Metagenomic identification of a novel salt tolerance gene from the human gut microbiome which encodes a membrane protein with homology to a brp/blh-family β-carotene 15,15′-monooxygenase

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

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

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c Department of Chemistry   (Ireland)

^d CARDIFF UNIVERSITY   (United Kingdom)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CAROTENE 15,15' MONOOXYGENASE; CAROTENOID; MEMBRANE PROTEIN; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENE; BRPAATFA GENE; BRPAL GENE; BRPAS GENE; CELL MEMBRANE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION; GENE IDENTIFICATION; GENE LIBRARY; HUMAN; INTESTINE FLORA; METAGENOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PIGMENTATION; SALT TOLERANCE; SEQUENCE HOMOLOGY; BACTERIUM; DNA SEQUENCE; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; PROCEDURES;

BACTERIA; BACTERIAL PROTEINS; BETA-CAROTENE 15,15'-MONOOXYGENASE; CLONING, MOLECULAR; GASTROINTESTINAL TRACT; HUMANS; MEMBRANE PROTEINS; METAGENOMICS; MOLECULAR SEQUENCE DATA; SALT-TOLERANCE; SEQUENCE ANALYSIS, DNA;

EID: 84904866512     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103318     Document Type: Article

References (82)

1. Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, et al. (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331: 463-467.
2. Iwai S, Chai B, Sul WJ, Cole JR, Hashsham SA, et al. (2010) Gene-targeted-metagenomics reveals extensive diversity of aromatic dioxygenase genes in the environment. ISME J 4: 279-285.
3. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, et al. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74. (Pubitemid 38451457)
4. Culligan EP, Sleator RD, Marchesi JR, Hill C (2013) Metagenomics and novel gene discovery: Promise and potential for novel therapeutics. Virulence 5.
5. Gillespie DE, Brady SF, Bettermann AD, Cianciotto NP, Liles 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. (Pubitemid 34988109)
6. 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.
7. Kallifidas D, Kang HS, Brady SF (2012) Tetarimycin A, an MRSA-active antibiotic identified through induced expression of environmental DNA gene clusters. J Am Chem Soc 134: 19552-19555.
8. Lammle K, Zipper H, Breuer M, Hauer B, Buta C, et al. (2007) Identification of novel enzymes with different hydrolytic activities by metagenome expression cloning. J Biotechnol 127: 575-592. (Pubitemid 44970498)
9. Feeney A, Sleator RD (2012) The human gut microbiome: the ghost in the machine. Future Microbiol 7: 1235-1237.
10. Sleator RD (2010) The human superorganism - of microbes and men. Med Hypotheses 74: 214-215.
11. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
12. Hoffmann RF, McLernon S, Feeney A, Hill C, Sleator RD (2013) A single point mutation in the listerial betL sigma (A) -dependent promoter leads to improved osmo- and chill-tolerance and a morphological shift at elevated osmolarity. Bioengineered 4.
13. Louis P, O'Byrne CP (2010) Life in the gut: microbial responses to stress in the gastrointestinal tract. Sci Prog 93: 7-36.
14. Sleator RD, Watson D, Hill C, Gahan CG (2009) The interaction between Listeria monocytogenes and the host gastrointestinal tract. Microbiology 155: 2463-2475.
15. Hill C, Cotter PD, Sleator RD, Gahan CGM (2001) Bacterial stress response in Listeria monocytogenes: jumping the hurdles imposed by minimal processing. International Dairy Journal 12: 273-283. (Pubitemid 34234404)
16. Sleator RD, Hill C (2002) Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26: 49-71. (Pubitemid 34454775)
17. Sleator RD, Gahan CG, Hill C (2003) A postgenomic appraisal of osmotolerance in Listeria monocytogenes. Appl Environ Microbiol 69: 1-9. (Pubitemid 36077450)
18. Epstein W (2003) The roles and regulation of potassium in bacteria. Prog Nucleic Acid Res Mol Biol 75: 293-320.
19. Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170: 319-330. (Pubitemid 28458129)
20. Kunte HJ (2006) Osmoregulation in Bacteria: Compatible Solute Accumulation and Osmosensing. Environmental Chemistry 3: 94-99.
21. Culligan EP, Marchesi JR, Hill C, Sleator RD (2012) Mining the human gut microbiome for novel stress resistance genes. Gut Microbes 3: 394-397.
22. Culligan EP, Sleator RD, Marchesi JR, Hill C (2012) Functional metagenomics reveals novel salt tolerance loci from the human gut microbiome. ISME J 6: 1916-1925.
23. Culligan EP, Sleator RD, Marchesi JR, Hill C (2013) Functional Environmental Screening of a Metagenomic Library Identifies stlA; A Unique Salt Tolerance Locus from the Human Gut Microbiome. PLOS ONE 8: e82985.
24. Kim YS, Kim NH, Yeom SJ, Kim SW, Oh DK (2009) In vitro characterization of a recombinant Blh protein from an uncultured marine bacterium as a β-carotene 15,15′-dioxygenase. J Biol Chem 284: 15781-15793.
25. Peck RF, Echavarri-Erasun C, Johnson EA, Ng WV, Kennedy SP, et al. (2001) brp and blh are required for synthesis of the retinal cofactor of bacteriorhodopsin in Halobacterium salinarum. J Biol Chem 276: 5739-5744.
26. Haardt M, Kempf B, Faatz E, Bremer E (1995) The osmoprotectant proline betaine is a major substrate for the binding-protein-dependent transport system ProU of Escherichia coli K-12. Mol Gen Genet 246: 783-786.
27. Hayes F, Daly C, Fitzgerald GF (1990) Identification of the Minimal Replicon of Lactococcus lactis subsp. lactis UC317 Plasmid pCI305. Appl Environ Microbiol 56: 202-209. (Pubitemid 20031203)
28. Jones BV, Marchesi JR (2007) Transposon-aided capture (TRACA) of plasmids resident in the human gut mobile metagenome. Nat Methods 4: 55-61. (Pubitemid 46029477)
29. Besemer J, Borodovsky M (2005) GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 33: W451-454. (Pubitemid 44529960)
30. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795. (Pubitemid 38829638)
31. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-37.
32. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, et al. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-229.
33. Sigrist CJ, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, et al. (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38: D161-166.
34. Soding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33: W244-248. (Pubitemid 44529917)
35. Sonnhammer EL, von Heijne G, Krogh A (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6: 175-182.
36. Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, et al. (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112: 531-552.
37. Jaroszewski L, Rychlewski L, Li Z, Li W, Godzik A (2005) FFAS03: a server for profile-profile sequence alignments. Nucleic Acids Res 33: W284-288. (Pubitemid 44529927)
38. Markowitz VM, Ivanova NN, Szeto E, Palaniappan K, Chu K, et al. (2008) IMG/M: a data management and analysis system for metagenomes. Nucleic Acids Res 36: D534-538. (Pubitemid 351149780)
39. Markowitz VM, Chen IM, Chu K, Szeto E, Palaniappan K, et al. (2012) IMG/M-HMP: a metagenome comparative analysis system for the Human Microbiome Project. PLoS One 7: e40151.
40. Human-Microbiome-Project-Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486: 207-214.
41. Hoffmann T, von Blohn C, Stanek A, Moses S, Barzantny H, et al. (2012) Synthesis, release, and recapture of compatible solute proline by osmotically stressed Bacillus subtilis cells. Appl Environ Microbiol 78: 5753-5762.
42. Sleator RD, Gahan CG, Hill C (2001) Identification and disruption of the proBA locus in Listeria monocytogenes: role of proline biosynthesis in salt tolerance and murine infection. Appl Environ Microbiol 67: 2571-2577. (Pubitemid 33639728)
43. Bayley DP, Rocha ER, Smith CJ (2000) Analysis of cepA and other Bacteroides fragilis genes reveals a unique promoter structure. FEMS Microbiol Lett 193: 149-154.
44. Vingadassalom D, Kolb A, Mayer C, Rybkine T, Collatz E, et al. (2005) An unusual primary sigma factor in the Bacteroidetes phylum. Mol Microbiol 56: 888-902. (Pubitemid 40646763)
45. Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318 (Pt 1): 1-14.
46. Martinez A, Bradley AS, Waldbauer JR, Summons RE, DeLong EF (2007) Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host. Proc Natl Acad Sci U S A 104: 5590-5595. (Pubitemid 47175725)
47. Wang Z, O'Shaughnessy TJ, Soto CM, Rahbar AM, Robertson KL, et al. (2012) Function and regulation of Vibrio campbellii proteorhodopsin: acquired phototrophy in a classical organoheterotroph. PLoS One 7: e38749.
48. Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, et al. (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 1902-1906.
49. Sabehi G, Loy A, Jung KH, Partha R, Spudich JL, et al. (2005) New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol 3: e273.
50. von Lintig J, Vogt K (2000) Filling the gap in vitamin A research. Molecular identification of an enzyme cleaving β-carotene to retinal. J Biol Chem 275: 11915-11920.
51. Rost B (1999) Twilight zone of protein sequence alignments. Protein Eng 12: 85-94.
52. Sleator RD (2012) Proteins: form and function. Bioeng Bugs 3: 80-85.
53. Kerfeld CA, Sawaya MR, Brahmandam V, Cascio D, Ho KK, et al. (2003) The crystal structure of a cyanobacterial water-soluble carotenoid binding protein. Structure 11: 55-65. (Pubitemid 36074967)
54. Gruszecki WI, Strzalka K (2005) Carotenoids as modulators of lipid membrane physical properties. Biochim Biophys Acta 1740: 108-115. (Pubitemid 40798219)
55. Maresca JA, Bryant DA (2006) Two genes encoding new carotenoid-modifying enzymes in the green sulfur bacterium Chlorobium tepidum. J Bacteriol 188: 6217-6223. (Pubitemid 44448563)
56. Pelz A, Wieland KP, Putzbach K, Hentschel P, Albert K, et al. (2005) Structure and biosynthesis of staphyloxanthin from Staphylococcus aureus. J Biol Chem 280: 32493-32498. (Pubitemid 41361862)
57. Kim SH, Lee PC (2012) Functional expression and extension of staphylococcal staphyloxanthin biosynthetic pathway in Escherichia coli. J Biol Chem 287: 21575-21583.
58. Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB J 9: 1551-1558.
59. Pevsner J (2009) Bioinformatics and Functional Genomics: 2nd Edition.: John Wiley & Sons Inc, Hoboken, New Jersey, USA.
60. Spudich JL, Sineshchekov OA, Govorunova EG (2013) Mechanism divergence in microbial rhodopsins. Biochim Biophys Acta.
61. Sleator RD (2013) A Beginner's Guide to Phylogenetics. Microb Ecol 66: 1-4.
62. Sleator RD (2011) Phylogenetics. Arch Microbiol 193: 235-239.
63. de la Torre JR, Christianson LM, Beja O, Suzuki MT, Karl DM, et al. (2003) Proteorhodopsin genes are distributed among divergent marine bacterial taxa. Proc Natl Acad Sci U S A 100: 12830-12835. (Pubitemid 37339985)
64. Sharma AK, Spudich JL, Doolittle WF (2006) Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol 14: 463-469. (Pubitemid 44537809)
65. McCarren J, DeLong EF (2007) Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environ Microbiol 9: 846-858. (Pubitemid 46397080)
66. Uchiyama T, Miyazaki K (2009) Functional metagenomics for enzyme discovery: challenges to efficient screening. Curr Opin Biotechnol 20: 616-622.
67. Stack HM, Sleator RD, Bowers M, Hill C, Gahan CG (2005) Role for HtrA in stress induction and virulence potential in Listeria monocytogenes. Appl Environ Microbiol 71: 4241-4247. (Pubitemid 41129473)
68. Battesti A, Majdalani N, Gottesman S (2011) The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 65: 189-213.
69. Bohringer J, Fischer D, Mosler G, Hengge-Aronis R (1995) UDP-glucose is a potential intracellular signal molecule in the control of expression of sigma S and sigma S-dependent genes in Escherichia coli. J Bacteriol 177: 413-422.
70. Hengge-Aronis R, Klein W, Lange R, Rimmele M, Boos W (1991) Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J Bacteriol 173: 7918-7924.
71. Cheville AM, Arnold KW, Buchrieser C, Cheng CM, Kaspar CW (1996) rpoS regulation of acid, heat, and salt tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 62: 1822-1824. (Pubitemid 26143469)
72. Chiang SM, Schellhorn HE (2012) Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch Biochem Biophys 525: 161-169.
73. Clauditz A, Resch A, Wieland KP, Peschel A, Gotz F (2006) Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect Immun 74: 4950-4953. (Pubitemid 44157287)
74. Kelman D, Ben-Amotz A, Berman-Frank I (2009) Carotenoids provide the major antioxidant defence in the globally significant N2-fixing marine cyanobacterium Trichodesmium. Environ Microbiol 11: 1897-1908.
75. Xu J, Johnson RC (1997) Activation of RpoS-dependent proP P2 transcription by the Fis protein in vitro. J Mol Biol 270: 346-359. (Pubitemid 27326675)
76. Xu J, Johnson RC (1997) Cyclic AMP receptor protein functions as a repressor of the osmotically inducible promoter proP P1 in Escherichia coli. J Bacteriol 179: 2410-2417. (Pubitemid 27146898)
77. Bjursell MK, Martens EC, Gordon JI (2006) Functional genomic and metabolic studies of the adaptations of a prominent adult human gut symbiont, Bacteroides thetaiotaomicron, to the suckling period. J Biol Chem 281: 36269-36279. (Pubitemid 46041362)
78. Kim SH, Ahn YO, Ahn MJ, Lee HS, Kwak SS (2012) Down-regulation of β-carotene hydroxylase increases β-carotene and total carotenoids enhancing salt stress tolerance in transgenic cultured cells of sweetpotato. Phytochemistry 74: 69-78.
79. Mathews-Roth MM (1987) Photoprotection by carotenoids. Fed Proc 46: 1890-1893.
80. Mishra NN, Liu GY, Yeaman MR, Nast CC, Proctor RA, et al. (2011) Carotenoid-related alteration of cell membrane fluidity impacts Staphylococcus aureus susceptibility to host defense peptides. Antimicrob Agents Chemother 55: 526-531.
81. Phongsisay V, Perera VN, Fry BN (2007) Expression of the htrB gene is essential for responsiveness of Salmonella typhimurium and Campylobacter jejuni to harsh environments. Microbiology 153: 254-262. (Pubitemid 46111840)
82. Reva ON, Weinel C, Weinel M, Bohm K, Stjepandic D, et al. (2006) Functional genomics of stress response in Pseudomonas putida KT2440. J Bacteriol 188: 4079-4092. (Pubitemid 43825411)