Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides

Science

Volumn 350, Issue 6256, 2015, Pages

  Wu, Meng ^a   McNulty, Nathan P ^a   Rodionov, Dmitry A ^b,c   Khoroshkin, Matvei S ^c   Griffin, Nicholas W ^a   Cheng, Jiye ^a   Latreille, Phil ^d   Kerstetter, Randall A ^d   Terrapon, Nicolas ^e   Henrissat, Bernard ^e,f   Osterman, Andrei L ^b   Gordon, Jeffrey I ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BURNHAM INSTITUTE   (United States)

^c INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

^d MONSANTO COMPANY   (United States)

^e AIX MARSEILLE UNIVERSITY   (France)

^f KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; BACTERIUM; DIET; DIGESTIVE SYSTEM; FITNESS; GENETIC ANALYSIS; HOMINID; NICHE; QUANTITATIVE ANALYSIS; RODENT;

ARTICLE; BACTEROIDES; BACTEROIDES CELLULOSILYTICUS; DIET; DIET SUPPLEMENTATION; FITNESS; GENE LIBRARY; HUMAN; IN VIVO STUDY; INTESTINE FLORA; MICROBIAL COMMUNITY; NONHUMAN; PRIORITY JOURNAL; TRANSPOSON; ANIMAL; DNA SEQUENCE; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC MARKER; GENETICS; GERMFREE ANIMAL; METABOLISM; MICROBIOLOGY; MOUSE; PROCEDURES; REPRODUCTIVE FITNESS;

BACTEROIDES; MUS;

ARABINOXYLAN; GENETIC MARKER; PREBIOTIC AGENT; TRANSPOSON; XYLAN;

ANIMALS; BACTEROIDES; DIET; DNA TRANSPOSABLE ELEMENTS; GASTROINTESTINAL TRACT; GENE LIBRARY; GENETIC FITNESS; GENETIC LOCI; GENETIC MARKERS; GERM-FREE LIFE; HUMANS; MICE; MUTAGENESIS, INSERTIONAL; PREBIOTICS; SEQUENCE ANALYSIS, DNA; XYLANS;

EID: 84947983159     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aac5992     Document Type: Article

References (27)

1. K. E. Nelson et al., A catalog of reference genomes from the human microbiome. Science 328, 994-999 (2010). doi: 10.1126/science.1183605; pmid: 20489017
2. J. Qin et al., MetaHIT Consortium, A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65 (2010). doi: 10.1038/nature08821; pmid: 20203603
3. J. J. Faith et al., The long-term stability of the human gut microbiota. Science 341, 1237439 (2013). doi: 10.1126/science.1237439; pmid: 23828941
4. J. Xu et al., A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299, 2074-2076 (2003). doi: 10.1126/science.1080029; pmid: 12663928
5. J. L. Sonnenburg et al., Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307, 1955-1959 (2005). doi: 10.1126/science.1109051; pmid: 15790854
6. E. C. Martens et al., Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLOS Biol. 9, e1001221 (2011). doi: 10.1371/journal.pbio.1001221; pmid: 22205877
7. N. P. McNulty et al., Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome. PLOS Biol. 11, e1001637 (2013). doi: 10.1371/journal.pbio.1001637; pmid: 23976882
8. J. J. Faith, N. P. McNulty, F. E. Rey, J. I. Gordon, Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science 333, 101-104 (2011). pmid: 21596954
9. A. L. Goodman et al., Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6, 279-289 (2009). doi: 10.1016/j.chom.2009.08.003; pmid: 19748469
10. A. L. Goodman, M. Wu, J. I. Gordon, Identifying microbial fitness determinants by insertion sequencing using genomewide transposon mutant libraries. Nat. Protoc. 6, 1969-1980 (2011). doi: 10.1038/nprot.2011.417; pmid: 22094732
11. C. R. Rao, in Multivariate Statistics and Matrices in Statistics, E.-M. Tiit, T. Kollo, H. Niemi, Eds. (VSP, Utrecht, Netherlands, 1995), pp. 143-161.
12. P. H. Degnan, N. A. Barry, K. C. Mok, M. E. Taga, A. L. Goodman, Human gut microbes use multiple transporters to distinguish vitamin B12 analogs and compete in the gut. Cell Host Microbe 15, 47-57 (2014). doi: 10.1016/j.chom.2013.12.007; pmid: 24439897
13. C. S. Holling, Resilience and stability of ecological systems. Annu. Rev. Ecol. Syst. 4, 1-23 (1973). doi: 10.1146/annurev.es.04.110173.000245
14. D. A. Ravcheev, A. Godzik, A. L. Osterman, D. A. Rodionov, Polysaccharides utilization in human gut bacterium Bacteroides thetaiotaomicron: Comparative genomics reconstruction of metabolic and regulatory networks. BMC Genomics 14, 873 (2013). doi: 10.1186/1471-2164-14-873; pmid: 24330590
15. R. Overbeek et al., The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33, 5691-5702 (2005). doi: 10.1093/nar/gki866; pmid: 16214803
16. A. G. Lindenstrauß et al., Transcriptome analysis of Enterococcus faecalis toward its adaption to surviving in the mouse intestinal tract. Arch. Microbiol. 196, 423-433 (2014). doi: 10.1007/s00203-014-0982-2; pmid: 24700373
17. A. R. Reeves, J. N. D'Elia, J. Frias, A. A. Salyers, A Bacteroides thetaiotaomicron outer membrane protein that is essential for utilization of maltooligosaccharides and starch. J. Bacteriol. 178, 823-830 (1996). pmid: 8550519
18. A. R. Reeves, G. R. Wang, A. A. Salyers, Characterization of four outer membrane proteins that play a role in utilization of starch by Bacteroides thetaiotaomicron. J. Bacteriol. 179, 643-649 (1997).pmid: 9006015
19. J. A. Shipman, J. E. Berleman, A. A. Salyers, Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J. Bacteriol. 182, 5365-5372 (2000). doi: 10.1128/JB.182.19.5365-5372.2000; pmid: 10986238
20. E. C. Martens, H. C. Chiang, J. I. Gordon, Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4, 447-457 (2008). doi: 10.1016/j.chom.2008.09.007; pmid: 18996345
21. P. C. Kashyap et al., Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota. Proc. Natl. Acad. Sci. U.S.A. 110, 17059-17064 (2013). doi: 10.1073/pnas.1306070110; pmid: 24062455
22. D. Dodd, R. I. Mackie, I. K. Cann, Xylan degradation, a metabolic property shared by rumen and human colonic Bacteroidetes. Mol. Microbiol. 79, 292-304 (2011). doi: 10.1111/j.1365-2958.2010.07473.x; pmid: 21219452
23. A. Rogowski et al., Glycan complexity dictates microbial resource allocation in the large intestine. Nat. Commun. 6, 7481 (2015).pmid: 26112186
24. T. W. Cullen et al., Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 347, 170-175 (2015). doi: 10.1126/science.1260580; pmid: 25574022
25. C. L. Shelton, F. K. Raffel, W. L. Beatty, S. M. Johnson, K. M. Mason, Sap transporter mediated import and subsequent degradation of antimicrobial peptides in Haemophilus. PLOS Pathog. 7, e1002360 (2011). doi: 10.1371/journal.ppat.1002360; pmid: 22072973
26. M. Krzywinski et al., Circos: An information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009). doi: 10.1101/gr.092759.109; pmid: 19541911
27. A. E. Darling, B. Mau, N. T. Perna, progressiveMauve: Multiple genome alignment with gene gain, loss and rearrangement. PLOS ONE 5, e11147 (2010). doi: 10.1371/journal.pone.0011147; pmid: 20593022