Nascent chain-monitored remodeling of the Sec machinery for salinity adaptation of marine bacteria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 40, 2015, Pages E5513-E5522

  Ishii, Eiji ^a   Chiba, Shinobu ^b   Hashimoto, Narimasa ^a   Kojima, Seiji ^c   Homma, Michio ^c   Ito, Koreaki ^b   Akiyama, Yoshinori ^a   Mori, Hiroyuki ^a   Randall, Linda L ^d  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO SANGYO UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

Protein export; Proton motive force; Ribosome; SecD; Translation arrest

Indexed keywords

BACTERIAL PROTEIN; HYDROGEN; POLYPEPTIDE; SEC PROTEIN; SECDF1 PROTEIN; SECDF2 PROTEIN; SODIUM ION; UNCLASSIFIED DRUG; VIBRIO EXPORT MONITORING POLYPEPTIDE; MESSENGER RNA; SEA WATER; SODIUM;

ARTICLE; BACTERIAL GENE; EVOLUTIONARY ADAPTATION; GENE DELETION; GENETIC ANALYSIS; MARINE BACTERIUM; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RIBOSOME; SALT TOLERANCE; SECDF1 GENE; SECDF2 GENE; SURVIVAL; TRANSLATION REGULATION; UPREGULATION; VIBRIO ALGINOLYTICUS; AMINO ACID SEQUENCE; CHEMISTRY; CONFORMATION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN TRANSPORT; PROTON MOTIVE FORCE; SALINITY; SEQUENCE HOMOLOGY; VIBRIO;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNOBLOTTING; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; PROTON-MOTIVE FORCE; RIBOSOMES; RNA, MESSENGER; SALINITY; SALT-TOLERANCE; SEAWATER; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM; VIBRIO;

EID: 84943302543     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1513001112     Document Type: Article

References (71)

1. Economou A, Wickner W (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78(5):835-843.
2. Van den Berg B, et al. (2004) X-ray structure of a protein-conducting channel. Nature 427(6969):36-44.
3. Nouwen N, Piwowarek M, Berrelkamp G, Driessen AJ (2005) The large first periplasmic loop of SecD and SecF plays an important role in SecDF functioning. J Bacteriol 187(16):5857-5860.
4. Pogliano KJ, Beckwith J (1994) Genetic and molecular characterization of the Escherichia coli secD operon and its products. J Bacteriol 176(3):804-814.
5. Tsukazaki T, et al. (2011) Structure and function of a membrane component SecDF that enhances protein export. Nature 474(7350):235-238.
6. Mio K, et al. (2014) Conformational variation of the translocon enhancing chaperone SecDF. J Struct Funct Genomics 15(3):107-115.
7. Reilly GD, Reilly CA, Smith EG, Baker-Austin C (2011) Vibrio alginolyticus-associated wound infection acquired in British waters, Guernsey, July 2011. Euro surveill 16(42):19994.
8. Zhang L, Orth K (2013) Virulence determinants for Vibrio parahaemolyticus infection. Curr Opin Microbiol 16(1):70-77.
9. Noguchi T, et al. (1987) Vibrio alginolyticus, a tetrodotoxin-producing bacterium, in the intestines of the fish Fugu vermicularis vermicularis. Mar Biol 94(4):625-630.
10. Zhang L, et al. (2012) Type III effector VopC mediates invasion for Vibrio species. Cell Reports 1(5):453-460.
11. Makino K, et al. (2003) Genome sequence of Vibrio parahaemolyticus: A pathogenic mechanism distinct from that of V. cholerae. Lancet 361(9359):743-749.
12. Heidelberg JF, et al. (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406(6795):477-483.
13. Kunioka E, Matsuyama S, Tokuda H (1998) Cloning and expression of the secA gene of a marine bacterium, Vibrio alginolyticus, and analysis of its function in Escherichia coli. Gene 216(2):303-309.
14. Bhattacharyya D, Das J (1997) The secY gene of V. cholerae: Identification, cloning and characterization. Gene 196(1-2):261-266.
15. Nishiyama K, Furuta M, Tokuda H (1998) Molecular cloning and functional characterization of SecE of a marine bacterium, Vibrio alginolyticus. Biochem Biophys Res Commun 251(3):894-897.
16. Tokuda H, Kim YJ, Mizushima S (1990) In vitro protein translocation into inverted membrane vesicles prepared from Vibrio alginolyticus is stimulated by the electrochemical potential of Na+ in the presence of Escherichia coli SecA. FEBS Lett 264(1):10-12.
17. Nakatogawa H, Ito K (2001) Secretion monitor, SecM, undergoes self-translation arrest in the cytosol. Mol Cell 7(1):185-192.
18. Nakatogawa H, Ito K (2002) The ribosomal exit tunnel functions as a discriminating gate. Cell 108(5):629-636.
19. Chiba S, Lamsa A, Pogliano K (2009) A ribosome-nascent chain sensor of membrane protein biogenesis in Bacillus subtilis. EMBO J 28(22):3461-3475.
20. Chiba S, Ito K (2015) MifM monitors total YidC activities of Bacillus subtilis, including that of YidC2, the target of regulation. J Bacteriol 197(1):99-107.
21. Murakami A, Nakatogawa H, Ito K (2004) Translation arrest of SecM is essential for the basal and regulated expression of SecA. Proc Natl Acad Sci USA 101(33):12330-12335.
22. Oliver DB, Beckwith J (1982) Regulation of a membrane component required for protein secretion in Escherichia coli. Cell 30(1):311-319.
23. Pogliano KJ, Beckwith J (1993) The Cs sec mutants of Escherichia coli reflect the cold sensitivity of protein export itself. Genetics 133(4):763-773.
24. Chiba S, Ito K (2012) Multisite ribosomal stalling: a unique mode of regulatory nascent chain action revealed for MifM. Mol Cell 47(6):863-872.
25. Ito K, Chiba S (2013) Arrest peptides: cis-acting modulators of translation. Annu Rev Biochem 82:171-202.
26. Muto H, Nakatogawa H, Ito K (2006) Genetically encoded but nonpolypeptide prolyltRNA functions in the A site for SecM-mediated ribosomal stall. Mol Cell 22(4): 545-552.
27. Mulkidjanian AY, Dibrov P, Galperin MY (2008) The past and present of sodium energetics: May the sodium-motive force be with you. Biochim Biophys Acta 1777(7-8): 985-992.
28. Okunishi I, Kawagishi I, Homma M (1996) Cloning and characterization of motY, a gene coding for a component of the sodium-driven flagellar motor in Vibrio alginolyticus. J Bacteriol 178(8):2409-2415.
29. Ito K, et al. (2011) Nascentome analysis uncovers futile protein synthesis in Escherichia coli. PLoS One 6(12):e28413.
30. Schoner BE, Belagaje RM, Schoner RG (1986) Translation of a synthetic two-cistron mRNA in Escherichia coli. Proc Natl Acad Sci USA 83(22):8506-8510.
31. Spanjaard RA, van Duin J (1989) Translational reinitiation in the presence and absence of a Shine and Dalgarno sequence. Nucleic Acids Res 17(14):5501-5507.
32. Pogliano JA, Beckwith J (1994) SecD and SecF facilitate protein export in Escherichia coli. EMBO J 13(3):554-561.
33. Deamer DW (1997) The first living systems: A bioenergetic perspective. Microbiol Mol Biol Rev 61(2):239-261.
34. Takekawa N, et al. (2015) Sodium-driven energy conversion for flagellar rotation of the earliest divergent hyperthermophilic bacterium. Sci Rep 5:12711.
35. Atsumi T, McCarter L, Imae Y (1992) Polar and lateral flagellar motors of marine Vibrio are driven by different ion-motive forces. Nature 355(6356):182-184.
36. McCarter L, Silverman M (1990) Surface-induced swarmer cell differentiation of Vibrio parahaemolyticus. Mol Microbiol 4(7):1057-1062.
37. Yang L, et al. (2010) The low-salt stimulon in Vibrio parahaemolyticus. Int J Food Microbiol 137(1):49-54.
38. Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211-231.
39. Xu Q, Dziejman M, Mekalanos JJ (2003) Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro. Proc Natl Acad Sci USA 100(3):1286-1291.
40. Bisharat N, Bronstein M, Korner M, Schnitzer T, Koton Y (2013) Transcriptome profiling analysis of Vibrio vulnificus during human infection. Microbiology 159(Pt 9): 1878-1887.
41. Cruz-Vera LR, Yanofsky C (2008) Conserved residues Asp16 and Pro24 of TnaCtRNAPro participate in tryptophan induction of Tna operon expression. J Bacteriol 190(14):4791-4797.
42. van der Sluis EO, Driessen AJ (2006) Stepwise evolution of the Sec machinery in Proteobacteria. Trends Microbiol 14(3):105-108.
43. Wilson DN, Beckmann R (2011) The ribosomal tunnel as a functional environment for nascent polypeptide folding and translational stalling. Curr Opin Struct Biol 21(2): 274-282.
44. Sohmen D, et al. (2015) Structure of the Bacillus subtilis 70S ribosome reveals the basis for species-specific stalling. Nat Commun 6:6941.
45. Ito K, Chiba S, Pogliano K (2010) Divergent stalling sequences sense and control cellular physiology. Biochem Biophys Res Commun 393(1):1-5.
46. Gong F, Ito K, Nakamura Y, Yanofsky C (2001) The mechanism of tryptophan induction of tryptophanase operon expression: tryptophan inhibits release factor-mediated cleavage of TnaC-peptidyl-tRNA(Pro). Proc Natl Acad Sci USA 98(16):8997-9001.
47. Ramu H, Mankin A, Vazquez-Laslop N (2009) Programmed drug-dependent ribosome stalling. Mol Microbiol 71(4):811-824.
48. Goldman DH, et al. (2015) Mechanical force releases nascent chain-mediated ribosome arrest in vitro and in vivo. Science 348(6233):457-460.
49. Shimoike T, et al. (1995) Product of a new gene, syd, functionally interacts with SecY when overproduced in Escherichia coli. J Biol Chem 270(10):5519-5526.
50. Baba T, et al. (1990) Characterization of cold-sensitive secY mutants of Escherichia coli. J Bacteriol 172(12):7005-7010.
51. Ohashi H, Shimizu Y, Ying BW, Ueda T (2007) Efficient protein selection based on ribosome display system with purified components. Biochem Biophys Res Commun 352(1):270-276.
52. Yap MN, Bernstein HD (2009) The plasticity of a translation arrest motif yields insights into nascent polypeptide recognition inside the ribosome tunnel. Mol Cell 34(2): 201-211.
53. Mori H, Akiyama Y, Ito K (2003) A SecE mutation that modulates SecY-SecE translocase assembly, identified as a specific suppressor of SecY defects. J Bacteriol 185(3): 948-956.
54. Terashima H, Koike M, Kojima S, Homma M (2010) The flagellar basal body-associated protein FlgT is essential for a novel ring structure in the sodium-driven Vibrio motor. J Bacteriol 192(21):5609-5615.
55. Miller JH (1972) Experiments in Molecular Genetics (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY).
56. Kanehara K, Ito K, Akiyama Y (2002) YaeL (EcfE) activates the sigma(E) pathway of stress response through a site-2 cleavage of anti-sigma(E), RseA. Genes Dev 16(16): 2147-2155.
57. Val ME, Skovgaard O, Ducos-Galand M, Bland MJ, Mazel D (2012) Genome engineering in Vibrio cholerae: A feasible approach to address biological issues. PLoS Genet 8(1):e1002472.
58. Kusumoto A, et al. (2006) Regulation of polar flagellar number by the flhF and flhG genes in Vibrio alginolyticus. J Biochem 139(1):113-121.
59. Zhu S, Kumar A, Kojima S, Homma M (2015) FliL associates with the stator to support torque generation of the sodium-driven polar flagellar motor of Vibrio. Mol Microbiol 23, 10.1111/mmi.13103.
60. Le Roux F, Binesse J, Saulnier D, Mazel D (2007) Construction of a Vibrio splendidus mutant lacking the metalloprotease gene vsm by use of a novel counterselectable suicide vector. Appl Environ Microbiol 73(3):777-784.
61. Aiba H (1983) Autoregulation of the Escherichia coli crp gene: CRP is a transcriptional repressor for its own gene. Cell 32(1):141-149.
62. Silhavy TJ, Berman ML, Enquist LW (1984) Experiments with Gene Fusions (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY).
63. Ito K, Akiyama Y (1991) In vivo analysis of integration of membrane proteins in Escherichia coli. Mol Microbiol 5(9):2243-2253.
64. Kihara A, Akiyama Y, Ito K (1995) FtsH is required for proteolytic elimination of uncomplexed forms of SecY, an essential protein translocase subunit. Proc Natl Acad Sci USA 92(10):4532-4536.
65. Akiyama Y, Ito K (1990) SecY protein, a membrane-embedded secretion factor of E. coli, is cleaved by the ompT protease in vitro. Biochem Biophys Res Commun 167(2): 711-715.
66. Mori H, Ito K (2006) The long alpha-helix of SecA is important for the ATPase coupling of translocation. J Biol Chem 281(47):36249-36256.
67. Nakatogawa H, Murakami A, Mori H, Ito K (2005) SecM facilitates translocase function of SecA by localizing its biosynthesis. Genes Dev 19(4):436-444.
68. Miller VL, Mekalanos JJ (1988) A novel suicide vector and its use in construction of insertion mutations: Osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170(6):2575-2583.
69. Tokuda H, Nakamura T, Unemoto T (1981) Potassium ion is required for the generation of pH-dependent membrane potential and delta pH by the marine bacterium Vibrio alginolyticus. Biochemistry 20(14):4198-4203.
70. Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177(14):4121-4130.
71. Morales VM, Bäckman A, Bagdasarian M (1991) A series of wide-host-range low-copynumber vectors that allow direct screening for recombinants. Gene 97(1):39-47.