18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond

Carolyn R. Bertozzi; Michael W. Schelle

doi:10.1128/9781555815783.ch18

18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond

Authors: Carolyn R. Bertozzi¹, Michael W. Schelle²

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Affiliations: 1: Departments of Chemistry and Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, CA 94720-1460; 2: Department of Chemistry, University of California, Berkeley, Berkeley, CA 94720-1460

Content Type: Monograph

Publication Year: 2008

Book DOI: 10.1128/9781555815783

Chapter DOI: 10.1128/9781555815783.ch18

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Abstract:

Sulfated metabolites are abundant in higher eukaryotes, where they play roles in cell-to-cell communication. This chapter highlights recent advances in the understanding of sulfolipid-1 (SL-1) biosynthesis and discusses the potential biological significance of SL-1 and other sulfated metabolites in the context of both historical observations and modern experiments. Sequencing of the Mycobacterium tuberculosis genome in 1998 provided the tools necessary to draw links from gene to protein and metabolite. A signaturetag mutagenesis (STM) screen identified mmpL7 as a gene essential for M. tuberculosis growth in a mouse model of infection. Sulfate ester functionality distinguishes SL-1 from other well-characterized mycobacterial lipids. Recently, Gap, a small integral membrane protein from Mycobacterium smegmatis was shown to be required for transport of glycopeptidolipids to the cell surface. In vivo analysis of the Δpks2 mutants left the SL-1 community questioning the importance of the molecule that had previously garnered so much attention. Attenuation of the ΔmmpL8 mutant in the persistent stage of M. tuberculosis infection contrasts with the reported phenotype of the Δpks2 mutants. Although M. tuberculosis is the most extensively studied species of the mycobacterial genus, several other mycobacteria have medical importance owing to their synergism with human immunodeficiency virus. One such species is the opportunistic environmental mycobacterium Mycobacterium avium, which preferentially infects individuals with compromised immunity. This pathogen also encodes nine putative sulfotransferases, the largest number of sulfotransferases of any sequenced mycobacterial species. As one's knowledge of human immunity grows, better cellular and in vivo models for M. tuberculosis virulence will be created.

Citation: Bertozzi C, Schelle M. 2008. 18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond, p 291-303. In Daffé M, Reyrat J, Avenir G (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC. doi: 10.1128/9781555815783.ch18

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18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond

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Figure 1.

The chemical structure of sulfolipid-1 (SL-1) and trehalose. The hydroxy-bearing carbons in the trehalose ring are numbered.

10.1128/9781555815783/f0292-01_thmb.gif

10.1128/9781555815783/f0292-01.gif

Figure 1.

The chemical structure of sulfolipid-1 (SL-1) and trehalose. The hydroxy-bearing carbons in the trehalose ring are numbered.

/content/10.1128/9781555815783.ch18.ch18fig02

Figure 2.

The biosynthesis of SL1278. Trehalose is sulfated by Stf0 to form trehalose-2-sulfate (T2S), which then is acylated with a palmitoyl group by PapA2 at the 2′ position to form SL659. This product is then acylated at the 3′ position by PapA1 with a hydroxyphthioceranoyl group synthesized by Pks2 to yield SL1278.

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10.1128/9781555815783/f0294-01.gif

Figure 2.

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Figure 3.

Two possible pathways for completion of SL-1 biosynthesis. (A) Intracellular acylation of SL1278 is accomplished in the presence of MmpL8 by PapA1 and Pks2. SL-1 is then transported by MmpL8. (B) Extracellular acylation is accomplished by transport of SL1278 by MmpL8. The hydroxyphthioceranoyl moiety is also transported by an unknown protein and then coupled to SL1278 by an extracellular acyltransferase.

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10.1128/9781555815783/f0295-01.gif

Figure 3.

/content/10.1128/9781555815783.ch18.ch18fig04

Figure 4.

Genetic arrangement of the SL-1 biosynthetic cluster.

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10.1128/9781555815783/f0297-01.gif

Figure 4.

Genetic arrangement of the SL-1 biosynthetic cluster.

/content/10.1128/9781555815783.ch18.ch18fig05

Figure 5.

The chemical structure of S-GPL.

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Figure 5.

The chemical structure of S-GPL.

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Tables

18 Sulfated Metabolites from Mycobacterium tuberculosis: Sulfolipid-1 and Beyond

/content/10.1128/9781555815783.ch18.ch18tab01

Table 1.

Metabolite profiles and phenotypes of SL-1 mutants

Table 1.

Metabolite profiles and phenotypes of SL-1 mutants