Functional metagenomics reveals novel salt tolerance loci from the human gut microbiome

ISME Journal

Volumn 6, Issue 10, 2012, Pages 1916-1925

  Culligan, Eamonn P ^a,b   Sleator, Roy D ^a,c   Marchesi, Julian R ^a,d   Hill, Colin ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c Munster Technological University   (Ireland)

^d CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Akkermansia; Collinsella; Eggerthella; Human gut microbiome; Metagenomics; Salt tolerance

Indexed keywords

BACTERIUM; BIOINFORMATICS; CLONE; DIGESTIVE SYSTEM; FUNCTIONAL ROLE; GENE EXPRESSION; GENOMICS; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; MUTATION; SALINITY TOLERANCE;

ARTICLE; BACTERIAL GENE; BACTERIUM; BIOLOGY; ESCHERICHIA COLI; GASTROINTESTINAL TRACT; GENE LIBRARY; GENETICS; HUMAN; METABOLISM; METAGENOME; METAGENOMICS; MICROBIOLOGY; MUTAGENESIS; SALT TOLERANCE; TRANSPOSON;

BACTERIA; COMPUTATIONAL BIOLOGY; DNA TRANSPOSABLE ELEMENTS; ESCHERICHIA COLI; GASTROINTESTINAL TRACT; GENES, BACTERIAL; GENOMIC LIBRARY; HUMANS; METAGENOME; METAGENOMICS; MUTAGENESIS; SALT-TOLERANCE;

ACTINOBACTERIA; AKKERMANSIA; AKKERMANSIA MUCINIPHILA; COLLINSELLA; COLLINSELLA AEROFACIENS; EGGERTHELLA; ESCHERICHIA COLI; POSIBACTERIA;

EID: 84863860051     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2012.38     Document Type: Article

References (78)

1. Banik JJ, Brady SF. (2008). Cloning and characterization of new glycopeptide gene clusters found in an environmental DNA megalibrary. Proc Natl Acad Sci USA 105: 17273-17277.
2. Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP et al. (2000). Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 1902-1906.
3. Bohringer J, Fischer D, Mosler G, Hengge-Aronis R. (1995). UDP-glucose is a potential intracellular signal mole-cule in the control of expression of sigma S and sigma S-dependent genes in Escherichia coli. J Bacteriol177: 413-422.
4. Chowdhury R, Sahu G, Das J. (1996). Stress response in pathogenic bacteria. JBiosci 21: 149-160.
5. Culham DE, Lasby B, Marangoni AG, Milner JL, Steer BA, van Nues RW et al. (1993). Isolation and sequencing of Escherichia coli gene pro P reveals unusual structural features of the osmoregulatory proline/betaine trans-porter, Pro P. J Mol Biol 229: 268-276.
6. Culligan EP, Hill C, Sleator RD. (2009). Probiotics and gastrointestinal disease: successes, problems and future prospects. Gut Pathog 1: 19.
7. Ellrott K, Jaroszewski L, Li W, Wooley JC, Godzik A. (2010). Expansion of the protein repertoire in newly explored environments: human gut microbiome specific protein families. PloS Comput Biol 6: e1000798.
8. Epstein W. (2003). The roles and regulation of pota-ssium in bacteria. Prog Nucleic Acid Res Mol Biol 75: 293-320.
9. Felsenstein J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
10. Fukasawa T, Jokura K, Kurahashi K. (1962). A new enzymic defect of galactose metabolism in Escherichia coli K-12 mutants. Biochem Biophys Res Commun 7: 121-125.
11. Galperin MY, Moroz OV, Wilson KS, Murzin AG. (2006). House cleaning, a part of good housekeeping. Mol Microbiol 59: 5-19.
12. Gardan R, Duche O, Leroy-Setrin S, Labadie J. (2003). Role of ctc from Listeria monocytogenes in osmotolerance. Appl Environ Microbiol 69: 154-161.
13. Giaever HM, Styrvold OB, Kaasen I, Strom AR. (1988). Biochemical and genetic characterization of osmor-egulatory trehalose synthesis in Escherichia coli J Bacteriol 170: 2841-2849.
14. Gillespie DE, Brady SF, Bettermann AD, Cianciotto NP, Liles MR, Rondon MR et al. (2002). Isolation of antibiotics turbomycin A and B from a metagenomic library of soil microbial DNA. Appl Environ Microbiol 68: 4301-4306.
15. Gloux K, Berteau O, El Oumami H, Beguet F, Leclerc M, Dore J. (2011). A metagenomic beta-glucuronidase uncovers a core adaptive function of the human intestinal microbiome. Proc Natl Acad Sci USA 108 (Suppl 1): 4539-4546.
16. Gralla JD, Huo YX. (2008). Remodeling and activation of Escherichia coli RNA polymerase by osmolytes. Biochemistry47: 13189-13196.
17. Gross M, Marianovsky I, Glaser G (2006). Maz G\-a regulator of programmed cell death in Escherichia coli. Mol Microbiol 59: 590-601.
18. Grundling A, Schneewind O. (2007). Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus. J Bacteriol189: 2521-2530.
19. Haardt M, Kempf B, Faatz E, Bremer E. (1995). The osmoprotectant proline betaine is a major substrate for the binding-protein-dependent transport system Pro U of Escherichia coli K-12. Mol Gen Genet 246: 783-786.
20. Hayes F, Daly C, Fitzgerald GF. (1990). Identification of the minimal replicon of Lactococcus lactis subsp. lactis UC317 plasmid p CI305. Appl Environ Microbiol 56: 202-209.
21. Heath C, Hu XP, Cary SC, Cowan D. (2009). Identification of a novel alkaliphilic esterase active at low temperatures by screening a metagenomic library from antarctic desert soil. Appl Environ Microbiol 75: 4657-4659.
22. Hengge-Aronis R, Klein W, Lange R, Rimmele M, Boos W. (1991). Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpo S and are involved in stationary-phase thermotolerance in Escherichia coli. J Bacteriol 173: 7918-7924.
23. Jones BV, Marchesi Jr. (2007). Transposon-aided capture (TRACA) of plasmids resident in the human gut mobile metagenome. Nat Methods 4: 55-61.
24. Kageyama A, Benno Y, Nakase T. (1999). Phylogenetic and phenotypic evidence for the transfer of Eubacterium aerofaciens to the genus Collinsella as Collinsella aerofaciens gen. nov., comb. nov. Int JSyst Bacteriol 49 (Pt 2): 557-565.
25. Kapardar R, Ranjan R, Puri M, Sharma R. (2010b). Sequence analysis of a salt tolerant metagenomic clone. Indian J Microbiol 50: 212-215.
26. Kapardar RK, Ranjan R, Grover A, Puri M, Sharma R. (2010a). Identification and characterization of genes conferring salt tolerance to Escherichia coli from pond water metagenome. Bioresour Technol 101: 3917-3924.
27. Kazimierczak KA, Rincon MT, Patterson AJ, Martin JC, Young P, Flint HJ et al. (2008). A new tetracycline efflux gene, tet(40), is located in tandem with tet (O/32/O) in a human gut firmicute bacterium and in metagenomic library clones. Antimicrob Agents Chemother 52: 4001-4009.
28. Kempf B, Bremer E. (1998). Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170: 319-330.
29. Kilstrup M, Jacobsen S, Hammer K, Vogensen FK. (1997). Induction of heat shock proteins Dna K, Gro EL, and Gro ES by salt stress in Lactococcus lactis. Appl Environ Microbiol 63: 1826-1837.
30. Kunte HJ. (2006). Osmoregulation in bacteria: compatible solute accumulation and osmosensing. Environ Chem 3: 94-99.
31. Kurokawa K, Itoh T, Kuwahara T, Oshima K, Toh H, Toyoda A et al. (2007). Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14: 169-181.
32. Lakhdari O, Cultrone A, Tap J, Gloux K, Bernard F, Ehrlich SD etal. (2010). Functional metagenomics: a high throughput screening method to decipher microbiota-driven NF-kappa B modulation in the human gut. PloS One 5: e13092.
33. Lee DG, Jeon JH, Jang MK, Kim NY, Lee JH, Kim SJ et al. (2007). Screening and characterization of a novel fibrinolytic metalloprotease from a metagenomic library. Biotechnol Lett 29: 465-472.
34. Lee SJ, Trostel A, Le P, Harinarayanan R, Fitzgerald PC, Adhya S. (2009). Cellular stress created by intermedi-ary metabolite imbalances. Proc Natl Acad Sci USA 106: 19515-19520.
35. Leloir LF. (1951). The enzymatic transformation of uridine diphosphate glucose into a galactose derivative. Arch Biochem Biophys 33: 186-190.
36. Lopez CS, Alice AF, Heras H, Rivas EA, Sanchez-Rivas C. (2006). Role of anionic phospholipids in the adapta-tion of Bacillus subtilis to high salinity. Microbiology 152: 605-616.
37. Lu LD, Sun Q, Fan XY, Zhong Y, Yao YF, Zhao GP. (2010). Mycobacterial Maz G is a novel NTP pyrophosphohy-drolase involved in oxidative stress response. J Biol Chem 285: 28076-28085.
38. Maniatis T, Fritsch EF, Sambrook J. (1982). Molecular Cloning, A Laboratory Manual. Cold Spring Harbor Laboratory: Cold Spring Harbor, New York.
39. Markovitz A. (1977). Genetics and regulation of bacterial capsular polysaccharide synthesis and radiation sensi-tivity. In: Sutherland WI (ed.). Surface Carbohydrates of the Prokaryotic Cell. Academic Press, Inc.: London, pp 415-462.
40. Matsuo M, Kurokawa K, Nishida S, Li Y, Takimura H, Kaito C et al. (2003). Isolation and mutation site determination of the temperature-sensitive mur B mutants of Staphylo-coccus aureus. FEMS Microbiol Lett 222: 107-113.
41. Mavromatis K, Ivanova N, Barry K, Shapiro H, Goltsman E, Mc Hardy AC et al. (2007). Use of simulated data sets to evaluate the fidelity of metagenomic processing methods. Nat Methods 4: 495-500.
42. Meilleur C, Hupe JF, Juteau P, Shareck F. (2009). Isolation and characterization of a new alkali-thermostable lipase cloned from a metagenomic library. J Ind Microbiol Biotechnol 36: 853-861.
43. Miyakawa T, Matsuzawa H, Matsuhashi M, Sugino Y (1972). Cell wall peptidoglycan mutants of Escher-ichia coli K-12: existence of two clusters of genes, mra and mrb, for cell wall peptidoglycan biosynthesis. J Bacteriol 112: 950-958.
44. Nguyen TT, Klueva N, Chamareck V, Aarti A, Magpantay G, Millena AC et al. (2004). Saturation mapping of QTL regions and identification of putative candidate genes for drought tolerance in rice. Mol Genet Genomics 272: 35-46.
45. Okada Y, Makino S, Tobe T, Okada N, Yamazaki S. (2002). Cloning of rel from Listeria monocytogenes as an osmotolerance involvement gene. Appl Environ Microbiol 68: 1541-1547.
46. Padilla L, Morbach S, Kramer R, Agosin E. (2004). Impact of heterologous expression of Escherichia coli UDP-glucose pyrophosphorylase on trehalose and glycogen synthesis in Corynebacterium glutamicum. Appl Environ Microbiol 70: 3845-3854.
47. Piuri M, Sanchez-Rivas C, Ruzal SM. (2003). Adaptation to high salt in Lactobacillus: role of peptides and proteolytic enzymes. J Appl Microbiol 95: 372-379.
48. Pumbwe L, Wareham DW, Aduse-Opoku J, Brazier JS, Wexler HM. (2007). Genetic analysis ofmechanisms of multidrug resistance in a clinical isolate of Bacter-oides fragilis. Clin Microbiol Infect 13: 183-189.
49. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
50. Quintela JC, de Pedro MA, Zollner P, Allmaier G, Garcia-del Portillo F. (1997). Peptidoglycan structure of Salmonella typhimurium growing within cultured mammalian cells. Mol Microbiol 23: 693-704.
51. Real G, Henriques AO. (2006). Localization of the Bacillus subtilis mur B gene within the dcw cluster is important for growth and sporulation. J Bacteriol188: 1721-1732.
52. Saitou N, Nei M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
53. Sakamoto T, Murata N. (2002). Regulation of the desatura-tion of fatty acids and its role in tolerance to cold and salt stress. Curr Opin Microbiol 5: 208-210.
54. Sassetti CM, Rubin EJ. (2003). Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100: 12989-12994.
55. Schiller C, Frohlich CP, Giessmann T, Siegmund W, Monnikes H, Hosten N et al. (2005). Intestinal fluid volumes and transit of dosage forms as assessed by magnetic resonance imaging. Aliment Pharmacol Ther 22: 971-979.
56. Schulman H, Kennedy EP. (1977). Identification of UDP-glucose as an intermediate in the biosynthesis of the membrane-derived oligosaccharides of Escher-ichia coli. J Biol Chem 252: 6299-6303.
57. Seltmann G, Holst O. (2002). Further cell wall components of Gram-positive bacteria. In: Seltmann and Holst (eds). Bacterial Cell Wall. Springer: Germany, pp 131-161.
58. Sheehan VM, Sleator RD, Fitzgerald GF, Hill C. (2006). Heterologous expression of Bet L, a betaine uptake system, enhances the stress tolerance of Lactobacillus salivarius UCC118. Appl Environ Microbiol 72: 2170-2177.
59. Sheehan VM, Sleator RD, Hill C, Fitzgerald GF. (2007). Improving gastric transit, gastrointestinal persistence and therapeutic efficacy of the probiotic strain Bifidobacterium breve UCC2003. Microbiology 153: 3563-3571.
60. Sleator RD. (2010a). Probiotic therapy\-recruiting old friends to fight new foes. Gut Pathog 2: 5.
61. Sleator RD. (2010b). Probiotics\-a viable therapeutic alternative for enteric infections especially in the developing world. Discov Med 10: 119-124.
62. Sleator RD. (2011). Phylogenetics. Arch Microbiol 193: 235-239.
63. Sleator RD, Hill C. (2002). Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26: 49-71.
64. Sleator RD, Hill C. (2005). A novel role for the Lis RK two-component regulatory system in listerial osmotoler-ance. Clin Microbiol Infect 11: 599-601.
65. Sleator RD, Hill C. (2006). Patho-biotechnology: using bad bugs to do good things. Curr Opin Biotechnol 17: 211-216.
66. Sleator RD, Shortall C, Hill C. (2008). Metagenomics. Lett Appl Microbiol 47: 361-366.
67. Sleator RD, Walsh P. (2010). An overview of in silico protein function prediction. Arch Microbiol 192: 151-155.
68. Stintzi A, Marlow D, Palyada K, Naikare H, Panciera R, Whitworth L et al. (2005). Use of genome-wide expression profiling and mutagenesis to study the intestinal lifestyle of Campylobacter jejuni. Infect Immun 73: 1797-1810.
69. Sylvester DR, Alvarez E, Patel A, Ratnam K, Kallender H, Wallis NG. (2001). Identification and characteri-zation of UDP-N- acetylenolpyruvylglucosamine reductase (Mur B) from the Gram-positive pathogen Streptococcuspneumoniae. Biochem J355: 431-435.
70. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
71. Thompson JD, Higgins DG, Gibson TJ. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
72. Van Heijenoort J. (1996). Murein synthesis. In: Neidhardt FC, Curtis R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaecter M, Umbarger HE (eds). Escherichia coli and Salmonella: cellular and molecular biology. American Society for Microbiology: Washington, DC, pp 1025-1034.
73. Van Passel MW, Kant R, Zoetendal EG, Plugge CM, Derrien M, Malfatti SA et al. (2011). The genome of Akker-mansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagen-omes. PloS One 6: e16876.
74. Vijaranakul U, Nadakavukaren MJ, de Jonge BL, Wilkinson BJ, Jayaswal RK. (1995). Increased cell size and shortened peptidoglycan interpeptide bridge of Na Cl-stressed Staphylococcus aureus and their reversal by glycine betaine. J Bacteriol 177: 5116-5121.
75. Watson D, Sleator RD, Hill C, Gahan CG. (2008). Enhancing bile tolerance improves survival and persistence of Bifidobacterium and Lactococcus in the murine gastrointestinal tract. BMC Microbiol 8: 176.
76. Wonderling LD, Wilkinson BJ, Bayles DO. (2004). The htr A (deg P) gene of Listeria monocytogenes 10403S is essential for optimal growth under stress conditions. Appl Environ Microbiol 70: 1935-1943.
77. Zhang J, Inouye M. (2002). Maz G, a nucleoside tripho-sphate pyrophosphohydrolase, interacts with Era, an essential GTPase in Escherichia coli. J Bacteriol 184: 5323-5329.
78. Zuckerkandl E, Pauling L. (1965). Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds). Evolving Genes and Proteins. Academic Press: New York, pp 97-166.