1887

Chapter 9 : Genes within Genes in Bacterial Genomes

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Genes within Genes in Bacterial Genomes, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781683670247/9781683670230_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781683670247/9781683670230_Chap09-2.gif

Abstract:

The most common result of the translation of a gene is the production of a single protein product ( Fig. 1a ). However, the redundancy of the genetic code and the plasticity of the mRNA structure allow for expansions of the proteome by unorthodox interpreting of genetic information. A familiar strategy leading to unusual interpretation of genetic information is collectively known as recoding and has been discussed in several excellent reviews ( ). The most conventional recoding involves programmed ribosomal frameshifting and can generate two gene products that are identical in their N-terminal segments but differ in the sequences of their C termini ( Fig. 1b ).

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Different strategies for encoding more than one protein in one gene. (a) The conventional one gene-one protein scenario. (b) Programmed ribosomal frameshifting results in translation of two proteins whose N-terminal sequences are the same but differ in their C-terminal segments. The alternative protein could be shorter or longer than the primary one depending on the position of the OOF stop codon. (c) Presence of an internal in-frame start codon within the ORF results in production of a truncated protein devoid of the N-terminal segment of the full-size translation product. If the internal start codon is OOF relative to the main ORF, the sequence of the alternative polypeptide is completely different from that of the protein encoded in the main ORF.

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Internal initiation alters protein localization. Full-size Mip-23.5 protein carries a signal sequence (SS) at its N terminus, which predisposes it to be secreted. The products of internal initiation, Mip-15.5 and Mip-15.0, lack the signal sequence and, as a result, remain in the cytoplasm.

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Alternative translation initiation accounts for production of two antibiotics by the same biochemical pathway. Production of the full-size PikAIV polyketide synthase module supports synthesis of the 14-atom macrolactone ring of pikromycin. The N-terminally truncated PikAIV variant leads to the synthesis of the smaller (12-atom) macrolactone ring of methymycin.

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Alternative protein restores stoichiometry of the functional restriction enzyme. Full-size McrB binds DNA and associates with the nucleolytic McrC to cleave DNA. McrB lacks the N-terminal DNA-binding domain (dark blue) but is able to titrate out the excess McrC to maintain optimal activity of the restriction enzyme complex. The general scheme of the figure was adapted from reference .

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

The isoforms of CcmM help to differentially organize RubisCO in β-carboxysome. The N-terminal segment of the full-size CcmM-58 (dark blue) anchors it to the inner shell of the β-carboxysome, while its C-terminal segment (light blue) arranges the first layer of RubisCO. The N-terminally truncated Ccm-35 organizes RubisCO into a lattice in the lumen of the β-carboxysome.

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

The alternative LysC isoform expands the amino acid-mediated regulation of the enzyme. The full-size (α) and N-terminally truncated (β) isoforms of LysC associate into a functional αβ tetramer, in which the binding sites for the regulatory amino acids lysine (orange) and threonine (red) are formed at the interface of the α-β subunits. Shown is the structure of LysC (PDB ID: 3AAW) ( ).

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 7
Figure 7

Elimination of the stop codon creates a fused gene with two translation starts. Two genes, and , which encode functionally distinct proteins and associate to form a functional complex, are organized in an operon in . Due to the elimination of the stop codon in , the two ORFs are fused into a single gene and can be expressed from the primary and the internal TIS.

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 8
Figure 8

The use of different promoters can regulate the utilization of alternative start sites within a gene. Two promoters (P1 and P2) precede the gene in 6803. The transcript initiated at P2 has a short 5′ UTR; the accessible pTIS favors translation of the full-size FNR. Folding of the long 5′ UTR of the transcripts initiated at the P1 promoter occludes the pTIS, thereby shifting the relative expression of the FNR isoforms in favor of the shorter FNR. While photosynthetic growth favors synthesis of FNR, heterotrophic conditions stimulate production of the FNR isoform.

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 9
Figure 9

Elimination of a start codon leads to gene occlusion. In , the neighboring genes of ribosomal protein L34 () and RNase P protein () are independently translated. In , the mutation of the translation initiation codon and appearance of an additional start site upstream of lead to occlusion of within the gene, but in an alternative reading frame. Start sites of both genes utilize the same SD sequence (blue), whose optimal spacing with the start codon shifts the balance of translation in favor of the ribosomal protein.

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 10
Figure 10

Retapamulin-assisted ribosome profiling illuminates sites of internal translation initiation. (a) (Left) Ribosome profiling in untreated cells shows the distribution of translating ribosomes along the mRNAs ( ). (Right) Brief pretreatment of cells with the translation initiation inhibitor retapamulin arrests the ribosomes at the translation start site of the ORFs. (b) Examples of primary and internal TISs revealed by retapamulin-assisted ribosome profiling in genes known to contain functional internal start codons. Note that the presence of the iTISs is difficult to detect when ribosome profiling is performed in untreated cells.

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781683670247.chap9
1. Atkins JF,, Loughran G,, Bhatt PR,, Firth AE,, Baranov PV . 2016. Ribosomal frameshifting and transcriptional slippage: from genetic steganography and cryptography to adventitious use. Nucleic Acids Res 44 : 7007 7078.
2. Baranov PV,, Atkins JF,, Yordanova MM . 2015. Augmented genetic decoding: global, local and temporal alterations of decoding processes and codon meaning. Nat Rev Genet 16 : 517 529.[CrossRef]
3. Caliskan N,, Peske F,, Rodnina MV . 2015. Changed in translation: mRNA recoding by -1 programmed ribosomal frameshifting. Trends Biochem Sci 40 : 265 274.[CrossRef]
4. Dinman JD . 2012. Mechanisms and implications of programmed translational frameshifting. Wiley Interdiscip Rev RNA 3 : 661 673.[CrossRef]
5. Miller ES,, Kutter E,, Mosig G,, Arisaka F,, Kunisawa T,, Rüger W . 2003. Bacteriophage T4 genome. Microbiol Mol Biol Rev 67 : 86 156.[CrossRef][PubMed]
6. Doore SM,, Baird CD,, 2012 University of Arizona Virology Undergraduate Lab, Roznowski AP,, Fane BA . 2014. The evolution of genes within genes and the control of DNA replication in microviruses. Mol Biol Evol 31 : 1421 1431.[CrossRef]
7. Shcherbakov DV,, Garber MB . 2000. Overlapping genes in bacterial and bacteriophage genomes. Mol Biol (Mosk) 34 : 572 583. (In Russian.)
8. Gualerzi CO,, Pon CL . 2015. Initiation of mRNA translation in bacteria: structural and dynamic aspects. Cell Mol Life Sci 72 : 4341 4367.[CrossRef][PubMed]
9. Kozak M . 2005. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361 : 13 37.[CrossRef][PubMed]
10. Laursen BS,, Sørensen HP,, Mortensen KK,, Sperling-Petersen HU . 2005. Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69 : 101 123.[CrossRef][PubMed]
11. Vellanoweth RL,, Rabinowitz JC . 1992. The influence of ribosome-binding-site elements on translational efficiency in Bacillus subtilis and Escherichia coli in vivo. Mol Microbiol 6 : 1105 1114.[CrossRef]
12. Shine J,, Dalgarno L . 1975. Determinant of cistron specificity in bacterial ribosomes. Nature 254 : 34 38.[CrossRef][PubMed]
13. Accetto T,, Avguštin G . 2011. Inability of Prevotella bryantii to form a functional Shine-Dalgarno interaction reflects unique evolution of ribosome binding sites in Bacteroidetes. PLoS One 6 : e22914.[CrossRef]
14. Moll I,, Grill S,, Gualerzi CO,, Bläsi U . 2002. Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol 43 : 239 246.[CrossRef]
15. Salis HM . 2011. The ribosome binding site calculator. Methods Enzymol 498 : 19 42.[CrossRef]
16. Valverde C,, Haas D . 2008. Small RNAs controlled by two-component systems. Adv Exp Med Biol 631 : 54 79.[CrossRef]
17. Whitaker WR,, Lee H,, Arkin AP,, Dueber JE . 2015. Avoidance of truncated proteins from unintended ribosome binding sites within heterologous protein coding sequences. ACS Synth Biol 4 : 249 257.[CrossRef][PubMed]
18. Miller MJ,, Wahba AJ . 1973. Chain initiation factor 2. Purification and properties of two species from Escherichia coli MRE 600. J Biol Chem 248 : 1084 1090.[PubMed]
19. Sacerdot C,, Dessen P,, Hershey JW,, Plumbridge JA,, Grunberg-Manago M . 1984. Sequence of the initiation factor IF2 gene: unusual protein features and homologies with elongation factors. Proc Natl Acad Sci U S A 81 : 7787 7791.[CrossRef]
20. Plumbridge JA,, Deville F,, Sacerdot C,, Petersen HU,, Cenatiempo Y,, Cozzone A,, Grunberg-Manago M,, Hershey JW . 1985. Two translational initiation sites in the infB gene are used to express initiation factor IF2α and IF2β in Escherichia coli. EMBO J 4 : 223 229.[PubMed]
21. Nyengaard NR,, Mortensen KK,, Lassen SF,, Hershey JW,, Sperling-Petersen HU . 1991. Tandem translation of E. coli initiation factor IF2β: purification and characterization in vitro of two active forms. Biochem Biophys Res Commun 181 : 1572 1579.[CrossRef]
22. Sacerdot C,, Vachon G,, Laalami S,, Morel-Deville F,, Cenatiempo Y,, Grunberg-Manago M . 1992. Both forms of translational initiation factor IF2 (α and β) are required for maximal growth of Escherichia coli: evidence for two translational initiation codons for IF2β. J Mol Biol 225 : 67 80.[CrossRef]
23. Laursen BS,, de A Steffensen SA,, Hedegaard J,, Moreno JM,, Mortensen KK,, Sperling-Petersen HU . 2002. Structural requirements of the mRNA for intracistronic translation initiation of the enterobacterial infB gene. Genes Cells 7 : 901 910.[CrossRef]
24. Shazand K,, Tucker J,, Chiang R,, Stansmore K,, Sperling-Petersen HU,, Grunberg-Manago M,, Rabinowitz JC,, Leighton T . 1990. Isolation and molecular genetic characterization of the Bacillus subtilis gene ( infB) encoding protein synthesis initiation factor 2. J Bacteriol 172 : 2675 2687.[CrossRef]
25. Caserta E,, Tomsic J,, Spurio R,, La Teana A,, Pon CL,, Gualerzi CO . 2006. Translation initiation factor IF2 interacts with the 30 S ribosomal subunit via two separate binding sites. J Mol Biol 362 : 787 799.[CrossRef]
26. Giuliodori AM,, Brandi A,, Gualerzi CO,, Pon CL . 2004. Preferential translation of cold-shock mRNAs during cold adaptation. RNA 10 : 265 276.[CrossRef][PubMed]
27. Madison KE,, Abdelmeguid MR,, Jones-Foster EN,, Nakai H . 2012. A new role for translation initiation factor 2 in maintaining genome integrity. PLoS Genet 8 : e1002648.[CrossRef]
28. Madison KE,, Jones-Foster EN,, Vogt A,, Kirtland Turner S,, North SH,, Nakai H . 2014. Stringent response processes suppress DNA damage sensitivity caused by deficiency in full-length translation initiation factor 2 or PriA helicase. Mol Microbiol 92 : 28 46.[CrossRef]
29. North SH,, Kirtland SE,, Nakai H . 2007. Translation factor IF2 at the interface of transposition and replication by the PriA-PriC pathway. Mol Microbiol 66 : 1566 1578.
30. Li GW,, Burkhardt D,, Gross C,, Weissman JS . 2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157 : 624 635.[CrossRef]
31. Hénaut A,, Lisacek F,, Nitschké P,, Moszer I,, Danchin A . 1998. Global analysis of genomic texts: the distribution of AGCT tetranucleotides in the Escherichia coli and Bacillus subtilis genomes predicts translational frameshifting and ribosomal hopping in several genes. Electrophoresis 19 : 515 527.[CrossRef]
32. Atlung T,, Nielsen HV,, Hansen FG . 2002. Characterisation of the allelic variation in the rpoS gene in thirteen K12 and six other non-pathogenic Escherichia coli strains. Mol Genet Genomics 266 : 873 881.[CrossRef][PubMed]
33. Subbarayan PR,, Sarkar M . 2004. A comparative study of variation in codon 33 of the rpoS gene in Escherichia coli K12 stocks: implications for the synthesis of σ S. Mol Genet Genomics 270 : 533 538.[CrossRef][PubMed]
34. Subbarayan PR,, Sarkar M . 2004. Escherichia coli rpoS gene has an internal secondary translation initiation region. Biochem Biophys Res Commun 313 : 294 299.[CrossRef]
35. Subbarayan PR,, Sarkar M . 2004. A stop codon-dependent internal secondary translation initiation region in Escherichia coli rpoS. RNA 10 : 1359 1365.[CrossRef]
36. Kato J,, Suzuki H,, Hirota Y . 1984. Overlapping of the coding regions for alpha and gamma components of penicillin-binding protein 1 b in Escherichia coli. Mol Gen Genet 196 : 449 457.[CrossRef]
37. Nakagawa J,, Matsuhashi M . 1982. Molecular divergence of a major peptidoglycan synthetase with transglycosylase-transpeptidase activities in Escherichia coli—penicillin-binding protein 1Bs. Biochem Biophys Res Commun 105 : 1546 1553.[CrossRef]
38. Henderson TA,, Dombrosky PM,, Young KD . 1994. Artifactual processing of penicillin-binding proteins 7 and 1b by the OmpT protease of Escherichia coli. J Bacteriol 176 : 256 259.[CrossRef]
39. Broome-Smith JK,, Edelman A,, Yousif S,, Spratt BG . 1985. The nucleotide sequences of the ponA and ponB genes encoding penicillin-binding protein 1A and 1B of Escherichia coli K12. Eur J Biochem 147 : 437 446.[CrossRef]
40. Zijderveld CA,, Aarsman ME,, den Blaauwen T,, Nanninga N . 1991. Penicillin-binding protein 1B of Escherichia coli exists in dimeric forms. J Bacteriol 173 : 5740 5746.[CrossRef]
41. Ünal CM,, Steinert M . 2015. FKBPs in bacterial infections. Biochim Biophys Acta 1850 : 2096 2102.[CrossRef]
42. Mo YY,, Seshu J,, Wang D,, Mallavia LP . 1998. Synthesis in Escherichia coli of two smaller enzymically active analogues of Coxiella burnetii macrophage infectivity potentiator (CbMip) protein utilizing a single open reading frame from the cbmip gene. Biochem J 335 : 67 77.[CrossRef]
43. Seshadri R,, Paulsen IT,, Eisen JA,, Read TD,, Nelson KE,, Nelson WC,, Ward NL,, Tettelin H,, Davidsen TM,, Beanan MJ,, Deboy RT,, Daugherty SC,, Brinkac LM,, Madupu R,, Dodson RJ,, Khouri HM,, Lee KH,, Carty HA,, Scanlan D,, Heinzen RA,, Thompson HA,, Samuel JE,, Fraser CM,, Heidelberg JF . 2003. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci U S A 100 : 5455 5460.[CrossRef][PubMed]
44. Kittendorf JD,, Sherman DH . 2009. The methymycin/pikromycin pathway: a model for metabolic diversity in natural product biosynthesis. Bioorg Med Chem 17 : 2137 2146.[CrossRef]
45. Almutairi MM,, Svetlov MS,, Hansen DA,, Khabibullina NF,, Klepacki D,, Kang HY,, Sherman DH,, Vázquez-Laslop N,, Polikanov YS,, Mankin AS . 2017. Co-produced natural ketolides methymycin and pikromycin inhibit bacterial growth by preventing synthesis of a limited number of proteins. Nucleic Acids Res 45 : 9573 9582.[CrossRef]
46. Xue Y,, Sherman DH . 2000. Alternative modular polyketide synthase expression controls macrolactone structure. Nature 403 : 571 575.[CrossRef][PubMed]
47. Hori T,, Maezawa I,, Nagahama N,, Suzuki M . 1971. Isolation and structure of narbonolide, narbomycin, aglycone, from Streptomyces venezuelae and its biological transformation into picromycin via narbomycin. J Chem Soc D Chem Commun 0 : 304 305.[CrossRef]
48. Lambalot RH,, Cane DE . 1992. Isolation and characterization of 10-deoxymethynolide produced by Streptomyces venezuelae. J Antibiot (Tokyo) 45 : 1981 1982.[CrossRef]
49. Zabrocka E,, Wegrzyn K,, Konieczny I . 2014. Two replication initiators—one mechanism for replication origin opening? Plasmid 76 : 72 78.[CrossRef]
50. Shingler V,, Thomas CM . 1984. Analysis of the trfA region of broad host-range plasmid RK2 by transposon mutagenesis and identification of polypeptide products. J Mol Biol 175 : 229 249.[CrossRef]
51. Smith CA,, Thomas CM . 1984. Nucleotide sequence of the trfA gene of broad host-range plasmid RK2. J Mol Biol 175 : 251 262.[CrossRef]
52. Kittell BL,, Helinski DR . 1991. Iteron inhibition of plasmid RK2 replication in vitro: evidence for intermolecular coupling of replication origins as a mechanism for RK2 replication control. Proc Natl Acad Sci U S A 88 : 1389 1393.[CrossRef]
53. Durland RH,, Helinski DR . 1987. The sequence encoding the 43-kilodalton trfA protein is required for efficient replication or maintenance of minimal RK2 replicons in Pseudomonas aeruginosa. Plasmid 18 : 164 169.[CrossRef]
54. Konieczny I . 2003. Strategies for helicase recruitment and loading in bacteria. EMBO Rep 4 : 37 41.[CrossRef]
55. Zhong Z,, Helinski D,, Toukdarian A . 2003. A specific region in the N terminus of a replication initiation protein of plasmid RK2 is required for recruitment of Pseudomonas aeruginosa DnaB helicase to the plasmid origin. J Biol Chem 278 : 45305 45310.[CrossRef]
56. Fang FC,, Helinski DR . 1991. Broad-host-range properties of plasmid RK2: importance of overlapping genes encoding the plasmid replication initiation protein TrfA. J Bacteriol 173 : 5861 5868.[CrossRef]
57. Doyle SM,, Genest O,, Wickner S . 2013. Protein rescue from aggregates by powerful molecular chaperone machines. Nat Rev Mol Cell Biol 14 : 617 629.[CrossRef]
58. Park SK,, Kim KI,, Woo KM,, Seol JH,, Tanaka K,, Ichihara A,, Ha DB,, Chung CH . 1993. Site-directed mutagenesis of the dual translational initiation sites of the clpB gene of Escherichia coli and characterization of its gene products. J Biol Chem 268 : 20170 20174.[PubMed]
59. Squires CL,, Pedersen S,, Ross BM,, Squires C . 1991. ClpB is the Escherichia coli heat shock protein F84.1. J Bacteriol 173 : 4254 4262.[CrossRef]
60. Beinker P,, Schlee S,, Groemping Y,, Seidel R,, Reinstein J . 2002. The N terminus of ClpB from Thermus thermophilus is not essential for the chaperone activity. J Biol Chem 277 : 47160 47166.[CrossRef][PubMed]
61. Impens F,, Rolhion N,, Radoshevich L,, Bécavin C,, Duval M,, Mellin J,, García Del Portillo F,, Pucciarelli MG,, Williams AH,, Cossart P . 2017. N-terminomics identifies Prli42 as a membrane miniprotein conserved in Firmicutes and critical for stressosome activation in Listeria monocytogenes. Nat Microbiol 2 : 17005.[CrossRef]
62. Chow IT,, Baneyx F . 2005. Coordinated synthesis of the two ClpB isoforms improves the ability of Escherichia coli to survive thermal stress. FEBS Lett 579 : 4235 4241.[CrossRef]
63. Eriksson MJ,, Clarke AK . 1996. The heat shock protein ClpB mediates the development of thermotolerance in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 178 : 4839 4846.[CrossRef]
64. Nagy M,, Guenther I,, Akoyev V,, Barnett ME,, Zavodszky MI,, Kedzierska-Mieszkowska S,, Zolkiewski M . 2010. Synergistic cooperation between two ClpB isoforms in aggregate reactivation. J Mol Biol 396 : 697 707.[CrossRef]
65. Clarke AK,, Eriksson MJ . 2000. The truncated form of the bacterial heat shock protein ClpB/HSP100 contributes to development of thermotolerance in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 182 : 7092 7096.[CrossRef]
66. Seol JH,, Yoo SJ,, Kim KI,, Kang MS,, Ha DB,, Chung CH . 1994. The 65-kDa protein derived from the internal translational initiation site of the clpA gene inhibits the ATP-dependent protease Ti in Escherichia coli. J Biol Chem 269 : 29468 29473.[PubMed]
67. Seol JH,, Yoo SJ,, Kang MS,, Ha DB,, Chung CH . 1995. The 65-kDa protein derived from the internal translational start site of the clpA gene blocks autodegradation of ClpA by the ATP-dependent protease Ti in Escherichia coli. FEBS Lett 377 : 41 43.[CrossRef]
68. Loh E,, Righetti F,, Eichner H,, Twittenhoff C,, Narberhaus F . 2018. RNA thermometers in bacterial pathogens. Microbiol Spectr 6 : RWR-0012-2017.[CrossRef]
69. Gilson L,, Mahanty HK,, Kolter R . 1987. Four plasmid genes are required for colicin V synthesis, export, and immunity. J Bacteriol 169 : 2466 2470.[CrossRef][PubMed]
70. Hwang J,, Manuvakhova M,, Tai PC . 1997. Characterization of in-frame proteins encoded by cvaA, an essential gene in the colicin V secretion system: CvaA* stabilizes CvaA to enhance secretion. J Bacteriol 179 : 689 696.[CrossRef]
71. Varcamonti M,, Nicastro G,, Venema G,, Kok J . 2001. Proteins of the lactococcin A secretion system: lcnD encodes two in-frame proteins. FEMS Microbiol Lett 204 : 259 263.[CrossRef][PubMed]
72. Loenen WA,, Raleigh EA . 2014. The other face of restriction: modification-dependent enzymes. Nucleic Acids Res 42 : 56 69.[CrossRef][PubMed]
73. Pieper U,, Groll DH,, Wünsch S,, Gast FU,, Speck C,, Mücke N,, Pingoud A . 2002. The GTP-dependent restriction enzyme McrBC from Escherichia coli forms high-molecular mass complexes with DNA and produces a cleavage pattern with a characteristic 10-base pair repeat. Biochemistry 41 : 5245 5254.[CrossRef]
74. Ross TK,, Achberger EC,, Braymer HD . 1989. Nucleotide sequence of the McrB region of Escherichia coli K-12 and evidence for two independent translational initiation sites at the mcrB locus. J Bacteriol 171 : 1974 1981.[CrossRef]
75. Beary TP,, Braymer HD,, Achberger EC . 1997. Evidence of participation of McrB S in McrBC restriction in Escherichia coli K-12. J Bacteriol 179 : 7768 7775.[CrossRef][PubMed]
76. Panne D,, Raleigh EA,, Bickle TA . 1998. McrBs, a modulator peptide for McrBC activity. EMBO J 17 : 5477 5483.[CrossRef]
77. Rae BD,, Long BM,, Badger MR,, Price GD . 2013. Functions, compositions, and evolution of the two types of carboxysomes: polyhedral microcompartments that facilitate CO 2 fixation in cyanobacteria and some proteobacteria. Microbiol Mol Biol Rev 77 : 357 379.[CrossRef][PubMed]
78. Long BM,, Badger MR,, Whitney SM,, Price GD . 2007. Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA. J Biol Chem 282 : 29323 29335.[CrossRef]
79. Price GD,, Sültemeyer D,, Klughammer B,, Ludwig M,, Badger MR . 1998. The functioning of the CO 2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins, and recent advances. Can J Bot 76 : 973 1002.[CrossRef]
80. Long BM,, Tucker L,, Badger MR,, Price GD . 2010. Functional cyanobacterial β-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein. Plant Physiol 153 : 285 293.[CrossRef][PubMed]
81. Abrusci P,, McDowell MA,, Lea SM,, Johnson S . 2014. Building a secreting nanomachine: a structural overview of the T3SS. Curr Opin Struct Biol 25 : 111 117.[CrossRef][PubMed]
82. Yu XJ,, Liu M,, Matthews S,, Holden DW . 2011. Tandem translation generates a chaperone for the Salmonella type III secretion system protein SsaQ. J Biol Chem 286 : 36098 36107.[CrossRef][PubMed]
83. Bzymek KP,, Hamaoka BY,, Ghosh P . 2012. Two translation products of Yersinia yscQ assemble to form a complex essential to type III secretion. Biochemistry 51 : 1669 1677.[CrossRef][PubMed]
84. McDowell MA,, Marcoux J,, McVicker G,, Johnson S,, Fong YH,, Stevens R,, Bowman LA,, Degiacomi MT,, Yan J,, Wise A,, Friede ME,, Benesch JL,, Deane JE,, Tang CM,, Robinson CV,, Lea SM . 2016. Characterisation of Shigella Spa33 and Thermotoga FliM/N reveals a new model for C-ring assembly in T3SS. Mol Microbiol 99 : 749 766.[CrossRef][PubMed]
85. Song M,, Sukovich DJ,, Ciccarelli L,, Mayr J,, Fernandez-Rodriguez J,, Mirsky EA,, Tucker AC,, Gordon DB,, Marlovits TC,, Voigt CA . 2017. Control of type III protein secretion using a minimal genetic system. Nat Commun 8 : 14737.[CrossRef]
86. Typas A,, Sourjik V . 2015. Bacterial protein networks: properties and functions. Nat Rev Microbiol 13 : 559 572.[CrossRef][PubMed]
87. Kofoid EC,, Parkinson JS . 1991. Tandem translation starts in the cheA locus of Escherichia coli. J Bacteriol 173 : 2116 2119.[CrossRef][PubMed]
88. Smith RA,, Parkinson JS . 1980. Overlapping genes at the cheA locus of Escherichia coli. Proc Natl Acad Sci U S A 77 : 5370 5374.[CrossRef][PubMed]
89. Wolfe AJ,, Stewart RC . 1993. The short form of the CheA protein restores kinase activity and chemotactic ability to kinase-deficient mutants. Proc Natl Acad Sci U S A 90 : 1518 1522.[CrossRef]
90. Wang H,, Matsumura P . 1997. Phosphorylating and dephosphorylating protein complexes in bacterial chemotaxis. J Bacteriol 179 : 287 289.[CrossRef][PubMed]
91. Dumas R,, Cobessi D,, Robin AY,, Ferrer JL,, Curien G . 2012. The many faces of aspartate kinases. Arch Biochem Biophys 519 : 186 193.[CrossRef][PubMed]
92. Chen NY,, Paulus H . 1988. Mechanism of expression of the overlapping genes of Bacillus subtilis aspartokinase II. J Biol Chem 263 : 9526 9532.[PubMed]
93. Kalinowski J,, Cremer J,, Bachmann B,, Eggeling L,, Sahm H,, Pühler A . 1991. Genetic and biochemical analysis of the aspartokinase from Corynebacterium glutamicum. Mol Microbiol 5 : 1197 1204.[CrossRef][PubMed]
94. Lo CC,, Bonner CA,, Xie G,, D’Souza M,, Jensen RA . 2009. Cohesion group approach for evolutionary analysis of aspartokinase, an enzyme that feeds a branched network of many biochemical pathways. Microbiol Mol Biol Rev 73 : 594 651.[CrossRef]
95. Yoshida A,, Tomita T,, Kuzuyama T,, Nishiyama M . 2010. Mechanism of concerted inhibition of α 2β 2-type hetero-oligomeric aspartate kinase from Corynebacterium glutamicum. J Biol Chem 285 : 27477 27486.[CrossRef][PubMed]
96. Bondaryk RP,, Paulus H . 1985. Expression of the gene for Bacillus subtilis aspartokinase II in Escherichia coli. J Biol Chem 260 : 592 597.[PubMed]
97. Lin TH,, Hu YN,, Shaw GC . 2014. Two enzymes, TilS and HprT, can form a complex to function as a transcriptional activator for the cell division protease gene ftsH in Bacillus subtilis. J Biochem 155 : 5 16.[CrossRef][PubMed]
98. Kharel MK,, Pahari P,, Shepherd MD,, Tibrewal N,, Nybo SE,, Shaaban KA,, Rohr J . 2012. Angucyclines: biosynthesis, mode-of-action, new natural products, and synthesis. Nat Prod Rep 29 : 264 325.[CrossRef][PubMed]
99. Kallio P,, Liu Z,, Mäntsälä P,, Niemi J,, Metsä-Ketelä M . 2008. A nested gene in Streptomyces bacteria encodes a protein involved in quaternary complex formation. J Mol Biol 375 : 1212 1221.[CrossRef]
100. Thomas CM,, Smith CA . 1986. The trfB region of broad host range plasmid RK2: the nucleotide sequence reveals incC and key regulatory gene trfB/korA/korD as overlapping genes. Nucleic Acids Res 14 : 4453 4469.[CrossRef]
101. Batt SM,, Bingle LE,, Dafforn TR,, Thomas CM . 2009. Bacterial genome partitioning: N-terminal domain of IncC protein encoded by broad-host-range plasmid RK2 modulates oligomerisation and DNA binding. J Mol Biol 385 : 1361 1374.[CrossRef]
102. Bowsher CG,, Dunbar B,, Emes MJ . 1993. The purification and properties of ferredoxin-NADP +-oxidoreductase from roots of P isum sativum L. Protein Expr Purif 4 : 512 518.[PubMed][CrossRef]
103. Neuhaus HE,, Emes MJ . 2000. Nonphotosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 51 : 111 140.[CrossRef][PubMed]
104. Omairi-Nasser A,, de Gracia AG,, Ajlani G . 2011. A larger transcript is required for the synthesis of the smaller isoform of ferredoxin:NADP oxidoreductase. Mol Microbiol 81 : 1178 1189.[CrossRef][PubMed]
105. Thomas JC,, Ughy B,, Lagoutte B,, Ajlani G . 2006. A second isoform of the ferredoxin:NADP oxidoreductase generated by an in-frame initiation of translation. Proc Natl Acad Sci U S A 103 : 18368 18373.[CrossRef][PubMed]
106. Omairi-Nasser A,, Galmozzi CV,, Latifi A,, Muro-Pastor MI,, Ajlani G . 2014. NtcA is responsible for accumulation of the small isoform of ferredoxin:NADP oxidoreductase. Microbiology 160 : 789 794.[CrossRef][PubMed]
107. Malakooti J,, Ely B,, Matsumura P . 1994. Molecular characterization, nucleotide sequence, and expression of the fliO, fliP, fliQ, and fliR genes of Escherichia coli. J Bacteriol 176 : 189 197.[CrossRef]
108. Schoenhals GJ,, Kihara M,, Macnab RM . 1998. Translation of the flagellar gene fliO of Salmonella typhimurium from putative tandem starts. J Bacteriol 180 : 2936 2942.[PubMed]
109. Yamagata H,, Adachi T,, Tsuboi A,, Takao M,, Sasaki T,, Tsukagoshi N,, Udaka S . 1987. Cloning and characterization of the 5′ region of the cell wall protein gene operon in Bacillus brevis 47. J Bacteriol 169 : 1239 1245.[CrossRef][PubMed]
110. Ebisu S,, Tsuboi A,, Takagi H,, Naruse Y,, Yamagata H,, Tsukagoshi N,, Udaka S . 1990. Conserved structures of cell wall protein genes among protein-producing Bacillus brevis strains. J Bacteriol 172 : 1312 1320.[CrossRef]
111. Adachi T,, Yamagata H,, Tsukagoshi N,, Udaka S . 1990. Use of both translation initiation sites of the middle wall protein gene in Bacillus brevis 47. J Bacteriol 172 : 511 513.[CrossRef][PubMed]
112. Ozin AJ,, Costa T,, Henriques AO,, Moran CP Jr . 2001. Alternative translation initiation produces a short form of a spore coat protein in Bacillus subtilis. J Bacteriol 183 : 2032 2040.[CrossRef]
113. Thomas S,, Holland IB,, Schmitt L . 2014. The type 1 secretion pathway—the hemolysin system and beyond. Biochim Biophys Acta 1843 : 1629 1641.[CrossRef][PubMed]
114. Felmlee T,, Pellett S,, Welch RA . 1985. Nucleotide sequence of an Escherichia coli chromosomal hemolysin. J Bacteriol 163 : 94 105.[PubMed]
115. Mackman N,, Nicaud JM,, Gray L,, Holland IB . 1985. Identification of polypeptides required for the export of haemolysin 2001 from E. coli. Mol Gen Genet 201 : 529 536.[CrossRef][PubMed]
116. Blight MA,, Menichi B,, Holland IB . 1995. Evidence for post-transcriptional regulation of the synthesis of the Escherichia coli HlyB haemolysin translocator and production of polyclonal anti-HlyB antibody. Mol Gen Genet 247 : 73 85.[CrossRef]
117. Flores-Díaz M,, Monturiol-Gross L,, Naylor C,, Alape-Girón A,, Flieger A . 2016. Bacterial sphingomyelinases and phospholipases as virulence factors. Microbiol Mol Biol Rev 80 : 597 628.[CrossRef]
118. Cota-Gomez A,, Vasil AI,, Kadurugamuwa J,, Beveridge TJ,, Schweizer HP,, Vasil ML . 1997. PlcR1 and PlcR2 are putative calcium-binding proteins required for secretion of the hemolytic phospholipase C of Pseudomonas aeruginosa. Infect Immun 65 : 2904 2913.[PubMed]
119. Shen BF,, Tai PC,, Pritchard AE,, Vasil ML . 1987. Nucleotide sequences and expression in Escherichia coli of the in-phase overlapping Pseudomonas aeruginosa plcR genes. J Bacteriol 169 : 4602 4607.[CrossRef]
120. Buskirk AR,, Green R . 2017. Ribosome pausing, arrest and rescue in bacteria and eukaryotes. Philos Trans R Soc Lond B Biol Sci 372 : 20160183.[CrossRef]
121. Hamoen LW,, Venema G,, Kuipers OP . 2003. Controlling competence in Bacillus subtilis: shared use of regulators. Microbiology 149 : 9 17.[CrossRef][PubMed]
122. D’Souza C,, Nakano MM,, Zuber P . 1994. Identification of comS, a gene of the srfA operon that regulates the establishment of genetic competence in Bacillus subtilis. Proc Natl Acad Sci U S A 91 : 9397 9401.[CrossRef][PubMed]
123. Hamoen LW,, Eshuis H,, Jongbloed J,, Venema G,, van Sinderen D . 1995. A small gene, designated comS, located within the coding region of the fourth amino acid-activation domain of srfA, is required for competence development in Bacillus subtilis. Mol Microbiol 15 : 55 63.[CrossRef]
124. Evans D,, Marquez SM,, Pace NR . 2006. RNase P: interface of the RNA and protein worlds. Trends Biochem Sci 31 : 333 341.[CrossRef][PubMed]
125. Ogasawara N,, Yoshikawa H . 1992. Genes and their organization in the replication origin region of the bacterial chromosome. Mol Microbiol 6 : 629 634.[CrossRef]
126. Feltens R,, Gossringer M,, Willkomm DK,, Urlaub H,, Hartmann RK . 2003. An unusual mechanism of bacterial gene expression revealed for the RNase P protein of Thermus strains. Proc Natl Acad Sci U S A 100 : 5724 5729.[CrossRef]
127. Osterman IA,, Evfratov SA,, Sergiev PV,, Dontsova OA . 2013. Comparison of mRNA features affecting translation initiation and reinitiation. Nucleic Acids Res 41 : 474 486.[CrossRef]
128. Yuan P,, D’Lima NG,, Slavoff SA . 2018. Comparative membrane proteomics reveals a nonannotated E. coli heat shock protein. Biochemistry 57 : 56 60.[CrossRef]
129. Chang JT,, Green CB,, Wolf RE Jr . 1995. Inhibition of translation initiation on Escherichia coli gnd mRNA by formation of a long-range secondary structure involving the ribosome binding site and the internal complementary sequence. J Bacteriol 177 : 6560 6567.[CrossRef]
130. Berry IJ,, Steele JR,, Padula MP,, Djordjevic SP . 2016. The application of terminomics for the identification of protein start sites and proteoforms in bacteria. Proteomics 16 : 257 272.[PubMed][CrossRef]
131. Bienvenut WV,, Giglione C,, Meinnel T . 2015. Proteome-wide analysis of the amino terminal status of Escherichia coli proteins at the steady-state and upon deformylation inhibition. Proteomics 15 : 2503 2518.[CrossRef]
132. Ingolia NT,, Ghaemmaghami S,, Newman JR,, Weissman JS . 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324 : 218 223.[CrossRef]
133. Schrader JM,, Zhou B,, Li GW,, Lasker K,, Childers WS,, Williams B,, Long T,, Crosson S,, McAdams HH,, Weissman JS,, Shapiro L . 2014. The coding and noncoding architecture of the Caulobacter crescentus genome. PLoS Genet 10 : e1004463.[CrossRef]
134. Fritsch C,, Herrmann A,, Nothnagel M,, Szafranski K,, Huse K,, Schumann F,, Schreiber S,, Platzer M,, Krawczak M,, Hampe J,, Brosch M . 2012. Genome-wide search for novel human uORFs and N-terminal protein extensions using ribosomal footprinting. Genome Res 22 : 2208 2218.[CrossRef]
135. Ingolia NT,, Lareau LF,, Weissman JS . 2011. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147 : 789 802.[CrossRef][PubMed]
136. Lee S,, Liu B,, Lee S,, Huang SX,, Shen B,, Qian SB . 2012. Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution. Proc Natl Acad Sci U S A 109 : E2424 E2432.[CrossRef]
137. Nakahigashi K,, Takai Y,, Kimura M,, Abe N,, Nakayashiki T,, Shiwa Y,, Yoshikawa H,, Wanner BL,, Ishihama Y,, Mori H . 2016. Comprehensive identification of translation start sites by tetracycline-inhibited ribosome profiling. DNA Res 23 : 193 201.[CrossRef]
138. Davidovich C,, Bashan A,, Auerbach-Nevo T,, Yaggie RD,, Gontarek RR,, Yonath A . 2007. Induced-fit tightens pleuromutilins binding to ribosomes and remote interactions enable their selectivity. Proc Natl Acad Sci U S A 104 : 4291 4296.[CrossRef]
139. Yan K,, Madden L,, Choudhry AE,, Voigt CS,, Copeland RA,, Gontarek RR . 2006. Biochemical characterization of the interactions of the novel pleuromutilin derivative retapamulin with bacterial ribosomes. Antimicrob Agents Chemother 50 : 3875 3881.[CrossRef]
140. Florin T,, Maracci C,, Graf M,, Karki P,, Klepacki D,, Berninghausen O,, Beckmann R,, Vázquez-Laslop N,, Wilson DN,, Rodnina MV,, Mankin AS . 2017. An antimicrobial peptide that inhibits translation by trapping release factors on the ribosome. Nat Struct Mol Biol 24 : 752 757.[CrossRef]
141. Thomason MK,, Bischler T,, Eisenbart SK,, Förstner KU,, Zhang A,, Herbig A,, Nieselt K,, Sharma CM,, Storz G . 2015. Global transcriptional start site mapping using differential RNA sequencing reveals novel antisense RNAs in Escherichia coli. J Bacteriol 197 : 18 28.[CrossRef][PubMed]

Tables

Generic image for table
Table 1

Bacterial genes with multiple TISs and the mRNA elements promoting translation initiation

Citation: Meydan S, Vázquez-Laslop N, Mankin A. 2019. Genes within Genes in Bacterial Genomes, p 133-154. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0020-2018

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error