Metagenomic reconstructions of gut microbial metabolism in weanling pigs

Microbiome

Volumn 7, Issue 1, 2019, Pages

  Wang, Weilan ^a,b   Hu, Huifeng ^b   Zijlstra, Ruurd T ^a   Zheng, Jinshui ^b   Gänzle, Michael G ^a,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^c HUBEI UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Fructan; Lactose; Metagenomic; Microbial degradation; Reconstructions; Starch; Weanling pigs

Indexed keywords

ALPHA GLUCOSIDASE; BETA GALACTOSIDASE; CARBOHYDRATE; DEXTRAN; RNA 16S; STARCH; BACTERIAL DNA; RIBOSOME DNA;

ANIMAL EXPERIMENT; ARTICLE; BACTEROIDETES; CFU COUNTING; FERMENTATION; FIRMICUTES; GENE SEQUENCE; GENETIC VARIATION; INTESTINE FLORA; LACTOBACILLUS FERMENTUM; MALE; METABOLISM; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL CONSORTIUM; MICROBIAL METABOLISM; NONHUMAN; PRIORITY JOURNAL; WEANING; ANIMAL; BACTERIUM; CARBOHYDRATE DIET; CLASSIFICATION; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; LACTOBACILLUS; PHYLOGENY; PIG; PROCEDURES;

ANIMALS; BACTERIA; BACTEROIDETES; DIETARY CARBOHYDRATES; DNA, BACTERIAL; DNA, RIBOSOMAL; FIRMICUTES; GASTROINTESTINAL MICROBIOME; LACTOBACILLUS; MALE; METAGENOMICS; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SWINE;

EID: 85063516385     PISSN: None     EISSN: 20492618     Source Type: Journal    
DOI: 10.1186/s40168-019-0662-1     Document Type: Article

References (81)

1. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690-703.
2. Blekhman R, Goodrich JK, Huang K, Sun Q, Bukowski R, Bell JT, et al. Host genetic variation impacts microbiome composition across human body sites. Genome Biol. 2015;16:191.
3. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA, Stares MD, et al. Culturing of 'unculturable' human microbiota reveals novel taxa and extensive sporulation. Nature. 2016;533:543-6.
4. Dethlefsen L, Eckburg PB, Bik EM, Relman DA. Assembly of the human intestinal microbiota. Trends Ecol Evol. 2006;21:517-23.
5. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. PNAS. 2010;107:18933-8.
6. Camarinha-Silva A, Maushammer M, Wellmann R, Vital M, Preuss S, Bennewitz J. Host genome influence on gut microbial composition and microbial prediction of complex traits in pigs. Genetics. 2017;206:1637-44.
7. Frese SA, Parker K, Calvert CC, Mills DA. Diet shapes the gut microbiome of pigs during nursing and weaning. Microbiome. 2015;3:28.
8. Koropatkin NM, Cameron EA, Martens EC. How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol. 2012;10:323-35.
9. Chung WSF, Walker AW, Louis P, Parkhill J, Vermeiren J, Bosscher D, et al. Modulation of the human gut microbiota by dietary fibres occurs at the species level. BMC Biol. 2016;14:1-14.
10. Sharon I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF. Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res. 2013;23:111-20.
11. Sullam KE, Rubin BER, Dalton CM, Kilham SS, Flecker AS, Russell JA. Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies. ISME J. 2015;9:1508-22.
12. Yang Y, Galle S, Le MHA, Zijlstra RT, Gänzle MG. Feed fermentation with reuteran- and levan-producing Lactobacillus reuteri reduces colonization of weanling pigs by enterotoxigenic Escherichia coli. Appl Env Microbiol. 2015;81:5743-52.
13. Molist F, van Oostrum M, Pérez JF, Mateos GG, Nyachoti CM, van der Aar PJ. Relevance of functional properties of dietary fibre in diets for weanling pigs. Anim Feed Sci Technol. 2014;189:1-10.
14. Bach Knudsen KE, Hedemann MS, Lærke HN. The role of carbohydrates in intestinal health of pigs. Anim Feed Sci Technol. 2012;173:41-53.
15. Jha R, Berrocoso JD. Review: dietary fiber utilization and its effects on physiological functions and gut health of swine. Animal. 2015;9:1441-52.
16. Magnúsdóttir S, Heinken A, Kutt L, Ravcheev DA, Bauer E, Noronha A, et al. Generation of genome-scale metabolic reconstructions for 773 members of the human gut microbiota. Nat Biotechnol. 2017;35:81-9.
17. Schmidt TSB, Raes J, Bork P. The human gut microbiome: from association to modulation. Cell. 2018;172:1198-215.
18. Slifierz MJ, Friendship RM, Weese JS. Longitudinal study of the early-life fecal and nasal microbiotas of the domestic pig. BMC Microbiol. 2015;15:1-12.
19. Yang Y, Zhao X, Le MHA, Zijlstra RT, Gänzle MG. Reutericyclin producing Lactobacillus reuteri modulates development of fecal microbiota in weanling pigs. Front Microbiol. 2015;6:762.
20. Xiao L, Estellé J, Kiilerich P, Ramayo-Caldas Y, Xia Z, Feng Q, et al. A reference gene catalogue of the pig gut microbiome. Nat Microbiol. 2016;1:1-6.
21. Zhao X, Wang W, Blaine A, Kane ST, Zijlstra RT, Gänzle MG. Impact of probiotic Lactobacillus sp.on autochthonous lactobacilli in weaned piglets. J Appl Microbiol. 2018; in press
22. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335-6.
23. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460-1.
24. Edgar RC. Accuracy of taxonomy prediction for 16S rRNA and fungal ITS sequences. PeerJ. 2018;6:e4652.
25. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114-20.
26. Wu Y, Tang Y, Tringe SG, Simmons BA, Singer SW. MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm. Microbiome. 2014;2:1-18.
27. Olm MR, Brown CT, Brooks B, Banfield JF. DRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 2017;11:2864-8.
28. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043-55.
29. Svartström O, Alneberg J, Terrapon N, Lombard V, de Bruijn I, Malmsten J, et al. Ninety-nine de novo assembled genomes from the moose (Alces alces) rumen microbiome provide new insights into microbial plant biomass degradation. ISME J. 2017;11:2538-51.
30. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11:119.
31. Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Bateman A, Eddy SR. HMMER web server: 2015 update. Nucleic Acids Res. 2015;43:W30-8.
32. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun. 2013;4:2304
33. Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J. 2017;11:2399-406.
34. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species culture-independent genomic approaches identify credibly distinct clusters, avoid cultivation bias, and provide true insights into microbial species. Microbe. 2014;9:111-7.
35. Gupta RS, Lo B, Son J. Phylogenomics and comparative genomic studies robustly support division of the genus Mycobacterium into an emended genus Mycobacterium and four novel genera. Front Microbiol. 2018;9:1-41.
36. Chen C, Zhou F, Ren J, Ai L, Dong Y, Wu Z, et al. Cloning, expression and functional validation of a β-fructofuranosidase from Lactobacillus plantarum. Process Biochem. 2014;49:758-67.
37. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3:289-306.
38. Martens EC, Koropatkin NM, Smith TJ, Gordon JI. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J Biol Chem. 2009;284:24673-7.
39. Ryan SM, Fitzgerald GF, Van Sinderen D. Screening for and identification of starch-, amylopectin-, and pullulan-degrading activities in bifidobacterial strains. Appl Env Microbiol. 2006;72:5289-96.
40. Scott KP, Martin JC, Chassard C, Clerget M, Potrykus J, Campbell G, et al. Substrate-driven gene expression in Roseburia inulinivorans: importance of inducible enzymes in the utilization of inulin and starch. PNAS. 2011;108:4672-9.
41. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, et al. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell. 2010;141:1241-52.
42. Ze X, Ben DY, Laverde-Gomez JA, Dassa B, Sheridan PO, Duncan SH, et al. Unique organization of extracellular amylases into amylosomes in the resistant starch-utilizing human colonic firmicutes bacterium Ruminococcus bromii. MBio. 2015;6:1-11.
43. Loponen J, Gänzle M, Loponen J, Gänzle MG. Use of sourdough in low FODMAP baking. Foods. 2018;7:96.
44. Looft T, Allen HK, Cantarel BL, Levine UY, Bayles DO, Alt DP, et al. Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations. ISME J. 2014;8:1566-76.
45. Metzler-Zebeli BU, Hooda S, Pieper R, Zijlstra RT, Van Kessel AG, Mosenthin R, et al. Nonstarch polysaccharides modulate bacterial microbiota, pathways for butyrate production, and abundance of pathogenic escherichia coli in the pig gastrointestinal tract. Appl Environ Microbiol. 2010;76:3692-701.
46. Zhang Q, Widmer G, Tzipori S. A pig model of the human gastrointestinal tract. Gut Microbes. 2013;4:193-200.
47. Pluske JR. Feed- and feed additives-related aspects of gut health and development in weanling pigs. J Anim Sci Biotechnol. 2013;4:1.
48. Walter J, Maldonado-Gomez MX, Martinez I. To engraft or not to engraft: an ecological framework for gut microbiome modulation with live microbes. Curr Opin Biotechnol. 2018;49:129-39.
49. Kristensen NB, Bryrup T, Allin KH, Nielsen T, Hansen TH, Pedersen O. Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials. Genome Med. 2016;8:52.
50. Hugerth LW, Larsson J, Alneberg J, Lindh MV, Legrand C, Pinhassi J, et al. Metagenome-assembled genomes uncover a global brackish microbiome. Genome Biol. 2015;16:1-18.
51. Peng Y, Leung HCM, Yiu SM, Chin FYL. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics. 2012;28:1420-8.
52. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, et al. A new view of the tree of life. Nat Microbiol. 2016;1:1-6.
53. Mukherjee S, Seshadri R, Varghese NJ, Eloe-Fadrosh EA, Meier-Kolthoff JP, Göker M, et al. 1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life. Nat Biotechnol. 2017;35:676-83.
54. Di Cesare A, Fontaneto D, Doppelbauer J, Corno G. Fitness and recovery of bacterial communities and antibiotic resistance genes in urban wastewaters exposed to classical disinfection treatments. Env Sci Technol. 2016;50:10153-61.
55. Hamaker BR, Tuncil YE. A perspective on the complexity of dietary fiber structures and their potential effect on the gut microbiota. J Mol Biol. 2014;426:3838-50.
56. Metzler-Zebeli BU, Schmitz-Esser S, Mann E, Grüll D, Molnar T, Zebeli Q. Adaptation of the cecal bacterial microbiome of growing pigs in response to resistant starch type 4. Appl Environ Microbiol. 2015;81:8489-99.
57. Robert C, Bernalier-Donadille A. The cellulolytic microflora of the human colon: evidence of microcrystalline cellulose-degrading bacteria in methane-excreting subjects. FEMS Microbiol Ecol. 2003;46:81-9.
58. Ze X, Duncan SH, Louis P, Flint HJ. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J. 2012;6:1535-43.
59. Haenen D, Zhang J, Souza da Silva C, Bosch G, van der Meer IM, van Arkel J, et al. A diet high in resistant starch modulates microbiota composition, SCFA concentrations, and gene expression in pig intestine. J Nutr. 2013;143:274-83.
60. Duar RM, Lin XB, Zheng J, Martino ME, Grenier T, Perez-Munoz ME, et al. Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS Microbiol Rev. 2017;41:S27-48.
61. van de Guchte M, Penaud S, Grimaldi C, Barbe V, Bryson K, Nicolas P, et al. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. PNAS. 2006;103:9274-9.
62. Sørensen HR, Pedersen S, Jørgensen CT, Meyer AS. Enzymatic hydrolysis of wheat arabinoxylan by a recombinant "minimal" enzyme cocktail containing β-xylosidase and novel endo-1,4-β-xylanase and α-L-arabinofuranosidase activities. Biotechnol Prog. 2007;23:100-7.
63. Cockburn DW, Orlovsky NI, Foley MH, Kwiatkowski KJ, Bahr CM, Maynard M, et al. Molecular details of a starch utilization pathway in the human gut symbiont Eubacterium rectale. Mol Microbiol. 2015;95:209-30.
64. Reichardt N, Vollmer M, Holtrop G, Farquharson FM, Wefers D, Bunzel M, et al. Specific substrate-driven changes in human faecal microbiota composition contrast with functional redundancy in short-chain fatty acid production. ISME J. 2018;12:610-22.
65. Krumbeck JA, Rasmussen HE, Hutkins RW, Clarke J, Shawron K, Keshavarzian A, et al. Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics. Microbiome. 2018;6:121.
66. Rumbak E, Rawlings DE, Lindsey GG, Woods DR. Characterization of the Butyrivibrio fibrisolvens glgB gene, which encodes a glycogen-branching enzyme with starch-clearing activity. J Bacteriol. 1991;173:6732-41.
67. Lee S, Cantarel B, Henrissat B, Gevers D, Birren BW, Huttenhower C, et al. Gene-targeted metagenomic analysis of glucan-branching enzyme gene profiles among human and animal fecal microbiota. ISME J. 2014;8:493-503.
68. D'Elia JN, Salyers AA. Contribution of a neopullulanase, a pullulanase, and an alpha-glucosidase to growth of Bacteroides thetaiotaomicron on starch. J Bacteriol. 1996;178:7173-9.
69. Wilson B, Whelan K. Prebiotic inulin-type fructans and galacto-oligosaccharides: definition, specificity, function, and application in gastrointestinal disorders. J Gastroenterol Hepatol. 2017;32:64-8.
70. Petrov K, Popova L, Petrova P. High lactic acid and fructose production via Mn2+-mediated conversion of inulin by Lactobacillus paracasei. Appl Env Microbiol. 2017;101:4433-45.
71. Schwab C, Vogel R, Gänzle MG. Influence of oligosaccharides on the viability and membrane properties of lactobacillus reuteri TMW1.106 during freeze-drying. Cryobiology. 2007;55:108-14.
72. Pridmore RD, Berger B, Desiere F, Vilanova D, Barretto C, Pittet A-C, et al. The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc Natl Acad Sci U S A. 2004;101:2512-7.
73. Flint HJ, Duncan SH, Louis P. The impact of nutrition on intestinal bacterial communities. Curr Opin Microbiol. 2017;38:59-65.
74. Klobasa F, Werhahn E, Butler JE. Composition of sow milk during lactation. J Anim Sci. 1987;64:1458-66.
75. Gänzle MG, Follador R. Metabolism of oligosaccharides and starch in Lactobacilli: a review. Front Microbiol. 2012;3:340.
76. Honda H, Kataoka F, Nagaoka S, Kawai Y, Kitazawa H, Itoh H, et al. β-Galactosidase, phospho-β-galactosidase and phospho-β- glucosidase activities in lactobacilli strains isolated from human faeces. Lett Appl Microbiol. 2007;45:461-6.
77. Schwab C, Sørensen KI, Gänzle MG. Heterologous expression of glycoside hydrolase family 2 and 42 β-galactosidases of lactic acid bacteria in Lactococcus lactis. Syst Appl Microbiol. 2010;33:300-7.
78. Arola H, Tamm A. Metabolism of lactose in the human body. Scand J Gastroenterol. 1994;29:21-5.
79. Krumbeck JA, Rasmussen HE, Hutkins RW, Clarke J, Shawron K, Keshavarzian A WJ. Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics. Microbiome. 2018;6(1):121.
80. Guilloteau P, Zabielski R, Hammon HM, Metges CC. Nutritional programming of gastrointestinal tract development. Is the pig a good model for man? Nutr Res Rev. 2010;23:4-22.
81. Heinritz SN, Mosenthin R, Weiss E. Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutr Res Rev. 2013;26:191-209.