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Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level

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  • Authors: Shoshy Altuvia1, Gisela Storz2, Kai Papenfort3
  • Editors: Gisela Storz4, Kai Papenfort5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    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: Munich Center for Integrated Protein Science (CIPSM) at the Department of Microbiology, Ludwig-Maximilians-University of Munich, 82152 Martinsried, Germany; 4: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 5: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0027-2018
  • Received 19 February 2018 Accepted 04 April 2018 Published 13 July 2018
  • Shoshy Altuvia, [email protected]; Gisela Storz, [email protected]; Kai Papenfort, [email protected]
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  • Abstract:

    The study of bacteriophages (phages) and prophages has provided key insights into almost every cellular process as well as led to the discovery of unexpected new mechanisms and the development of valuable tools. This is exemplified for RNA-based regulation. For instance, the characterization and exploitation of the antiphage CRISPR (clustered regularly interspaced short palindromic repeat) systems is revolutionizing molecular biology. Phage-encoded proteins such as the RNA-binding MS2 protein, which is broadly used to isolate tagged RNAs, also have been developed as valuable tools. Hfq, the RNA chaperone protein central to the function of many base-pairing small RNAs (sRNAs), was first characterized as a bacterial host factor required for Qβ phage replication. The ongoing studies of RNAs are continuing to reveal regulatory connections between infecting phages, prophages, and bacteria and to provide novel insights. There are bacterial and prophage sRNAs that regulate prophage genes, which impact bacterial virulence as well as bacterial cell killing. Conversely, phage- and prophage-encoded sRNAs modulate the expression of bacterial genes modifying metabolism. An interesting subcategory of the prophage-encoded sRNAs are sponge RNAs that inhibit the activities of bacterial-encoded sRNAs. Phages also affect posttranscriptional regulation in bacteria through proteins that inhibit or alter the activities of key bacterial proteins involved in posttranscriptional regulation. However, what is most exciting about phage and prophage research, given the millions of phage-encoded genes that have not yet been characterized, is the vast potential for discovering new RNA regulators and novel mechanisms and for gaining insight into the evolution of regulatory RNAs.

  • Citation: Altuvia S, Storz G, Papenfort K. 2018. Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level. Microbiol Spectrum 6(4):RWR-0027-2018. doi:10.1128/microbiolspec.RWR-0027-2018.

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/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0027-2018
2018-07-13
2018-09-23

Abstract:

The study of bacteriophages (phages) and prophages has provided key insights into almost every cellular process as well as led to the discovery of unexpected new mechanisms and the development of valuable tools. This is exemplified for RNA-based regulation. For instance, the characterization and exploitation of the antiphage CRISPR (clustered regularly interspaced short palindromic repeat) systems is revolutionizing molecular biology. Phage-encoded proteins such as the RNA-binding MS2 protein, which is broadly used to isolate tagged RNAs, also have been developed as valuable tools. Hfq, the RNA chaperone protein central to the function of many base-pairing small RNAs (sRNAs), was first characterized as a bacterial host factor required for Qβ phage replication. The ongoing studies of RNAs are continuing to reveal regulatory connections between infecting phages, prophages, and bacteria and to provide novel insights. There are bacterial and prophage sRNAs that regulate prophage genes, which impact bacterial virulence as well as bacterial cell killing. Conversely, phage- and prophage-encoded sRNAs modulate the expression of bacterial genes modifying metabolism. An interesting subcategory of the prophage-encoded sRNAs are sponge RNAs that inhibit the activities of bacterial-encoded sRNAs. Phages also affect posttranscriptional regulation in bacteria through proteins that inhibit or alter the activities of key bacterial proteins involved in posttranscriptional regulation. However, what is most exciting about phage and prophage research, given the millions of phage-encoded genes that have not yet been characterized, is the vast potential for discovering new RNA regulators and novel mechanisms and for gaining insight into the evolution of regulatory RNAs.

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Figures

Image of FIGURE 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.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0027-2018
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Image of FIGURE 2
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.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0027-2018
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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.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0027-2018
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Tables

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TABLE 1

Examples of posttranscriptional cross-regulation between bacteria and phages

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0027-2018

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