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Chapter 7 : Diverse Cell-Cell Signaling Molecules Control Formation of Aerial Hyphae and Secondary Metabolism in Streptomycetes

Authors: Joanne M. Willey1, Justin R. Nodwell2
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Affiliations: 1: Department of Biology, Hofstra University, Hempstead, New York 11549; 2: Department of Biochemistry, Health Sciences Centre, McMaster University, Hamilton, Ontario, Canada, L8N 3Z5
Content Type: Monograph
Publication Year: 2008

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

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Abstract:

The , including the genus , constitute, on average, about 13% of soil bacterial communities, making them a dominant form of life on Earth. Research has shown that many wild isolates of spp. are capable of intercellular communication, and in one instance, the extracellular compound is a desferrioxamine siderophore. This apparent diversity of intercellular signaling mechanisms suggests that the streptomycetes rely extensively on cell-cell communication to coordinate growth with the production of secondary metabolites and sporulation. As morphological and physiological differentiation can be visually monitored, extracellular rescue of mutant phenotypes can be quite striking. However, the streptomycetes present challenges that need to be considered when investigating cell-cell signaling. The best-understood signaling systems exhibited by the streptomycetes are those mediated by the γ-butyrolactones. In certain species, including and , the roles of the γ-butyrolactones appear to be restricted to secondary metabolism. To date, three classes of secreted, hydrophobic molecules have been shown to be involved in aerial hyphae formation. In , these include the chaplins and a small lanthionine-containing peptide, SapB, which has orthologues in , , and , as well as a functional homologue, SapT, produced by . The pamamycins, a group of macrolide antibiotics produced by , demonstrate that a single molecule may serve more than one distinct function. At subinhibitory concentrations, they stimulate the formation of aerial hyphae, while at higher concentrations they inhibit the growth of nonproducing streptomycetes and other gram-positive bacteria.

Citation: Willey J, Nodwell J. 2008. Diverse Cell-Cell Signaling Molecules Control Formation of Aerial Hyphae and Secondary Metabolism in Streptomycetes, p 91-104. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch7
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Diverse Cell-Cell Signaling Molecules Control Formation of Aerial Hyphae and Secondary Metabolism in Streptomycetes
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Citation: Willey J, Nodwell J. 2008. Diverse Cell-Cell Signaling Molecules Control Formation of Aerial Hyphae and Secondary Metabolism in Streptomycetes, p 91-104. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch7
/content/10.1128/9781555815578.ch07.ch07fig01
FIGURE 1
Two well-characterized γ-butyrolactones are A-factor of (A), which regulates antibiotic production and sporulation, and SCB-1 of (B), which regulates antibiotic production exclusively.
10.1128/9781555815578/f0093-01_thmb.gif
10.1128/9781555815578/f0093-01.gif
Image of FIGURE 1
FIGURE 1

Two well-characterized γ-butyrolactones are A-factor of (A), which regulates antibiotic production and sporulation, and SCB-1 of (B), which regulates antibiotic production exclusively.

Citation: Willey J, Nodwell J. 2008. Diverse Cell-Cell Signaling Molecules Control Formation of Aerial Hyphae and Secondary Metabolism in Streptomycetes, p 91-104. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch7
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/content/10.1128/9781555815578.ch07.ch07fig02
FIGURE 2
Three γ-butyrolactone-regulated pathways. The best-characterized pathway controls antibiotic production and sporulation in The A-factor receptor, ArpA, represses expression of the autoregulatory gene which in turn controls the expression of at least six genes implicated in antibiotic production or sporulation ( ). Of these target genes, two, ( ) and ( ), encode transcription factors that activate other developmental genes, while others encode proteins directly involved in spore maturation () ( ) or proteins involved in extracellular proteolysis () ( ). ArpA repression of is reversed by its interaction with A-factor. In a γ-butyrolactone receptor called TylP represses expression of and which control tylosin production ( ). In the SCB-1 receptor ScbR directly represses an activator of the gene cluster, and feeds into the other antibiotic biosynthetic pathways in a less-well-characterized manner ( ). Repression by TylP and ScbR is relieved when their cognate γ-butyrolactones bind ( ).
10.1128/9781555815578/f0094-01_thmb.gif
10.1128/9781555815578/f0094-01.gif
Image of FIGURE 2
FIGURE 2

Three γ-butyrolactone-regulated pathways. The best-characterized pathway controls antibiotic production and sporulation in The A-factor receptor, ArpA, represses expression of the autoregulatory gene which in turn controls the expression of at least six genes implicated in antibiotic production or sporulation ( ). Of these target genes, two, ( ) and ( ), encode transcription factors that activate other developmental genes, while others encode proteins directly involved in spore maturation () ( ) or proteins involved in extracellular proteolysis () ( ). ArpA repression of is reversed by its interaction with A-factor. In a γ-butyrolactone receptor called TylP represses expression of and which control tylosin production ( ). In the SCB-1 receptor ScbR directly represses an activator of the gene cluster, and feeds into the other antibiotic biosynthetic pathways in a less-well-characterized manner ( ). Repression by TylP and ScbR is relieved when their cognate γ-butyrolactones bind ( ).

Citation: Willey J, Nodwell J. 2008. Diverse Cell-Cell Signaling Molecules Control Formation of Aerial Hyphae and Secondary Metabolism in Streptomycetes, p 91-104. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch7
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/content/10.1128/9781555815578.ch07.ch07fig03
FIGURE 3
Structural similarities between the apo structures of (A) TetR ( ) and (B) CprB ( ). For clarity, features are only identified for one monomer in each dimer; the second monomer is shown only as a C-alpha backbone trace. An internal cavity is shown as a mesh surface representation for each protein. For TetR, this cavity shows the tetracycline-binding region as seen in several structures of TetR bound to tetracycline or its derivatives ( ). The corresponding cavity in CprB also seems likely to be a ligand-binding site. Structurally analogous helices are numbered identically in each protein; the only exception is the structurally analogous helices numbered 10 and 9 in TetR and CprB, respectively, reflecting the numbering in the original publications. To emphasize structural similarities between the two proteins, unique helices (helices 9 and 10 in CprB and TetR, respectively) are not shown.
10.1128/9781555815578/f0096-01_thmb.gif
10.1128/9781555815578/f0096-01.gif
Image of FIGURE 3
FIGURE 3

Structural similarities between the apo structures of (A) TetR ( ) and (B) CprB ( ). For clarity, features are only identified for one monomer in each dimer; the second monomer is shown only as a C-alpha backbone trace. An internal cavity is shown as a mesh surface representation for each protein. For TetR, this cavity shows the tetracycline-binding region as seen in several structures of TetR bound to tetracycline or its derivatives ( ). The corresponding cavity in CprB also seems likely to be a ligand-binding site. Structurally analogous helices are numbered identically in each protein; the only exception is the structurally analogous helices numbered 10 and 9 in TetR and CprB, respectively, reflecting the numbering in the original publications. To emphasize structural similarities between the two proteins, unique helices (helices 9 and 10 in CprB and TetR, respectively) are not shown.

Citation: Willey J, Nodwell J. 2008. Diverse Cell-Cell Signaling Molecules Control Formation of Aerial Hyphae and Secondary Metabolism in Streptomycetes, p 91-104. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch7
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