1887

Abstract

species are important denizens of the human gut microbiome that ferment complex polysaccharides to butyrate as a terminal fermentation product, which influences human physiology and serves as an energy source for colonocytes. Previous comparative genomics analyses of the genus have examined polysaccharide degradation genes. Here, we characterize the core and pangenomes of the genus with respect to central carbon and energy metabolism, as well as biosynthesis of amino acids and B vitamins using orthology-based methods, uncovering significant differences among species in their biosynthetic capacities. Variation in gene content among species and strains was most significant for cofactor biosynthesis. Unlike all other species of that we analysed, strains lacked biosynthetic genes for riboflavin or pantothenate but possessed folate biosynthesis genes. Differences in gene content for B vitamin synthesis were matched with differences in putative salvage and synthesis strategies among species. For example, we observed extended biotin salvage capabilities in strains, which further suggest that B vitamin acquisition strategies may impact fitness in the gut ecosystem. As differences in the functional potential to synthesize components of biomass (e.g. amino acids, vitamins) can drive interspecies interactions, variation in auxotrophies of the spp. genomes may influence gut ecology. This study serves to advance our understanding of the potential metabolic interactions that influence the ecology of spp. and, ultimately, may provide a basis for rational strategies to manipulate the abundances of these species.

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2020-06-26
2020-08-09
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References

  1. Liu C, Finegold SM, Song Y, Lawson PA. Reclassification of Clostridium coccoides, Ruminococcus hansenii, Ruminococcus hydrogenotrophicus, Ruminococcus luti, Ruminococcus productus and Ruminococcus schinkii as Blautia coccoides gen. nov., comb. nov. Blautia hansenii comb. nov., Blaut. Int J Syst Evol Microbiol 2008; 58:1896–1902
    [Google Scholar]
  2. Tamanai-Shacoori Z, Smida I, Bousarghin L, Loreal O, Meuric V et al. Roseburia spp.: a marker of health?. Future Microbiol 2017; 12:157–170
    [Google Scholar]
  3. Rosero JA, Killer J, Sechovcová H, Mrázek J, Benada O et al. Reclassification of Eubacterium rectale (Hauduroy, et al. 1937) Prévot 1938 in a new genus Agathobacter gen. nov. as Agathobacter rectalis comb. nov., and description of Agathobacter ruminis sp. nov., isolated from the rumen contents of sheep and cows. Int J Syst Evol Microbiol 2016; 66:768–773
    [Google Scholar]
  4. Scott KP, Duncan SH, Flint HJ. Dietary fibre and the gut microbiota. Nutr Bull 2008; 33:201–211
    [Google Scholar]
  5. Duncan SH, Aminov RI, Scott KP, Louis P, Stanton TB et al. Proposal of Roseburia faecis sp. nov., Roseburia hominis sp. nov. and Roseburia inulinivorans sp. nov., based on isolates from human faeces. Int J Syst Evol Microbiol 20062437–2441
    [Google Scholar]
  6. Duncan SH, Louis P, Flint HJ, Bacteria L-U. Isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Micobiology 2004; 70:5810–5817
    [Google Scholar]
  7. Duncan SH, Hold GL, Barcenilla A, Stewart CS, Flint HJ. Roseburia intestinalis sp. nov., a novel saccharolytic, butyrate-producing bacterium from human faeces. Int J Syst Evol Microbiol 2002; 52:1615–1620
    [Google Scholar]
  8. Louis P, Diversity FHJ. Metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 2009; 294:1–8
    [Google Scholar]
  9. Lazarova DL, Vimentin BM. Colon cancer progression and resistance to butyrate and other HDACIs main hypothesis Wnt signalling and butyrate vimentin and epithelial to mesenchymal transition in colorectal cancer cells. J Cell Mol Med 2016; 20:989–993
    [Google Scholar]
  10. Corrêa RO, Fachi JL, Vieira A, Sato FT, Vinolo MAR. Regulation of immune cell function by short-chain fatty acids. Clin Transl Immunol. 2016; 5:1–8
    [Google Scholar]
  11. Si X, Shang W, Zhou Z, Strappe P, Wang B et al. Gut Microbiome-Induced shift of acetate to butyrate positively manages dysbiosis in high fat diet. Mol Nutr Food Res 2018; 62:1–12
    [Google Scholar]
  12. Machiels K, Joossens M, Sabino J, De Preter V, Arijs I et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 2014; 63:1275–1283 [CrossRef][PubMed]
    [Google Scholar]
  13. Borges-canha M, Portela-cidade JP, Dinis-ribeiro M, Leite-moreira AF, Pimentel-nunes P. Role of colonic microbiota in colorectal carcinogenesis : A systematic review. Rev Española Enfermedades Dig 2015; 107:659–671
    [Google Scholar]
  14. Rivière A, Selak M, Lantin D, Leroy F, De VL. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 2016; 7:
    [Google Scholar]
  15. Wu T, Zhang Z, Liu B, Hou D, Liang Y et al. Gut microbiota dysbiosis and bacterial community assembly associated with cholesterol gallstones in large-scale study. BMC Genomics 2013; 14:1
    [Google Scholar]
  16. Kasahara K, Krautkramer KA, Org E, Romano KA, Kerby RL et al. Interactions between Roseburia intestinalis and diet modulate atherogenesis in a murine model. Nat Microbiol [Internet] 2018; 3:1461–1471
    [Google Scholar]
  17. Hu Y, Feng Y, Wu J, Liu F, Zhang Z et al. The gut microbiome signatures discriminate healthy from pulmonary tuberculosis patients. Front Cell Infect Microbiol 2019; 9:1–8
    [Google Scholar]
  18. Romine MF, Rodionov DA, Maezato Y, Osterman AL, Nelson WC. Underlying mechanisms for syntrophic metabolism of essential enzyme cofactors in microbial communities. ISME J 2017; 11:1434–1446 [CrossRef][PubMed]
    [Google Scholar]
  19. Konopka A, Lindemann S, Fredrickson J. Dynamics in microbial communities : unraveling mechanisms to identify principles. ISME J 2015; 9:1488–1495
    [Google Scholar]
  20. Degnan PH, Barry NA, Mok KC, Taga ME, Goodman AL. Human gut microbes use multiple transporters to distinguish vitamin B 12 analogs and compete in the gut. Cell Host Microbe 2014; 15:47–57
    [Google Scholar]
  21. Degnan PH, Taga ME, Goodman AL. Vitamin B12 as a modulator of gut microbial ecology. Cell Metab 2014; 20:769–778 [CrossRef][PubMed]
    [Google Scholar]
  22. Watanabe F. Vitamin B12 sources and bioavailability. Exp Biol Med 2007; 232:1266–1274
    [Google Scholar]
  23. Okuda K. Discovery of vitamin B 12 in the liver and its absorption factor in the stomach : A historical review*. J Gastroenterol Hepatol 1999; 14:301–308
    [Google Scholar]
  24. Sheridan PO, Martin JC, Lawley TD, Browne HP, Harris HMB et al. Polysaccharide utilization loci and nutritional specialization in a dominant group of butyrate-producing human colonic Firmicutes. Microb Genomics 2016; 2:1–16
    [Google Scholar]
  25. Anand S, Kaur H, Mande SS. Comparative in silico analysis of butyrate production pathways in gut Commensals and pathogens. Front Microbiol 2016; 7:1–12
    [Google Scholar]
  26. Louis P, Young P, Holtrop G, Flint HJ. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ Microbiol 2010; 12:304–314
    [Google Scholar]
  27. Trachsel J, Bayles DO, Looft T, Levine UY, Allen K. Function and Phylogeny of Bacterial Butyryl Coenzyme A : Acetate Transferases and Their Diversity in the Proximal Colon of Swine. Appl Environ Micobiology 2016; 82:6788–6798
    [Google Scholar]
  28. Rossi M, Amaretti A, Raimondi S. Folate production by probiotic bacteria; 2011118–134
  29. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA et al. Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation. Nature 2016; 533:543–546
    [Google Scholar]
  30. 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; 25:1043–1055
    [Google Scholar]
  31. Arkin AP, Cottingham RW, Henry CS, Harris NL, Stevens RL et al. KBase: the United States department of energy systems biology knowledgebase. Nat Biotechnol 2018; 36:566–569
    [Google Scholar]
  32. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75
    [Google Scholar]
  33. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The seed and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014; 42:206–214
    [Google Scholar]
  34. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S et al. RASTtk : A modular and extensible implementation of the RAST algorithm for annotating batches of genomes. Sci Rep 2015; 5:1–6
    [Google Scholar]
  35. Meyer F, Overbeek R, Rodriguez A. FIGfams : yet another set of protein families. Nucleic Acids Res 2009; 37:6643–6654
    [Google Scholar]
  36. Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Informatics 2009; 23:205–211
    [Google Scholar]
  37. Haft DH, Selengut JD, Richter RA, Harkins D, Basu MK et al. TIGRFAMs and genome properties in 2013. Nucleic Acids Res 2013; 41:387–395
    [Google Scholar]
  38. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt Y et al. Pfam : the protein families database. Nucleic Acids Res 2014; 42:222–230
    [Google Scholar]
  39. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016; 428:726–731 [CrossRef][PubMed]
    [Google Scholar]
  40. Tabari E, Su Z. PorthoMCL : Parallel orthology prediction using MCL for the realm of massive genome availability.. Big Data Anal [Internet] 20171–5
    [Google Scholar]
  41. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016msw054
    [Google Scholar]
  42. Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948
    [Google Scholar]
  43. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526
    [Google Scholar]
  44. Wu M, Scott AJ. Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 2012; 28:1033–1034
    [Google Scholar]
  45. Nei M. Molecular Evolutionary Genetics Columbia university press; 1987
    [Google Scholar]
  46. Levine UY, Looft T, Allen HK, Stanton TB. Butyrate-prodcing bacteria, including mucin degraders, from the swine intestinal tract. Appl Environ Micobiology 2013; 79:3879–3881
    [Google Scholar]
  47. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ et al. A new view of the tree of life. Nat Microbiol 2016; 1:1–6
    [Google Scholar]
  48. Wu M, Eisen JA, simple A. Fast, and accurate method of phylogenomic inference. Genome Biol 2008; 9:R151
    [Google Scholar]
  49. Hasegawa M, Hashimoto T. Ribosomal RNA trees misleading?. Nature 1993; 361:23
    [Google Scholar]
  50. Lockhart PJ, Howe CJ, Bryant DA, Beanland TJ, Larkum AW. Substitutional bias confounds inference of cyanelle origins from sequence data. J Mol Evol 1992; 34:153–162
    [Google Scholar]
  51. Stincone A, Prigione A, Cramer T, Wamelink MMC, Campbell K et al. The return of metabolism : biochemistry and physiology of the pentose phosphate pathway. Biol Rev 2015; 90:927–963
    [Google Scholar]
  52. Miller TL, Wolin MJ. Pathways of acetate, propionate, and butyrate formation by the human fecal microbial flora. Appl Environ Micobiology 1996; 62:1589–1592
    [Google Scholar]
  53. Flamholz A, Noor E, Bar-Even A, Liebermeister W, Milo R. Glycolytic strategy as a tradeoff between energy yield and protein cost. Proc Natl Acad Sci U S A 2013; 110:10039–10044
    [Google Scholar]
  54. Leanti La Rosa S, Leth ML, Michalak L, Hansen ME, Pudlo NA et al. The human gut firmicute Roseburia intestinalis is a primary degrader of dietary β -mannans. Nat Commun 20191–14
    [Google Scholar]
  55. Kawahara R, Saburi W, Odaka R, Taguchi H, Ito S et al. Metabolic mechanism of mannan in a ruminal bacterium, Ruminococcus albus, involving two mannoside phosphorylases and cellobiose 2-epimerase: discovery of a new carbohydrate phosphorylase, beta-1,4-mannooligosaccharide phosphorylase. J Biol Chem 2012; 287:42389–42399
    [Google Scholar]
  56. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 2010; 5:220–230
    [Google Scholar]
  57. Hillman ET, Lu H, Yao T, Nakatsu CH. Microbial ecology along the gastrointestinal tract. Microbes Environ 2017; 32:
    [Google Scholar]
  58. Singh RK, Chang HW, Yan D, Lee KM, Ucmak D et al. Influence of diet on the gut microbiome and implications for human health. J Transl Med 20171–17
    [Google Scholar]
  59. So D, Whelan K, Rossi M, Morrison M, Holtmann G et al. Dietary fiber intervention on gut microbiota composition in healthy adults : a systematic review and meta-analysis. Am J Clin Nutr 2018965–983
    [Google Scholar]
  60. Quivey RG, Kuhnert WL. Genetics of acid adaptation in oral streptococci. Critcal Rev Oral Biol Med. 2001; 12:301–314
    [Google Scholar]
  61. Beyenbach KW, Wieczorek H. The V-type H + ATPase : molecular structure and function, physiological roles and regulation. J Exp Biol 2006; 209:577–589
    [Google Scholar]
  62. Nelson N, Perzov N, Cohen A, Hagai K, Padler V et al. The cellular biology of proton-motive force generation by V-ATPases. J Exp Biol 2000; 95:89–95
    [Google Scholar]
  63. Takase K, Kakinuma S, Yamato I, Konishi K, Igarashi K et al. Sequencing and characterization of the ntp gene cluster for vacuolar-type Na(+)-translocating ATPase of Enterococcus hirae. J Biol Chem 1994; 269:11037–11044
    [Google Scholar]
  64. Hilario E, Gogarten JP. Horizontal transfer of ATPase genes-the tree of life becomes a net of life. Biosystems 1993; 31:111–119
    [Google Scholar]
  65. Lolkema JS, Chaban Y, Boekema EJ. Subunit composition, structure, and distribution of bacterial V-type ATPases. J Bioenerg Biomembr 2003; 35:323–335
    [Google Scholar]
  66. Schuchmann K, Muller V. A bacterial electron-bifurcating hydrogenase. J Biol Chem 2012; 287:31165–31171
    [Google Scholar]
  67. Wolf PG, Biswas A, Morales SE, Greening C. Gaskins R. H2 metabolism is widespread and diverse among human colonic microbes. Gut Microbes 2016; 7:234–245
    [Google Scholar]
  68. Duncan SH, Barcenilla A, Stewart CS, Pryde SE, Flint HJ. Acetate Utilization and Butyryl Coenzyme A (CoA): Acetate-CoA Transferase in Butyrate-Producing Bacteria from the Human Large Intestine. Appl Environ Micobiology 2002; 68:5186–5190
    [Google Scholar]
  69. Chowdhury NP, Mowafy AM, Demmer JK, Upadhyay V, Koelzer S et al. Studies on the mechanism of electron bifurcation catalyzed by electron transferring flavoprotein (ETF) and butyryl-CoA dehydrogenase (BCD) of Acidaminococcus fermentans. J Biol Chem 2014; 289:5145–5157
    [Google Scholar]
  70. Buckel W, Thauer RK, Bifurcation F-BE. Ferredoxin, Flavodoxin, and Anaerobic Respiration With Protons (Ech) or NAD + (Rnf) as Electron Acceptors : A Historical Review. Front Microbiol 2018; 9:1–24
    [Google Scholar]
  71. Macfarlane GT, McBain AJ, Microbiota C. In: colonic microbiota. Nutrition and Health 19991–27 p.
    [Google Scholar]
  72. Ríos-Covián D, Ruas-Madiedo P, Margolles A, Gueimonde M, De los Reyes-Gavilán CG et al. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol 2016; 7:1–9
    [Google Scholar]
  73. Donohoe DR, Collins LB, Wali A, Bigler R, Sun W et al. The Warburg effect dictates the mechanism of Butyrate-Mediated histone acetylation and cell proliferation. Mol Cell 2012; 48:612–626
    [Google Scholar]
  74. Thamer W, Cirpus I, Hans M, Pierik AJ, Selmer T. Bill E. A two [4Fe-4S]-cluster-containing ferredoxin as an alternative electron donor for 2-hydroxyglutaryl-CoA dehydratase from Acidaminococcus fermentans. Arch Microbiol 2003; 179:197–204
    [Google Scholar]
  75. Site G, Frey M, Rothe M, Wagner V, Knappes J et al. Adenosylmethionine-dependent synthesis of the glycyl radical in pyruvate formate-lyase by abstraction of the glycine C-2 pro-S hydrogen atom. Studies of [2H]glycine-substituted enzyme and peptides homologous to the glycine 734 site. J Biolo 1994; 269:12432–12437
    [Google Scholar]
  76. Atalysis C, Frey PA. Radical mechanisms of enzymatic catalysis. Annu Rev Biochem 2001; 70:121–148
    [Google Scholar]
  77. Falony G, Verschaeren A, De BF, De PV, Verbeke K. In vitro kinetics of prebiotic inulin-type fructan fermentation by butyrate-producing colon bacteria: implementation of online gas chromatography for quantitative analysis of carbon dioxide and hydrogen gas production. Appl Environ Micobiology 2009; 75:5884–5892
    [Google Scholar]
  78. Folsom JP, Parker AE, Carlson RP. Physiological and proteomic analysis of Escherichia coli iron-limited chemostat growth. J Bacteriol 2014; 196:2748–2761
    [Google Scholar]
  79. Dostal A, Lacroix C, Bircher L, Pham VT, Follador R et al. Iron modulates butyrate production by a child gut microbiota in. MBio 2015; 6:1–12
    [Google Scholar]
  80. Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS et al. Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr 2004; 91:915–923
    [Google Scholar]
  81. Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS et al. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Micobiology 2000; 66:1654–1661
    [Google Scholar]
  82. Louis P, Mccrae SI, Charrier C, Flint HJ. Organization of butyrate synthetic genes in human colonic bacteria : phylogenetic conservation and horizontal gene transfer. FEMS Microbiol Lett 2007; 269:240–247
    [Google Scholar]
  83. Herrmann G, Jayamani E, Mai G, Buckel W. Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J Bacteriol 2008; 190:784–791
    [Google Scholar]
  84. Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W et al. Coupled ferredoxin and Crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase / ETF complex from Clostridium kluyveri. J Bacteriol 2008; 190:843–850
    [Google Scholar]
  85. Bennett GN, Rudolph FB. The central metabolic pathway from acetyl-CoA to butyryl-CoA in Clostridium acetobutylicum. FEMS Microbiol Rev 1995; 17:241–249
    [Google Scholar]
  86. Aboulnaga E, Pinkenburg O, Schiffels J, El-refai A, Buckel W et al. Effect of an oxygen-tolerant bifurcating butyryl coenzyme A dehydrogenase / electron-transferring flavoprotein complex from Clostridium difficile on butyrate production in Escherichia coli . J Bacteriol 2013; 195:3704–3713
    [Google Scholar]
  87. Demmer JK, Chowdhury NP, Selmer T, Ermler U, Buckel W. The semiquinone swing in the bifurcating electron transferring flavoprotein/butyryl-CoA dehydrogenase complex from Clostridium difficil . Nat Commun 2017; 8:1–10
    [Google Scholar]
  88. Heßlinger C, Fairhurst SA. Novel keto acid formate-lyase and propionate kinase enzymes are components of an anaerobic pathway in Escherichia coli that degrades L -threonine to propionate. Mol Microbiol 1998; 27:477–492
    [Google Scholar]
  89. Scott KP, Martin JC, Campbell G, Mayer C, Flint HJ. Whole-Genome transcription profiling reveals genes up-regulated by growth on fucose in the human gut bacterium Roseburia inulinivorans . J Bacteriol 2006; 188:4340–4349
    [Google Scholar]
  90. Reichardt N, Duncan SH, Young P, Belenguer A, Leitch CM et al. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J 2014; 8:1323–1335
    [Google Scholar]
  91. Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Publ Gr [Internet]. 2014;(September). Available from: http://dx.doi.org/10.1038/nrmicro3344 .
  92. Walker AW, Duncan SH, Leitch ECM, Child MW, Flint HJ. pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Micobiology 2005; 71:3692–3700
    [Google Scholar]
  93. Lindemann SR, Mobberley JM, Cole JK, Markillie LM, Taylor RC et al. Predicting Species-Resolved macronutrient acquisition during succession in a model phototrophic biofilm using an integrated ‘ omics approach. Front Microbiol 2017; 8:1–15
    [Google Scholar]
  94. Duarte AG, Santos AA, Pereira IAC. Electron transfer between the QmoABC membrane complex and adenosine 5 ′ -phosphosulfate reductase. Biochim Biophys Acta 1857; 2016:380–386
    [Google Scholar]
  95. Fuller MF, Reeds PJ. Nitrogen cycling in the gut. Annu Rev Nutr 1998; 18:385–411
    [Google Scholar]
  96. Sheffner AL, Kirsner JB, Palmer WL. Studies on amino acid excretion in man; amino acids in feces. J Biol Chem 1948; 176:89–93
    [Google Scholar]
  97. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ et al. Metagenomic analysis of the human distal gut microbiome. Science 2006; 312:1355–1360
    [Google Scholar]
  98. Weinstock O, Sella C, Chipman DM, Barak ZEE V. Properties of subcloned subunits of bacterial acetohydroxy acid synthases. J Bacteriol. 1992; 174:5560–5566
    [Google Scholar]
  99. Wang P, Tang S, Nemr K, Flick R, Yan J et al. Refined experimental annotation reveals conserved corrinoid autotrophy in chloroform-respiring Dehalobacter isolates. Isme J 2017; 11:626–640
    [Google Scholar]
  100. Mee MT, Collins JJ, Church GM, Wang HH. Syntrophic exchange in synthetic microbial communities. Proc Natl Acad Sci U S A 2014; 111:E2149–2156
    [Google Scholar]
  101. Singh SK, Yang K, Karthikeyan S, Huynh T, Zhang X et al. The thrH Gene Product of Pseudomonas aeruginosa Is a Dual Activity Enzyme with a Novel Phosphoserine:Homoserine Phosphotransferase Activity. J. Biol. Chem. 2004; 279:13166–13173 [CrossRef]
    [Google Scholar]
  102. Typas A, Banzhaf M, Gross CA, Vollmer W. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Publ Gr 2011; 10:123–136
    [Google Scholar]
  103. Akashi H, Gojobori T. Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis . Proc Natl Acad Sci U S A 2002; 99:3695–3700 [CrossRef]
    [Google Scholar]
  104. Fani R, Alifano P, Allotta G, Bazzicalupo M, Carlomagno MS et al. The histidine operon of Azospirillum brasilense: organization, nucleotide sequence and functional analysis. Res Microbiol 1993; 144:187–200 [CrossRef][PubMed]
    [Google Scholar]
  105. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G et al. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 1997; 390:249–256 [CrossRef][PubMed]
    [Google Scholar]
  106. Price MN, Alm EJ, Arkin AP. The histidine operon is ancient. J Mol Evol 2006; 62:807–808 [CrossRef][PubMed]
    [Google Scholar]
  107. Bond JP, Francklyn C. Proteobacterial histidine-biosynthetic pathways are paraphyletic. J Mol Evol 2000; 50:339–347 [CrossRef][PubMed]
    [Google Scholar]
  108. Myers RS, Amaro RE, Luthey-Schulten ZA, Davisson VJ. Reaction coupling through interdomain contacts in imidazole glycerol phosphate synthase. Biochemistry 2005; 44:11974–11985 [CrossRef][PubMed]
    [Google Scholar]
  109. Winkler ME, Ramos-Montañez S. Biosynthesis of histidine. EcoSal Plus 2009; 3:1–34 [CrossRef]
    [Google Scholar]
  110. Sissler M, Delorme C, Bond J, Ehrlich SD, Renault P et al. An aminoacyl-tRNA synthetase paralog with a catalytic role in histidine biosynthesis. Proc Natl Acad Sci U S A 1999; 96:8985–8990 [CrossRef][PubMed]
    [Google Scholar]
  111. Bovee ML, Champagne KS, Demeler B, Francklyn CS. The quaternary structure of the HisZ-HisG N-1-(5'-phosphoribosyl)-ATP transferase from Lactococcus lactis. Biochemistry 2002; 41:11838–11846 [CrossRef][PubMed]
    [Google Scholar]
  112. Ajdić D, McShan WM, McLaughlin RE, Savic G, Chang J, Carson MB et al. Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci U S A 2002; 99:14434–14439 [CrossRef][PubMed]
    [Google Scholar]
  113. Sañudo-Wilhelmy SA, Cutter LS, Durazo R, Smail EA, Gómez-Consarnau L et al. Multiple B-vitamin depletion in large areas of the coastal Ocean. Proc Natl Acad Sci U S A 2012; 109:14041–14045 [CrossRef][PubMed]
    [Google Scholar]
  114. Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS. Comparative genomics of thiamin biosynthesis in procaryotes. J Biol Chem 2002; 277:48949–48959 [CrossRef]
    [Google Scholar]
  115. Bousis S, Setyawati I, Diamanti E, Slotboom DJ, Hirsch AKH. Energy-Coupling factor transporters as novel antimicrobial targets. Adv Therap. 2019; 2:1800066–17 [CrossRef]
    [Google Scholar]
  116. Rodionov DA, Hebbeln P, Eudes A, ter Beek J, Rodionova IA et al. A novel class of modular transporters for vitamins in prokaryotes. J Bacteriol 2009; 191:42–51 [CrossRef][PubMed]
    [Google Scholar]
  117. Gerdes S, Lerma-Ortiz C, Frelin O, Seaver SMD, Henry CS et al. Plant B vitamin pathways and their compartmentation: a guide for the perplexed. J Exp Bot 2012; 63:5379–5395 [CrossRef][PubMed]
    [Google Scholar]
  118. Magnttir Stefan­a, Ravcheev D, de Crcy-Lagard Valrie, Thiele I, Magnúsdóttir S, De C-lagardV. Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front Genet 2015; 6:1–18 [CrossRef]
    [Google Scholar]
  119. Lin S, Cronan JE. Closing in on complete pathways of biotin biosynthesis. Mol Biosyst 2011; 7:1811–1821 [CrossRef][PubMed]
    [Google Scholar]
  120. Satiaputra J, Shearwin KE, Booker GW, Polyak SW. Mechanisms of biotin-regulated gene expression in microbes. Synth Syst Biotechnol 2016; 1:17–24 [CrossRef][PubMed]
    [Google Scholar]
  121. Finkenwirth F, Kirsch F, Eitinger T. Solitary BioY proteins mediate biotin transport into recombinant Escherichia coli. J Bacteriol 2013; 195:4105–4111 [CrossRef][PubMed]
    [Google Scholar]
  122. Santander PJ, Roessner CA, Stolowich NJ, Holderman MT, Scott AI. How corrinoids are synthesized without oxygen: nature's first pathway to vitamin B12. Chem Biol 1997; 4:659–666 [CrossRef][PubMed]
    [Google Scholar]
  123. Raux E, Schubert HL, Warren MJ. Biosynthesis of cobalamin (vitamin B12): a bacterial conundrum. Cell Mol Life Sci 2000; 57:1880–1893 [CrossRef][PubMed]
    [Google Scholar]
  124. Lawrence AD, Deery E, McLean KJ, Munro AW, Pickersgill RW et al. Identification, characterization, and structure/function analysis of a corrin reductase involved in adenosylcobalamin biosynthesis. J Biol Chem 2008; 283:10813–10821 [CrossRef][PubMed]
    [Google Scholar]
  125. Locher KP, Lee AT, Rees DC. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 2002; 296:1091–1098 [CrossRef][PubMed]
    [Google Scholar]
  126. Ivetac A, Campbell JD, Sansom MSP. Dynamics and function in a bacterial ABC transporter: simulation studies of the BtuCDF system and its components. Biochemistry 2007; 46:2767–2778 [CrossRef][PubMed]
    [Google Scholar]
  127. Santos JA, Rempel S, Mous STM, Pereira CT, Ter Beek J et al. Functional and structural characterization of an ECF-type ABC transporter for vitamin B12. eLife 2018; 7:e35828 [CrossRef][PubMed]
    [Google Scholar]
  128. Stegen JC, Lin X, Konopka AE, Fredrickson JK. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 2012; 6:1653–1664 [CrossRef][PubMed]
    [Google Scholar]
  129. de Muinck EJ, Lundin KEA, Trosvik P. Linking spatial structure and community-level biotic interactions through Cooccurrence and time series modeling of the human intestinal microbiota. mSystems 2017; 2: [CrossRef][PubMed]
    [Google Scholar]
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