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Chapter 29 : Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level

Authors: Shoshy Altuvia1, Gisela Storz2, Kai Papenfort3
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Affiliations: 1: Department of Microbiology and Molecular Genetics, IMRIC, The Hebrew University-Hadassah Medical School, Jerusalem, Israel; 2: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892; 3: Faculty of Biology, Department of Microbiology, Ludwig-Maximilians-University of Munich, 82152 Martinsried, Germany
Content Type: Monograph
Publication Year: 2019

Category: Microbial Genetics and Molecular Biology

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Abstract:

The impact that the study of phages, both in their lytic form and as prophages integrated into bacterial chromosomes, has had on molecular biology and microbiology is hard to overstate. The ease of phage manipulation helped establish several of the central dogmas in molecular biology. For example, characterization of various phage DNA polymerases contributed to the understanding of replication ( ), and models of transcription regulation were greatly influenced by studies of I, the phage λ repressor ( ). Phages also have continually provided important tools such as transduction, the phage-assisted movement of DNA from one bacterium to another, which has been an essential tool since the early years of molecular biology ( ). As another example, the development of chain termination DNA-sequencing approaches benefited from single-stranded DNA cloning vectors derived from phage M13 ( ).

Citation: Altuvia S, Storz G, Papenfort K. 2019. Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level, p 501-514. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0027-2018
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Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level
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Citation: Altuvia S, Storz G, Papenfort K. 2019. Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level, p 501-514. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0027-2018
/content/10.1128/9781683670247.chap29.fig29-1
Figure 1
Repression of both prophage- and bacterial-encoded mRNAs by sRNAs encoded by horizontally acquired elements and the bacterial core genome. (A) Following host-cell invasion, the prophage-encoded sRNA PinT (purple) is activated by the core genome-encoded transcription factor PhoP (blue). PinT is an Hfq-binding sRNA that regulates multiple target genes through direct base-pairing. These include the mRNAs of the two horizontally acquired effector proteins, SopE and SopE2, as well as the core genome-encoded mRNA. The Crp protein acts as an activator of SPI-2 (intracellular) virulence genes of . (B) The core genome-encoded (blue) OxyS sRNA is activated by the OxyR transcription factor under conditions of oxidative stress. OxyS associates with Hfq to regulate at least two targets: the mRNA encoding the FhlA transcription regulator of formate metabolism and the transcript encoding NusG, an important transcription termination factor. OxyS repression of NusG, which normally blocks expression of the prophage-encoded (purple) KilR protein together with the Rho termination factor, results in increased production of KilR, which transiently inhibits cell division.
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10.1128/9781683670247/fig29-1.gif
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Figure 1

Repression of both prophage- and bacterial-encoded mRNAs by sRNAs encoded by horizontally acquired elements and the bacterial core genome. (A) Following host-cell invasion, the prophage-encoded sRNA PinT (purple) is activated by the core genome-encoded transcription factor PhoP (blue). PinT is an Hfq-binding sRNA that regulates multiple target genes through direct base-pairing. These include the mRNAs of the two horizontally acquired effector proteins, SopE and SopE2, as well as the core genome-encoded mRNA. The Crp protein acts as an activator of SPI-2 (intracellular) virulence genes of . (B) The core genome-encoded (blue) OxyS sRNA is activated by the OxyR transcription factor under conditions of oxidative stress. OxyS associates with Hfq to regulate at least two targets: the mRNA encoding the FhlA transcription regulator of formate metabolism and the transcript encoding NusG, an important transcription termination factor. OxyS repression of NusG, which normally blocks expression of the prophage-encoded (purple) KilR protein together with the Rho termination factor, results in increased production of KilR, which transiently inhibits cell division.

Citation: Altuvia S, Storz G, Papenfort K. 2019. Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level, p 501-514. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0027-2018
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Figure 2
Prophage-encoded sRNAs that regulate the expression of host genes. (A) The prophage-encoded (purple) sRNA DicF is processed from a polycistronic transcript by RNase E, and, for the second DicF isoform, by RNase III. DicF associates with Hfq to repress synthesis of the core genome-encoded (blue) FtsZ protein, required for cell division, as well as XylR, PykA, and ManX, all involved in carbon metabolism. (B) Esr41 is a prophage-encoded (purple) sRNA that binds Hfq to inhibit translation of the core genome-encoded (blue) , , and mRNAs. The gene products of the mRNAs are involved in iron metabolism, and repression of results in colicin resistance. Esr41 also leads to increased motility by upregulation of FliC; however, the molecular mechanism underlying this process has not yet been determined.
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Figure 2

Prophage-encoded sRNAs that regulate the expression of host genes. (A) The prophage-encoded (purple) sRNA DicF is processed from a polycistronic transcript by RNase E, and, for the second DicF isoform, by RNase III. DicF associates with Hfq to repress synthesis of the core genome-encoded (blue) FtsZ protein, required for cell division, as well as XylR, PykA, and ManX, all involved in carbon metabolism. (B) Esr41 is a prophage-encoded (purple) sRNA that binds Hfq to inhibit translation of the core genome-encoded (blue) , , and mRNAs. The gene products of the mRNAs are involved in iron metabolism, and repression of results in colicin resistance. Esr41 also leads to increased motility by upregulation of FliC; however, the molecular mechanism underlying this process has not yet been determined.

Citation: Altuvia S, Storz G, Papenfort K. 2019. Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level, p 501-514. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0027-2018
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Figure 3
Prophage-encoded and core genome-encoded sRNAs that act as sponges to block the activities of core-encoded sRNAs. The prophage-encoded (purple) AgvB sRNA, as well as the core genome-encoded sRNA (blue) SroC use Hfq to base-pair with the GcvB sRNA to inhibit the function of the GcvB global regulator of amino acid uptake and metabolism. SroC is generated from RNase E-mediated endonucleolytic processing of a polycistronic transcript, while AgvB is transcribed from a freestanding gene.
10.1128/9781683670247/fig29-3_thmb.gif
10.1128/9781683670247/fig29-3.gif
Image of Figure 3
Figure 3

Prophage-encoded and core genome-encoded sRNAs that act as sponges to block the activities of core-encoded sRNAs. The prophage-encoded (purple) AgvB sRNA, as well as the core genome-encoded sRNA (blue) SroC use Hfq to base-pair with the GcvB sRNA to inhibit the function of the GcvB global regulator of amino acid uptake and metabolism. SroC is generated from RNase E-mediated endonucleolytic processing of a polycistronic transcript, while AgvB is transcribed from a freestanding gene.

Citation: Altuvia S, Storz G, Papenfort K. 2019. Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level, p 501-514. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0027-2018
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Tables

Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level
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Citation: Altuvia S, Storz G, Papenfort K. 2019. Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level, p 501-514. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0027-2018
/content/10.1128/9781683670247.chap29.tab29-1
Table 1
Examples of posttranscriptional cross-regulation between bacteria and phages
Generic image for table
Table 1

Examples of posttranscriptional cross-regulation between bacteria and phages

Citation: Altuvia S, Storz G, Papenfort K. 2019. Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level, p 501-514. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0027-2018

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