https://doi.org/10.1016/j.soilbio.2016.04.005
|
47 |
T Jin, Y Wang, Y Huang, J Xu, P Zhang, N Wang, X Liu, H Chu, G Liu, H Jianget al. (2017) Taxonomic structure and functional association of foxtail millet root microbiome. Giga Sci 6:1–12
https://doi.org/10.1093/gigascience/gix089
|
48 |
M Kanehisa, S Goto (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30
https://doi.org/10.1093/nar/28.1.27
|
49 |
M Kanehisa, Y Sato, K Morishima (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428:726–731
https://doi.org/10.1016/j.jmb.2015.11.006
|
50 |
DD Kang, J Froula, R, Egan Z Wang (2015) MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3:e1165
https://doi.org/10.7717/peerj.1165
|
51 |
A Klindworth, E, Pruesse T, Schweer J, Peplies C, Quast M Horn, FO Glöckner (2012) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencingbased diversity studies. Nucleic Acids Res 41:e1–e1
https://doi.org/10.1093/nar/gks808
|
52 |
R Knight, A Vrbanac, BC Taylor, A Aksenov, C, Callewaert J, Debelius A Gonzalez, T, Kosciolek L-I, McCall D McDonaldet al. (2018) Best practices for analysing microbiomes. Nat Rev Microbiol 16:410–422
https://doi.org/10.1038/s41579-018-0029-9
|
53 |
D Knights, J Kuczynski, ES Charlson, J Zaneveld, MC Mozer, RG Collman, FD Bushman, R Knight, ST Kelley (2011) Bayesian community-wide culture-independent microbial source tracking. Nat Methods 8:761
https://doi.org/10.1038/nmeth.1650
|
54 |
ZD Kurtz, CL Müller, ER Miraldi, DR Littman, MJ, Blaser RA Bonneau (2015) Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol 11:e1004226
https://doi.org/10.1371/journal.pcbi.1004226
|
55 |
J-C Lagier, G Dubourg, M Million, F Cadoret, M Bilen, F Fenollar, A Levasseur, J-M Rolain, P-E Fournier, D Raoult (2018) Culturing the human microbiota and culturomics. Nat Rev Microbiol 16:540–550
https://doi.org/10.1038/s41579-018-0041-0
|
56 |
MGI Langille, J Zaneveld, JG Caporaso, D McDonald, D Knights, JA Reyes, JC Clemente, DE Burkepile, RL Vega Thurber, R Knightet al. (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814
https://doi.org/10.1038/nbt.2676
|
57 |
B Langmead, SL Salzberg (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
https://doi.org/10.1038/nmeth.1923
|
58 |
I, Letunic P Bork (2019) Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47:W256–W259
https://doi.org/10.1093/nar/gkz239
|
59 |
A Levy, I, Salas Gonzalez M Mittelviefhaus, S, Clingenpeel S Herrera Paredes, J, Miao K Wang, G, Devescovi K Stillman, F Monteiroet al. (2018) Genomic features of bacterial adaptation to plants. Nat Genet 50:138–150
https://doi.org/10.1038/s41588-017-0012-9
|
60 |
D Li, C-M Liu, R Luo, K Sadakane, T-W Lam (2015) MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31:1674–1676
https://doi.org/10.1093/bioinformatics/btv033
|
61 |
J, Li H Jia, X Cai, H Zhong, Q Feng, S Sunagawa, M Arumugam, JR Kultima, E Prifti, T Nielsenet al. (2014) An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol 32:834–841
https://doi.org/10.1038/nbt.2942
|
62 |
C Liu, N Zhou, M-X, Du Y-T Sun, K Wang, Y-J Wang, D-H Li, H-Y, Yu Y Song, B-B Baiet al. (2020) The mouse gut microbial Biobank expands the coverage of cultured bacteria. Nat Commun 11:79
https://doi.org/10.1038/s41467-019-13836-5
|
63 |
Y-X Liu, Y, Qin Y Bai (2019) Reductionist synthetic community approaches in root microbiome research. Curr Opin Microbiol 49:97–102
https://doi.org/10.1016/j.mib.2019.10.010
|
64 |
Y-X Liu, Y, Qin X Guo, Y Bai(2019) Methods and applications for microbiome data analysis. Hereditas (Beijing) 41:1–18
|
65 |
S Louca, LW Parfrey, M Doebeli (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277
https://doi.org/10.1126/science.aaf4507
|
66 |
A Mahnert, C Moissl-Eichinger, M Zojer, D Bogumil, I Mizrahi, T Rattei, JL Martinez, G Berg (2019) Man-made microbial resistances in built environments. Nat Commun 10:968
https://doi.org/10.1038/s41467-019-08864-0
|
67 |
JR Marchesi, J Ravel (2015) The vocabulary of microbiome research: a proposal. Microbiome 3:31
https://doi.org/10.1186/s40168-015-0094-5
|
68 |
D McDonald, MN Price, J, Goodrich EP Nawrocki, TZ DeSantis, A Probst, GL Andersen, R Knight, P Hugenholtz (2011) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610
https://doi.org/10.1038/ismej.2011.139
|
69 |
BDC Members (2019) Database resources of the BIG data center in 2019. Nucleic Acids Res 47:D8–D14
|
70 |
JL Metcalf, ZZ Xu, S Weiss, S Lax, W Van Treuren, ER Hyde, SJ Song, A Amir, P Larsen, N Sangwanet al. (2016) Microbial community assembly and metabolic function during mammalian corpse decomposition. Science 351:158–162
https://doi.org/10.1126/science.aad2646
|
71 |
HC Metsky, KJ Siddle, A Gladden-Young, J Qu, DK Yang, P Brehio, A Goldfarb, A Piantadosi, S Wohl, A Carteret al. (2019) Capturing sequence diversity in metagenomes with comprehensive and scalable probe design. Nat Biotechnol 37:160–168
https://doi.org/10.1038/s41587-018-0006-x
|
72 |
A Mikheenko, V Saveliev, A Gurevich (2016) MetaQUAST: evaluation of metagenome assemblies. Bioinformatics 32:1088–1090
https://doi.org/10.1093/bioinformatics/btv697
|
73 |
AL Mitchell, A Almeida, M Beracochea, M Boland, J Burgin, G Cochrane, MR Crusoe, V Kale, SC Potter, LJ Richardsonet al. (2020) MGnify: the microbiome analysis resource in 2020. Nucleic Acids Res 48:D570–D578
https://doi.org/10.1093/nar/gkz1035
|
74 |
EL Moss, DG Maghini, and AS Bhatt (2020) Complete, closed bacterial genomes from microbiomes using nanopore sequencing. Nat Biotechnol
https://doi.org/10.1038/s41587-020-0422-6
|
75 |
D-S Mu, Q-Y Liang, X-M, Wang D-C Lu, M-J, Shi G-J Chen, Z-J Du (2018) Metatranscriptomic and comparative genomic insights into resuscitation mechanisms during enrichment culturing. Microbiome 6:230
https://doi.org/10.1186/s40168-018-0613-2
|
76 |
L-T Nguyen, HA Schmidt, A von Haeseler, BQ Minh (2014) IQTREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274
https://doi.org/10.1093/molbev/msu300
|
77 |
K Ning, Y Tong (2019) The fast track for microbiome research. Genom Proteom Bioinf 17:1–3
https://doi.org/10.1016/j.gpb.2019.04.001
|
78 |
S Nurk, D Meleshko, A Korobeynikov, PA Pevzner (2017) metaSPAdes: a new versatile metagenomic assembler. Genome Res 27:824–834
https://doi.org/10.1101/gr.213959.116
|
79 |
J Oksanen, R Kindt, P Legendre, B O’Hara, MHH Stevens, MJ Oksanen, M Suggests (2007) The vegan package. Commun Ecol Pack 10:631–637
|
80 |
DH Parks, GW Tyson, P Hugenholtz, RG Beiko (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124
https://doi.org/10.1093/bioinformatics/btu494
|
81 |
E Pasolli, F Asnicar, S Manara, M Zolfo, N Karcher, F Armanini, F Beghini, P Manghi, A Tett, P Ghensiet al. (2019) Extensive unexplored human microbiome diversity revealed by over 150,000 genomes from metagenomes spanning age, geography, and lifestyle. Cell 176:649–662.e620
https://doi.org/10.1016/j.cell.2019.01.001
|
82 |
R Patro, G Duggal, MI Love, RA Irizarry, C Kingsford (2017) Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods 14:417–149
https://doi.org/10.1038/nmeth.4197
|
83 |
HK Pedersen, SK Forslund, V Gudmundsdottir, AØ Petersen, F Hildebrand, T Hyötyläinen, T Nielsen, T Hansen, P, Bork SD Ehrlichet al. (2018) A computational framework to integrate highthroughput ‘-omics’ datasets for the identification of potential mechanistic links. Nat Protoc 13:2781–2800
https://doi.org/10.1038/s41596-018-0064-z
|
84 |
LM Proctor, HH Creasy, JM Fettweis, J, Lloyd-Price A Mahurkar, W Zhou, GA Buck, MP Snyder, JF Strauss, GM Weinstocket al. (2019) The integrative human microbiome project. Nature 569:641–648
https://doi.org/10.1038/s41586-019-1238-8
|
85 |
X Qian, Y-X Liu, X Ye, W Zheng, S Lv, M Mo, J Lin, W Wang, W Wang, X Zhanget al. (2020) Gut microbiota in children with juvenile idiopathic arthritis: characteristics, biomarker identification, and usefulness in clinical prediction. BMC Genom 21:286
https://doi.org/10.1186/s12864-020-6703-0
|
86 |
J Qin, R Li, J Raes, M Arumugam, KS Burgdorf, C Manichanh, T, Nielsen N Pons, F Levenez, T Yamadaet al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65
https://doi.org/10.1038/nature08821
|
87 |
C Quast, E Pruesse, P Yilmaz, J Gerken, T Schweer, P Yarza, J Peplies, FO Glockner (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–596
https://doi.org/10.1093/nar/gks1219
|
88 |
C Quince, AW Walker, JT Simpson, NJ Loman, N Segata (2017) Shotgun metagenomics, from sampling to analysis. Nat Biotechnol 35:833
https://doi.org/10.1038/nbt.3935
|
89 |
Z Ren, A Li, J Jiang, L Zhou, Z Yu, H Lu, H Xie, X Chen, L Shao, R Zhanget al. (2019) Gut microbiome analysis as a tool towards targeted non-invasive biomarkers for early hepatocellular carcinoma. Gut 68:1014–1023
https://doi.org/10.1136/gutjnl-2017-315084
|
90 |
MD Robinson, DJ McCarthy, GK Smyth (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140
https://doi.org/10.1093/bioinformatics/btp616
|
91 |
T, Rognes T Flouri, B Nichols, C Quince, F Mahé (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584
https://doi.org/10.7717/peerj.2584
|
92 |
AA Ross, KM Müller, JS Weese, JD Neufeld (2018) Comprehensive skin microbiome analysis reveals the uniqueness of human skin and evidence for phylosymbiosis within the class mammalia. Proc Natl Acad Sci USA 115:E5786–E5795
https://doi.org/10.1073/pnas.1801302115
|
93 |
D Rothschild, O Weissbrod, E Barkan, A Kurilshikov, T, Korem D Zeevi, PI Costea, A Godneva, IN Kalka, N Baret al. (2018) Environment dominates over host genetics in shaping human gut microbiota. Nature 555:210
https://doi.org/10.1038/nature25973
|
94 |
S Roux, EM Adriaenssens, BE Dutilh, EV Koonin, AM Kropinski, M Krupovic, JH Kuhn, R Lavigne, JR Brister, A Varsaniet al. (2019) Minimum information about an uncultivated virus genome (MIUViG). Nat Biotechnol 37:29–37
https://doi.org/10.1038/nbt.4306
|
95 |
R Saito, ME Smoot, K Ono, J, Ruscheinski P-L Wang, S Lotia, AR Pico, GD Bader, T Ideker (2012) A travel guide to cytoscape plugins. Nat Methods 9:1069–1076
https://doi.org/10.1038/nmeth.2212
|
96 |
G Salazar, L Paoli, A Alberti, J Huerta-Cepas, H-J Ruscheweyh, M Cuenca, CM Field, LP Coelho, C Cruaud, S Engelenet al. (2019) Gene expression changes and community turnover differentially shape the global ocean metatranscriptome. Cell 179:1068–1083.e1021
https://doi.org/10.1016/j.cell.2019.10.014
|
97 |
T Seemann (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069
https://doi.org/10.1093/bioinformatics/btu153
|
98 |
N Segata, J Izard, L Waldron, D Gevers, L Miropolsky, WS Garrett, C Huttenhower (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60
https://doi.org/10.1186/gb-2011-12-6-r60
|
99 |
L Shenhav, M Thompson, TA Joseph, L Briscoe, O Furman, D Bogumil, I, Mizrahi I, Pe’er and E Halperin (2019) FEAST: fast expectation-maximization for microbial source tracking. Nat Methods
https://doi.org/10.1038/s41592-019-0431-x
|
100 |
W Shi, M Li, G Wei, R Tian, C Li, B Wang, R Lin, C Shi, X Chi, B Zhouet al. (2019) The occurrence of potato common scab correlates with the community composition and function of the geocaulosphere soil microbiome. Microbiome 7:14
https://doi.org/10.1186/s40168-019-0629-2
|
101 |
W Shi, H Qi, Q Sun, G, Fan S Liu, J Wang, B Zhu, H Liu, F, Zhao X Wanget al. (2019) gcMeta: a global catalogue of metagenomics platform to support the archiving, standardization and analysis of microbiome data. Nucleic Acids Res 47:D637–D648
https://doi.org/10.1093/nar/gky1008
|
102 |
CMK Sieber, AJ Probst, A Sharrar, BC Thomas, M Hess, SG Tringe, JF Banfield (2018) Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat Microbiol 3:836–843
https://doi.org/10.1038/s41564-018-0171-1
|
103 |
R, Sinha G Abu-Ali, E, Vogtmann AA Fodor, B Ren, A Amir, E Schwager, J, Crabtree S Ma, CC Abnetet al. (2017) Assessment of variation in microbial community amplicon sequencing by the microbiome quality control (MBQC) project consortium. Nat Biotechnol 35:1077–1086
https://doi.org/10.1038/nbt.3981
|
104 |
SA Smits, J Leach, ED Sonnenburg, CG Gonzalez, JS Lichtman, G Reid, R Knight, A Manjurano, J Changalucha, JE Eliaset al. (2017) Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. Science 357:802–806
https://doi.org/10.1126/science.aan4834
|
105 |
RD Stewart, MD Auffret, A Warr, AW Walker, R Roehe, M Watson (2019) Compendium of 4,941 rumen metagenome-assembled genomes for rumen microbiome biology and enzyme discovery. Nat Biotechnol 37:953–961
https://doi.org/10.1038/s41587-019-0202-3
|
106 |
RD Stewart, MD Auffret, A Warr, AH Wiser, MO Press, KW Langford, I Liachko, TJ Snelling, RJ Dewhurst, AW Walkeret al. (2018) Assembly of 913 microbial genomes from metagenomic sequencing of the cow rumen. Nat Commun 9:870
https://doi.org/10.1038/s41467-018-03317-6
|
107 |
S Subramanian, S Huq, T, Yatsunenko R Haque, M Mahfuz, MA Alam, A Benezra, J DeStefano, MF Meier, BD Mueggeet al. (2014) Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510:417
https://doi.org/10.1038/nature13421
|
108 |
O Tange(2018). Gnu parallel 2018 (Lulu. com).
|
109 |
BT Tierney, Z Yang, JM Luber, M Beaudin, MC Wibowo , C, Baek E Mehlenbacher , CJ Patel, AD Kostic (2019) The landscape of genetic content in the gut and oral human microbiome. Cell Host Microbe 26:283–295.e288
https://doi.org/10.1016/j.chom.2019.07.008
|
110 |
A Tkacz, M, Hortala PS Poole (2018) Absolute quantitation of microbiota abundance in environmental samples. Microbiome 6:110
https://doi.org/10.1186/s40168-018-0491-7
|
111 |
DT Truong, EA Franzosa, TL Tickle, M Scholz, G Weingart, E Pasolli, A Tett, C Huttenhower, N Segata (2015) MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods 12:902–903
https://doi.org/10.1038/nmeth.3589
|
112 |
PJ Turnbaugh, RE Ley, M Hamady, CM Fraser-Liggett, R Knight, JI Gordon (2007) The human microbiome project. Nature 449:804–810
https://doi.org/10.1038/nature06244
|
113 |
TR Turner, K Ramakrishnan, J Walshaw, D Heavens, M Alston, D Swarbreck, A Osbourn, A Grant, PS Poole (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7:2248–2258
https://doi.org/10.1038/ismej.2013.119
|
114 |
GV Uritskiy, J DiRuggiero, J Taylor (2018) MetaWRAP—a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome 6:158
https://doi.org/10.1186/s40168-018-0541-1
|
115 |
D Vandeputte, G Kathagen, K D’hoe, S Vieira-Silva, M Valles-Colomer, J Sabino, J Wang, RY Tito, L De Commer, Y Darzi, et al. (2017) Quantitative microbiome profiling links gut community variation to microbial load. Nature 551:507–511
https://doi.org/10.1038/nature24460
|
116 |
P, Vangay BM Hillmann, D Knights (2019) Microbiome Learning Repo (ML Repo): A public repository of microbiome regression and classification tasks. GigaScience 8:giz042
https://doi.org/10.1093/gigascience/giz042
|
117 |
J Wang, L Chen, N Zhao, X Xu, Y Xu, B Zhu (2018) Of genes and microbes: solving the intricacies in host genomes. Protein Cell 9:446–461
https://doi.org/10.1007/s13238-018-0532-9
|
118 |
J Wang, Z Jia, B Zhang, L Peng, and F Zhao (2019) Tracing the accumulation of in vivo human oral microbiota elucidates microbial community dynamics at the gateway to the GI tract. Gut, gutjnl-2019–318977
https://doi.org/10.1136/gutjnl-2019-318977
|
119 |
J Wang, LB Thingholm, J Skiecevičienė, P, Rausch M Kummen, JR Hov, F Degenhardt, F-A Heinsen, MC Rühlemann, S Szymczaket al. (2016) Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nat Genet 48:1396–1406
https://doi.org/10.1038/ng.3695
|
120 |
J Wang, J Zheng, W Shi, N Du, X Xu, Y Zhang, P, Ji F Zhang, Z Jia, Y Wanget al. (2018) Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus. Gut 67:1614–1625
https://doi.org/10.1136/gutjnl-2018-315988
|
121 |
W Wang, J Yang, J Zhang, Y-X Liu, C Tian, B Qu, C Gao, P Xin, S Cheng, W Zhanget al. (2020) An Arabidopsis secondary metabolite directly targets expression of the bacterial type III secretion system to inhibit bacterial virulence. Cell Host Microbe 27:601–613.e607
https://doi.org/10.1016/j.chom.2020.03.004
|
122 |
X, Wang M, Wang X Xie, S Guo, Y Zhou, X Zhang, N Yu, and E Wang (2020b) An amplification-selection model for quantified rhizosphere microbiota assembly. Sci Bull
https://doi.org/10.1016/j.scib.2020.03.005
|
123 |
Y Wang, F Song, J Zhu, S Zhang, Y Yang, T Chen, B Tang, L Dong, N Ding, Q Zhanget al.(2017) GSA: genome sequence archive*. Genom Proteom Bioinf 15:14–18
https://doi.org/10.1016/j.gpb.2017.01.001
|
124 |
T Ward, J, Larson J Meulemans, B Hillmann, J Lynch, D Sidiropoulos, JR Spear, G Caporaso, R Blekhman, R Knightet al. (2017) BugBase predicts organism-level microbiome phenotypes. bioRxiv 133462
https://doi.org/10.1101/133462
|
125 |
N Wilck, MG Matus, SM Kearney, SW Olesen, K Forslund, H Bartolomaeus, S Haase, A Mähler, A Balogh, L Markóet al. (2017) Salt-responsive gut commensal modulates TH17 axis and disease. Nature 551:585–589
https://doi.org/10.1038/nature24628
|
126 |
DE Wood, J Lu, and B Langmead (2019) Improved metagenomic analysis with Kraken 2. bioRxiv 762302
https://doi.org/10.1186/s13059-019-1891-0
|
127 |
Y-W Wu, BA Simmons, SW Singer (2015) MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32:605–607
https://doi.org/10.1093/bioinformatics/btv638
|
128 |
L Xiao, Q Feng, S Liang, SB Sonne, Z Xia, X Qiu, X Li, H Long, J, Zhang D Zhanget al. (2015) A catalog of the mouse gut metagenome. Nat Biotechnol 33:1103
https://doi.org/10.1038/nbt.3353
|
129 |
J Xu, Y Zhang, P Zhang, P Trivedi, N Riera, Y Wang, X Liu, G Fan, J Tang, HD Coletta-Filhoet al. (2018) The structure and function of the global citrus rhizosphere microbiome. Nat Commun 9:4894
https://doi.org/10.1038/s41467-018-07343-2
|
130 |
Y Xu, F Zhao (2018) Single-cell metagenomics: challenges and applications. Protein Cell 9:501–510
https://doi.org/10.1007/s13238-018-0544-5
|
131 |
J Yang, J Yu (2018) The association of diet, gut microbiota and colorectal cancer: what we eat may imply what we get. Protein Cell 9:474–487
https://doi.org/10.1007/s13238-018-0543-6
|
132 |
SH Ye, KJ Siddle, DJ Park, PC Sabeti (2019) Benchmarking metagenomics tools for taxonomic classification. Cell 178:779–794
https://doi.org/10.1016/j.cell.2019.07.010
|
133 |
P Yilmaz, R Kottmann, D Field, R Knight, JR Cole, L Amaral-Zettler, JA Gilbert, I Karsch-Mizrachi, A Johnston, G Cochraneet al. (2011) Minimum information about a marker gene sequence (MIMARKS) and minimum information about any (x) sequence (MIxS) specifications. Nat Biotechnol 29:415–420
https://doi.org/10.1038/nbt.1823
|
134 |
R Zgadzaj, R Garrido-Oter , DB Jensen, A Koprivova, P Schulze-Lefert, S Radutoiu (2016) Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities. Proc Natl Acad Sci USA 113: E7996–E8005
https://doi.org/10.1073/pnas.1616564113
|
135 |
F Zhang, B Cui, X He, Y, Nie K Wu, D Fan, B Feng, D Chen, J Ren, M Denget al. (2018) Microbiota transplantation: concept, methodology and strategy for its modernization. Protein Cell 9:462–473
https://doi.org/10.1007/s13238-018-0541-8
|
136 |
J Zhang, Y-X Liu, N Zhang, B Hu, T Jin, H Xu, Y Qin, P Yan, X Zhang, X Guoet al. (2019) NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol 37:676–684
https://doi.org/10.1038/s41587-019-0104-4
|
137 |
J Zhang, N Zhang, Y-X Liu, X Zhang, B Hu, Y Qin, H Xu, H Wang, X Guo, J Qianet al. (2018) Root microbiota shift in rice correlates with resident time in the field and developmental stage. Sci China Life Sci 61:613–621
https://doi.org/10.1007/s11427-018-9284-4
|
138 |
M Zheng, N Zhou, S Liu, C Dang, Y-X, Liu S He, Y Zhao, W Liu, X Wang (2019) N2O and NO emission from a biological aerated filter treating coking wastewater: main source and microbial community. J Clean Prod 213:365–374
https://doi.org/10.1016/j.jclepro.2018.12.182
|
139 |
W Zhu, A Lomsadze, M Borodovsky (2010) Ab initio gene identification in metagenomic sequences. Nucleic Acids Res 38:e132–e132
https://doi.org/10.1093/nar/gkq275
|
140 |
Y Zou, W Xue, G, Luo Z, Deng P Qin, R Guo, H Sun, Y Xia, S Liang, Y Daiet al. (2019) 1,520 reference genomes from cultivated human gut bacteria enable functional microbiome analyses. Nat Biotechnol 37:179–185
https://doi.org/10.1038/s41587-018-0008-8
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